Download Russell, MJ, Hall, AJ, and Mellersh, AR, 2003

Russell, M.J., Hall, A.J., and Mellersh, A.R., 2003, On the dissipation of thermal and
chemical energies on the early Earth: The onsets of hydrothermal convection,
chemiosmosis, genetically regulated metabolism and oxygenic photosynthesis, in
Ikan, R., ed., Natural and Laboratory-Simulated Thermal Geochemical Processes:
Dordrecht, Kluwer Academic Publishers, p. 325-388.
ON THE DISSIPATION OF THERMAL AND CHEMICAL ENERGIES ON THE
EARLY EARTH
The onsets of hydrothermal convection, chemiosmosis, genetically regulated metabolism
and oxygenic photosynthesis
M.J. RUSSELL
Scottish Universities Environmental Research Centre
Glasgow, G75 0QF, Scotland
A.J. HALL
Department of Archaeology
University of Glasgow, G12 8QQ, Scotland
A.R. MELLERSH
Chemistry Department
University of Derby, DE22 1GB, U.K.
"It is the inorganic elements that bring organic chemistry to life"
David Garner
1. Introduction
To this day the Earth is kept active by gravitational, radioactive and solar energies. The
convective mass transfer of heat driven by one or more of these forms of energy, from the
very core of our planet through to the upper atmosphere, eventually conduces the
interfacing of the chemical tensions appropriate to the nurturing of life. Without
convection in the Earth's mantle there would be no plate tectonics, no volcanoes, no hot
springs, no mountains — in effect, no fresh surfaces and thus no chemical potential on
Earth to drive the metabolic process. Without advection and convection in the seas and
atmosphere there would be no rain to irrigate the land. And without those spiralling
currents in the liquid iron core there would be no electromagnetic field to protect us from
lethal cosmic radiation. In particular we may say that genetically regulated metabolism and
convection are coupled on our planet and must have always been so, right back to life's
origin (Russell et al. 1988).
Just as convection is inevitable where thermal gradients are steep enough in
particular conditions, so too there is an inexorable drive, through chemiosmosis, toward
metabolism. Metabolism, the combined processes of biosynthesis of complex organic
molecules and their exergonic breakdown within a cell, results from chemical tensions on
this, and for that matter any other wet, rocky, sunlit planet in the Universe: water is
required as polar solvent and to provide hydrogen, protons, electrons and eventually
oxygen; rock to provide the trace elements and reduced molecules; sunlight to split charge.
Metabolism is a downstream corollary of hydrothermal convection and the two processes
have certain parallels. Like steady state convection, life should be recognized as an
emergent dissipative (kinetic) structure — a structure, unlike a crystal, that can bear
perturbation. Metabolism quickens, by many orders of magnitude, oxidation and reduction
reactions on our planet. Convection involves juxtaposed molecules behaving in concert as
they transfer heat to a lower temperature sink. In the metabolic case too, orderly and
commensurate flows through a membrane of electrons, protons, anions, cations as well as
uncharged small molecules, ensures that reactions will fall into step in the kind of
neighbourly co-operation that leads to the rapid dissipation of up to a volt or so of
renewable electrochemical energy.
Thus we may expect the chemical tensions responsible for the onset of life to be
quite evident and various; the components simple, obvious and readily available (Russell
and Hall 1997, 2001; Amend and Shock 2001). Availability of similar components from
more than one source, and appropriate energies derived from several mechanisms, as well
as autocatalytic feedback cycles, confers robustness to the embryonic chemical co-
operative. The way in which life was conceived should not surprise us: a hypothesis
should be economical and not resort to special pleading. More than this, it should be clear
how, given the controlling freedom conferred by genes, life was driven to evolve that it
might tap other energy sources that could contribute to metabolism from further afield and
to tolerate perturbation through the generations. In this contribution we consider the major
evolutionary jumps, from the origin of life itself up to and including the onset of oxygenic
photosynthesis, as the earliest steps are taken up the hierarchy of manageable energy
sources available to life on Earth. During this early exploration, cells enrolled pre-existing
inorganic metal clusters as active centres, became well armoured, ever more able to exploit
the more complex molecules for their operations, and, where illuminated, capable of
converting ultraviolet light to waste heat and, eventually, to use it to generate electrons and
protons from H2 S and then H2 O (Fig. 1).
The initial conditions from which life must have emerged may be gleaned from the
calculable states of the solar system and the Earth in Priscoan (~Hadean) times between
4.5 and 3.9 billion years ago (Ga). Just how the conditions for emergence might translate
to a chemical model and experimental reconstruction of key aspects are addressed. The
ultimate sources of the carbon, hydrogen and oxygen that comprise our organic molecules
was, and is, the carbon dioxide and water that comprise our 'volatisphere'. We attempt to
identify counterparts between our alkaline hydrothermal model for the origin of life with a
proposed nexus of chemical reactors containing heterogeneous catalysts, so that a
reconstruction of how life emerged might be brought about in conditions comparable to
those obtaining on young planets such as Earth or Mars (Shock 1996; Russell and Hall
1997; 1999). The emergence of oxygenic photosynthesis is a biochemical rather than a
geochemical issue. Even so, we speculate that a pre-existing inorganic CaMn4 complex
may have been sequestered by proteins to enable the oxidation of water (Russell and Hall
2001). Thus, a suggestion is made as to how a reaction centre belonging to an ancestor of
a purple or green non-sulfur bacterium might chelate such a molecule.
2. The Scale of the Problem
In order to understand how life emerged we need to assess the scales of the various
processes involved. Generally chemists and biochemists, using the 'top-down' or backtracking method, have underestimated the spatial scale, overestimated its duration, and
considered a myriad of long-chained hydrocarbons necessary as fuel and building blocks.
The 'bottom-up' approach adopted here, on the other hand, views the initial conditions as
all-important and is open to the notion of miniaturization and sophistication of the
regulated metabolic system during the rapid evolution to the first chemoautotrophic
prokaryotes (Martin and Russell 2003). For our purposes we can ignore the fact that the
Universe itself had to have evolved for hundreds of millions of years before the elements
required for the life process had condensed in isolated giant stars (Riordan and Schramm
1991). We can note in passing the dimensions of the "habitable zone", both in regard to
our galaxy and in our solar system (Gonzalez et al. 2001; Kasting et al. 1993).
Once initial conditions had been met on Earth for life to emerge, then the spatial
dimensions to hold in mind are of a few thousand cubic kilometres to encompass
hydrothermal convection, as well as advection, of ocean water. At the loci of emergence
itself we suggest that a duration of weeks or months is all that is required for an
encapsulated, regulated metabolism to ensue. More than a million hydrothermal seepages
will be conveying energy to the deep ocean at any one time. Geochemical heterogeneities
are to be expected and fluid deliveries will pulsate (Blichert-Toft and Albarède 1994). The
large spatial scale encompasses the geochemical pathways of anabolism as well as the
delivery of the photolytic electron acceptor from the ocean surface. Yet the scale of the
carbon-bearing building blocks is C1 to C3 rather than long-chained hydrocarbons. We
suggest that the energy for emergence is best understood in terms of a chemiosmotic
coupling to provide a protonmotive force through a semiconducting and semipermeable
inorganic membrane, a membrane that separates activated reagents in space (Williams
1961; Mitchell 1967; Russell et al. 1994). Origin-of-life experimentalists have yet to take
the protonmotive force and acid-base catalysis into account.
Fig. 1 The focusing of solar energy to produce a) photolytic iron oxidation and the potentiation of
chemosynthetic life (Cairns-Smith et al. 1992); b) reduction of ferredoxin and the onset of photo-induced
non-cyclic electron transport (Vermaas 2002; Blankenship 2002); c) photo-oxidation of calciummanganese bicarbonate and the generation of a precursor to the water oxidising complex (cf. ranciéite)
(Russell and Hall 2001; Dismukes et al. 2001; Sauer and Yachandra 2002); d) oxygenic photosynthesis
through reduction of Mn4IV (Blankenship 2002). Iron and manganese are exhaled from hot springs at
ocean floor spreading centres.
3. The Early Earth
An ocean had precipitated on Earth by 4.4 Ga (Wilde et al. 2001). Although it may have
been vapourized many times over by massive bolide impacts in the ensuing 500 million
years, dust clouds produced by these impacts would have effected rapid cooling of the
deep ocean, during intermissions, to less 20°C (Godderis and Veizer 2000). This cooling
would then have allowed regulated mesophilic metabolic processes to begin at around
40°C (Forterre and Philippe 1999) at a submarine seep. Once conceived in the ocean deep,
microbes could have survived further impacts as they were entrained in ocean waters
percolating to depth in the crust (Parkes et al. 1994; Summit and Baross 2001). There
were no continents (Godderis and Veizer 2000; Kamber et al. 2001) and land masses and
bodies of fresh water, if any, would have been ephemeral in this violent era.
Radioactive heat production within the Earth four billion years ago exceeded
present production more than five-fold (Turcotte 1980). Convection in the mantle
culminated in a spreading rate of ocean crust at a metre or more per year, from numerous
short active centres (Lagabrielle et al. 1997) (Fig. 2). The ocean floor also suffered
extensive submarine volcanic resurfacing. Concomitant destruction occurred over
convective down-draughts hundreds of kilometres from the spreading centres (Abbott and
Hoffman 1984). High temperature submarine hydrothermal convection cells, involving
ocean water, developed to dissipate heat from all these zones. Lower temperature springs
and seepages occurred in the somewhat restricted, quieter conditions of the deep ocean
floor. Yet although thermal energy was dissipated in this way, chemical disequilibrium was
exacerbated. The lower temperature springs and seepages in particular focused a strong
chemical disequilibrium at the ocean floor, a disequilibrium that was to be partially
resolved by the emergence of life through the self-organizing process of chemiosmotic
coupling (Russell et al. 1994). The main redox states of concern involving one or two
electron transfer in the onset of chemosynthetic life, are of iron  as Fe0 and FeII in the
crust, and FeIII from Fe2+ in the ocean, photo-oxidized at a wavelength of 350 to 400 nm,
and deposited as Fe(OH)3 on the seafloor (Braterman et al. 1983) (Fig. 1).
Fig. 2 Cross-section of mantle convection cell assumed for the Earth at 4.4 to 4.3 Ga (Smith 1981;
Macleod et al. 1994). Note the warm (50°-100°C) alkaline seepage, one of a myriad in the deep ocean at
which the hydroxide/sulfide/carbonate mounds developed (cf. Kelley et al. 2001; Bounama et al. 2001;
Marteinsson et al. 2001; Geptner et al. 2002).
4. The two classes of hydrothermal convection
The convection of ocean water in fractures transferred a quantity of heat from the fresh hot
crust, in a myriad of open system convection cells, to the intermittently cool ocean where,
ultimately, it was radiated to space. Hydrothermal convection cells, sourced from the ocean
and operating in oceanic crust, self-organize into two distinct classes as described below
(Cathles 1990).
4.1. 400°C HYDROTHERMAL CONVECTION
High enthalpy, high temperature, convection cells are fed from cool ocean water and are
driven directly by magmatic heat. Such cells would have been driven by shallow magmatic
intrusion at oceanic spreading centres and other sites of high temperature intrusion (Barrie
et al. 2001), some of them a response to meteoritic impact (Whitehead et al. 1990; Ames et
al. 1998; Price 2001). Although a portion of this water interacts with invasive magmatic
dykes at up to about 800°C, overall it is physically buffered today at the two-phase
boundary to exhale at ~400°C (Von Damm 2000). These high temperature solutions are
rendered acidic (pH ~ 3) by loss of magnesium from the circulating ocean waters
(Seyfried and Bischoff 1981):
Mg2 + + 2H2 O → Mg(OH)2
(silicate)
+ 2H+
(1)
Prior to self-stabilization at its present volume (Kasting and Holm 1992) the earliest ocean
may have been up to three times the present depth (Bounama et al. 2001). And, with heat
flow higher and the crust weaker then, the ocean ridges were probably less salient. If so
then temperatures of exhaling fluids may have been even higher as they tracked the two
phase boundary of seawater toward 800 atmospheres (Bischoff and Rosenbauer 1984),
though rapid mineral precipitation may have prevented such large temperature excursions
(Cathles 1990). Moreover, the intrusion of magma would have rendered the host rocks
plastic and therefore relatively impermeable, although volatiles emanating from the
crystallizing magma could have brecciated this envelope and escaped (Fournier 1999;
Fisher and Becker 2000). Even at 400°C fluids are able to convey up to 25 mM/l of
ferrous iron, and minor to trace quantities of other "biophile" elements such as Mn, Zn, Ni,
Co, Mo, Se and W, to the ocean (Goldschmidt 1937; Hemley et al. 1992; Von Damm
1990). They also carry hydrogen sulfide (generally ~10 mM/l), but in the Priscoan there
would have been no contribution from the thermal reduction of sulfate, so sulfide
concentrations would have been appreciably lower (Walker and Brimblecombe 1985).
Thus very little mineral precipitation would have taken place at, and in the immediate
surrounds of these very hot springs, especially as, unlike modern times, their pH and Eh
would not have contrasted greatly with that of the acidulous Priscoan ocean. This low
oceanic pH of between 5 and 6 (Macleod et al. 1994) was a consequence of the high CO2
partial pressure on the early Earth (≥1 atmosphere; Walker 1985; Kasting 1993). Thus we
can expect the early ocean to have contained ferrous iron at concentrations between 10 and
20 mM/l, tenors comparable to those in the carbonic lakes with a pH of ~5.5 in Cameroon
(Sigurdsson et al. 1987; Kling et al. 1989). Nevertheless, quenching would have led to the
widespread precipitation of iron monosulfide on the ocean floor (Walker and
Brimblecombe 1985).
4.2. 75° TO 150°C HYDROTHERMAL CONVECTION
The temperature at the base of a hydrothermal cell, reached at a depth of five kilometres or
so in areas of high heat flow but in the absence of magmatic intrusion, depends on the
chemistry and mineralogy of rocks comprising the crust. Though excursions to 200°C are
possible, aqueous fluids are normally buffered at around 75° to 150°C in solid oceanic
crust by serpentinization (hydration and oxidation) and pressure solution of minerals
composing the walls of initially permeable fracture sets which can extend to depths of
several kilometres (Fehn and Cathles 1986). While mafic and ultramafic crust is
particularly prone to hydration, carbonation and oxidation, fractures would have retained
their permeability as the crust was continually flexed by active tectonics as well as the tidal
forces exerted by the close and rapidly orbiting moon (Gaffey 1997). And as we shall see,
alkaline fluids of moderate temperature emanating from the oceanic crust are the likely site
for life's emergence (Russell et al. 1988, 1994; Shock 1992).
To understand the dynamic inter-relatednesses of the processes by which these
fluids attain their chemical make-up we must first investigate the geochemistry of iron, the
most common element with a variable valency. Iron has a negligible solubility in alkaline
solutions (Macleod et al. 1994). Instead it is responsible for the contribution of hydrogen
to these low to moderate temperature hydrothermal solutions. Iron in the ferrous state was
especially concentrated in the silicate and sulfide minerals comprising the Earth's earliest
mantle and crust, to the extent of 10 weight % (Francis et al. 1999). Moreover, vestiges of
meteoritic native iron and nickel were left in the crust as the remainder gravitated to the
Earth's core (Righter et al. 1997). We can think of this Fe0/FeII couple constituting a
hydrogen electrode as hydrothermal solutions began to oxidise the iron with the emission
of hydrogen:
Fe0 + H2O → FeO + H2 ↑
(2)
3Fe0 + 4H2O → Fe3 O4 + 4H2 ↑
(3)
and
Of more general significance is the serpentinization of pyroxene, another constituent of the
oceanic crust which has the effect of increasing pH at these temperatures to a value of 10
or more (Neal and Stanger 1984; Macleod et al. 1994):
12Ca0.25Mg1.5Fe0.25Si2 O6 + 16H2 O →
6Mg3 Si2 O5 (OH)4 + 12SiO2 + Fe3 O4 + 3Ca2 + + 6OH- + H2 ↑
(4)
But the early crust also comprised a large fraction of relatively iron-rich olivine (Francis et
al. 1999). Where carbon dioxide was introduced to this crust, hydrogen would have been
joined by methane as a reduced gas. Abrajano et al. (1990) record that methane represents
over half the gas phase emitted during the present-day serpentinization of the Zambales
ophiolite (exposed oceanic crust) in the Philippines. A notional reaction is offered in
equation 5 and geological evidence of such alteration is shown in Figure 3:
6Mg2 SiO4 + 12Fe2 SiO4 + 14H2O + CO2 →
8Fe3 O4 + 4Mg3 Si2 O5 (OH)4 + 10SiO2 + CH4 ↑ + 4H2 ↑
(5)
We therefore surmise that waters, derived from this same ocean, exothermically
serpentinized the mafic and ultramafic crust to become the alkaline, H2- and CH4-bearing
convecting fluids at temperatures peaking at about 150°C (equ. 3), much of which
ultimately seeped into the still carbonic, mildly oxidized, deep ocean (Fig. 4). In theory the
alkaline fluids are capable of dissolving large concentrations of sulfide (as HS-), if
introduced to the base of the cell (as S2-) by magma degassing (Seward and Barnes 1997;
Katsura and Nagashima 1974). Otherwise, concentrations of hydrosulfide (HS-)
generated solely by water-rock reactions can reach 10 mM/l or so (Rahman 2002).
Kelley et al. (2001) have discovered just such a warm (≤75°C) alkaline (pH ~9.8)
spring emanating from 1.5 Myr old crust in the North Atlantic, though lacking in sulfide.
The main precipitates are of CaCO3 and Mg(OH)2 . Comparable also is a fresh-water,
warm (72°C) alkaline (pH 10) submarine spring discovered off the coast of Iceland
characterised by cones of Mg-rich clay tens of metres high (Geptner et al. 2002).
As downward excavation of the ancient hydrothermal cell took place so C1
molecules previously generated in the crust (section 6.1) could be entrained at its base. For
example, gaseous magmatic emanations can be occluded in glasses and newly crystallized
rock (Kelley and Früh-Green 1999), from where they may be stripped out and entrained
when hydrothermal solutions of medium temperature gain access to the crust. Alternatively
volatiles could leak directly into the base of such hydrothermal convection cells (Gerlach
1989). Appel et al. (2001) have reported the discovery of methane in fluid inclusions
associated with what appears to be a fossil hydrothermal system at least 3.75 billion years
old in the Isua Greenstone Belt, West Greenland.
Fig. 3. Serpentinized olivine (equ. 5).
Fig. 4. Model environment for the emergence of life at a submarine alkaline ~40°C seepage on the floor
of the Priscoan ocean comprising a hydroxide/sulfide/carbonate mound (Russell and Hall 1997). The
acidulous ocean contains the electron acceptor, photolytic FeOOH, that induces chemiosmosis.
Fig. 5. Early Earth as photelectrochemical cell.
Volatiles such as formaldehyde, ammonia and cyanide also may have been present in
certain portions of the oceanic crust (section 6.1). With this chemical and physical
knowledge of the two hydrothermal fluid types as well as of the early ocean we can
investigate how they may have reacted together to produce the first living system.
5. Model for the onset of chemosynthetic life
The Priscoan Earth was a giant photoelectrochemical cell with a potential approaching one
volt, commensurate with the needs of chemosynthetic life (Fig. 5). The atmosphere
comprised ≥1 bar of CO2 (Walker 1985), with minor concentrations of HCl
(Maisonneuve 1982). The ocean was the fluid matrix to a dispersed positive electrode, γFeIIIOOH, generated by the impact of UVC on Fe2 + supplied through 400°C submarine
springs (Cairns-Smith et al. 1992) (Fig. 1):
2Fe2 + + 2H+ + hν → 2FeIII + H2 ↑
(6)
The consequential hydrogen was lost to space. Yet a hydrogen electrode was maintained at
the cooler, deep, alkaline springs through the reduction of water, a consequence of the
oxidation of ferrous silicates and nickeliferous iron during hydrothermal convection within
the crust (Fig. 4, equations 3-5). Titration of this H2 -bearing hydrothermal fluid (which
also contained CH4 , HCHO, CH3 OH, CH3 COO-, HS-, CH3 CH2 S-, NH3 , CN-, and
simple amino acids and nucleic acid bases generated in the hydrothermal mound) with the
acidulous ocean was inhibited by the precipitation of barriers of sulfides and superposed
clays, as well as the γ-FeIIIOOH and FeII2 FeIII(OH)7 which had been eddy-pumped to the
ocean floor (Fig. 1a). These "precipitate membranes" (cf. Beutner 1913), comprised
essentially of a myriad of nanocrystals of mackinawite (Fe1+xS) (Fig. 6, 7), prevented
direct neutralization. However, they did permit restricted electron and proton flow as
hydrogen was oxidized by the external FeIII, a reversal of reactions 4-6, there being no
photons to disturb normal redox potentials:
1/
2 H2
+ FeIII → H+ + Fe2+
(7)
Protons carried thus towards the outside of the barrier are partly responsible for the build
up of an inward directed proton potential, and may cause the coupled chemiosmotic
dehydration of inorganic phosphate (Baltscheffsky 1996, and see Josse 1966):
H+ + MgPO3 OH + PO3 OH2- → MgP2 O6 OH- + H2 O
(8)
These two separated reactions are linked electrically through the membrane, simplified as:
1/
2 H2
+ FeIII + 2PO3 OH2- + H+ [out] → Fe2+ + HOP2 O6 3- + H2 O + H+ [in]
(9)
Or, in Mitchell's words, "oxidoreduction (is) coupled to hydrodehydration" (Mitchell
1967), though he was referring to oxidoreduction in aerobic conditions. This (reversible)
coupling through a membrane was, in our view, the fundamental chemical process in
anaerobic oxidative phosphorylation and thus brought about the onset of metabolism. The
protonic potential drove, via the generation of pyrophosphate, organic polymerization. At
the same time a portion of H2 was activated on the iron monosulfide surface to react with
CO (later, aidedby enzymes, with CO2 ) (cf. Gunter et al. 1987; Bourcier et al. 1987):
H2 → H* + H+ + e-
(10)
Also formaldehyde and cyanide, supplied from the alkaline solution, were concentrated
Fig. 6. The mackinawite structure, FeS (from Russell et al. 1998). Note that it can contain some Ni and
Co, and minor Mg and Ca, in place of Fe (Morse and Arakaki 1993). Electrons can be transported along
the metal-rich layers in the 'a' and 'b' planes (Ferris et al. 1992). Thus mackinawite could have acted as an
electron transfer agent driving chemiosmosis, Fe(III) acting as an electron acceptor (cf. Fig. 7). It could
also have been responsible for hydrogenations, nickel acting as the catalytic site (cf. Volbeda et al., 1995).
Note too that the double layer of sulfur atoms render mackinawite an insulator along the 'c' axis, perhaps a
factor in maintaining an electrochemical gradient across the inorganic "precipitate membrane".
Fig. 7. Supposed emergence of chemiosmosis driven by the reduction of Fe(III) on the exterior of the FeS
membrane. Electrons are conducted through the mackinawite nanocrystallites of appropriate orientation
from H2 on the membrane interior. Protons track the electrons through aqueous films to conserve charge
balance. Elsewhere in the membrane mackinawite may act as an insulator (cf. lipids). The membrane
potential is augmented by protons in the acidulaous ocean — an ambient protonmotive force.
on the mineral surfaces comprising earlier chemical sediments at the seepage site (Woods
1976; Rickard et al. 2001). Concentrated thus these species polymerized to sugars and
nucleic acids which, along with amino acids generated in the same milieu, were passed
upward to the inorganic membrane, where they were prepared for phosphorylation,
interaction and polymerization. It is the inorganic barriers, constantly supplied with
hydrogen as well as with small reduced organic molecules, phosphate and trace metals that,
we suggest, formed the compartments which comprised the combinatorial chemical
reactors from which chemosynthetic life emerged (Russell et al. 1994).
Genetic control was rudimentary in these early metabolists (see sections 11 and
12), so only self-assembling clusters could be relied upon as coopted catalysts and
electron transfer agents. Chief amongst these was the "ready made" [Fe4 S4 ]2 + cubane
which either contributed to the mineral greigite (as [SNiS][Fe4 S4 ][SFeS]) (Vaughan and
Craig 1978), or, in the presence of newly generated peptides, to the electron-transfer agent,
ferredoxin ([Fe4 S4 ][SR]4 2-/3-) (Russell et al. 1994) (Fig. 8). Also the half cell of greigite
(Fe5 NiS8 ) could have acted as a primitive carbon monoxide dehydrogenase (cf. Huber and
Wächtershäuser 1997). Certainly it is rather similar to the active [Fe4 NiS5 ] centre of this
enzyme (Russell et al. 1998; Dobbeck et al. 2001). Comparable sulfide clusters,
characterised as modular, multipurpose structures by Beinert et al. (1997), fullfilled other
catalytic roles. But genetic control was required to add the necessary molybdenum atom to
the cofactor in nitrogenase required by life as it was weaned from hydrothermal ammonia.
This binding and reduction site, the (Fe7 MoS9 ) cluster, is twinned on a plane comprising
tree inorganic sulfurs, though with one known exception, with molybdenum instead of iron
in one of the apices (Davis et al. 1996). Nitrogenase also contains the 'iron-only' inorganic
sulfide cluster ([Fe3 S4 ][Fe4 S3 ]) (Peters et al. 1997). Together, these components, ligated
through six cysteines in protein, are capable of reducing water and nitrogen to ammonia.
Fig. 8. Similarity in structure of the Fe42.5+S 4 ‘cubane’ unit of the metastable thiospinel greigite,
Fe5NiS8 (a), with the Fe4S 4 ‘thiocubane’ unit in protoferredoxins and ferredoxins (b), and an iron, nickelsulfide [Fe4 NiS5 ] open cuboidal complex (c), as found in CO-dehydrogenase (from Dobbeck et al. 2001).
Having gauged how the cooption of metal sulfide clusters enabled life to emerge
and begin the process of exploration, adaptation and colonization into every niche where
comparable forces could be exploited, we now turn to the values of these forces.
6. Energy transfer and translocation gradients
6.1. PARALLEL PROCESSING
We are concerned here in representing how energy was used and processed when our
planet was young and especially energetic. Co-operative behaviour is a feature of physical
and chemical systems far from thermodynamic equilibrium — nearest neighbour
conformity and accommodation leads to the generation of dissipative or kinetic structures
(Glansdorff and Prigogine 1971; Avnir 1989). The two major dissipative structures of
concern are fracture-controlled hydrothermal convection and genetically controlled
chemosynthetic metabolism. These kinetic structures are coupled on our planet. Their
emergence is brought about and driven by thermal and electrochemical potentials
respectively. Interaction and exothermic reaction of water with hot rock transfers thermal
energy via open system hydrothermal convection to the cold sink of the ocean. We have
argued that water and volcanogenic carbon dioxide are reduced or 'electrified' at the same
time to hydrogen, carbon monoxide, methane and formaldehyde, before being returned to
the pyrophosphate-bearing carbonic ocean (Yamagata et al. 1991), an ocean which also
contains photolytic ferric iron, the first electron sink.
6.2. THERMAL GRADIENT
The onset of convection occurs inevitably when the Rayleigh number for a particular fluid
is exceeded. Convection can operate in a single phase, or by mass transfer within porous
media. Convection in the Earth's core and mantle transports heat to the surface where it in
turn engenders hydrothermal convection involving ocean-derived waters within the
permeable oceanic crust (Combarnous and Bories 1975). Buoyant acceleration of the hot
aqueous fluid takes place when the thermal gradient acting through a thickness of
permeable crust overcomes the frustrating effects of the kinematic viscosity, where the
thermal diffusion through the water-saturated medium is relatively slow. This is reflected
in Elder's (1976, p. 130) formulation of the Rayleigh equation:
R = KαgHΔT
Kmν
(11)
where R is the Rayleigh Number (empirically this dimensionless number must exceed 40
if convection is to occur in this system); K is permeability; α the coefficient of cubic
expansion; g the acceleration due to gravity; H is the thickness of the permeable layer; ΔT
the temperature contrast between the overlying free standing ocean and the base of the
hydrothermal cell, Km the thermal diffusivity of the water-saturated medium and ν the
kinematic viscosity of the fluid. Of these terms it is fracture permeability, varying between
10-13 and 10-18 m2 that is the most significant variable in the oceanic crust (Lister, 1975).
The action of horizontal deviatoric stress constantly reopens fractures which have been
narrowed by the hydration and pressure solution of minerals constituting the walls of
fractures in the crust (Miller and Nur 2000). So we have to make many assumptions
regarding the values inserted into the equation, the chief being fracture width, spacing and
connectivity. In fact the R far exceeds the critical value in areas where the geothermal
gradient is moderate to high in crystalline crust (Elder 1976). As the ocean is likely to have
cooled quickly to <20°C in intermissions between bolide impacts in the Priscoan, the
medium enthalpy hydrothermal convection cells in the crust would have operated, as now,
at about 100°C (i.e., ΔT ~100°C) (Davis et al. 1980). Occasional temperature excursions
to 250°C are possible (Fehn and Cathles 1986; Russell and Skauli 1991).
It is the very frustration caused by the interaction between the viscous fluid and the
permeable fractures that leads to cooperative behaviour between neighbouring molecules in
the aqueous fluid. Indeed, irreversible mass-transfer of heat can take place even against
local thermal gradients in, for example, the diffuse down-draught limbs of a selforganizing hydrothermal convection cell. The continual operation of a convection cell in
such circumstances is assisted by positive feedbacks, some of them non-linear. These are
consequences of, i) the cooling of the crust through the brittle-to-ductile transition zone
and the downward excavation of the cell, so that further heat is tapped, ii) the increased
height of the cell, iii) the increase in effective stress brought about by hydrostatic pressure
in newly opened pores at the base of the cell, iv) exothermic hydration and oxidation
reactions as the convecting water is 'metamorphosed' in the crust, v) the decrease in thermal
conductivity of the medium as porosity is increased, vi) the decrease of kinematic viscosity
of water with temperature (Fyfe, 1974; Lister 1975; Russell and Skauli 1991; Haack and
Zimmermann, 1996; Miller and Nur 2000). On the other hand the system is dampened
somewhat by hydration which has the effect of both weakening and expanding the rock
matrix. Thus fluid delivery to the seepage site will tend to pulsate. Yet the hydrothermal
up-draught, guided by a particularly permeable structure such as a fault intersection, is
maintained in place over many thousands of years, an example of stored information at
large scale (Russell 1973).
6.3. ELECTRIC AND PROTONIC POTENTIALS
Just as a temperature gradient leads to the onset of hydrothermal convection in a partially
permeable crust, so redox and pH contrasts across a spontaneously precipitated
semipermeable membrane will result in the onset of chemiosmosis and, thereby, of
metabolism (section 6.1). A formulation of the Nernst equation (e.g., Nernst 1923, p. 863)
can depict the measure of a potential that results from concentration (activity) contrasts of
an ion across a newly precipitated inorganic semi-permeable membrane (cf. Brünings'
"Niederschlagsmembranen", 1907; Beutner 1913):
E = RT ln C1
nF
C2
(12)
where E is the electrode potential, R is the gas constant, T is the temperature, C1 and C2 are
the respective activities of an ion in compartments either side of the membrane, n is the
number of valence electrons, and F is the Faraday constant. In the case where the ion is
H+, this equation provides the potential generated by a pH contrast across a membrane.
The Nernst equation can be reformulated (and a conversion made to base 10 logs)
to show the electric potential Δψ which is a consequence of a redox contrast either side of
a membrane (e.g., Blankenship 2002). In the case of the couples H2 /H+ and Fe3+/Fe2+
(see reaction 6) the equation is stated as:
ΔE'0 ≈ Δψ= -2.3RT log [a2 Fe2+ . a2 H+]
nF
[a2 Fe3+ . aH2 ]
(13)
where E'0 is the effective potential measured in volts at zero pH. An alternative approach is
to consider that, when the redox contrast results from specific redox couples on either side
of a membrane and operates at the molecular level, the potential generated reflects the
standard electrode potential of the half-reactions of each couple. Oxidation of H2 on one
side of the membrane and reduction, through electron transfer, of Fe3+ on the other side of
the membrane, generates a potential of 0.77 eV as follows (Fig. 5):
since,
and,
Eo (Fe3+/Fe2+)
Eo (H+/H2 )
Δψ
= 0.77 eV
= 0 eV
= 0.77 - 0 = 0.77 eV
(14)
However, this provides the maximum theoretical redox potential assuming that the ferric
ion species is the aqueous cation Fe3+. Other species such a Fe(OH)3 have lower redox
potentials, for example Fe(OH)3 /Fe(OH)2 = 0.27 eV (Garrels and Christ 1965, p. 183).
The redox reaction of concern (equ. 7) can be simply coupled chemiosmotically to
hydrodehydration (equ. 8) as shown in equation 9.
We suggest that this (reversible) coupling, through a semiconducting and
semipermeable inorganic membrane, was the fundamental chemiosmotic process driving
emergent anaerobic oxidative phosphorylation, a process which led to the onset of
metabolism (cf. Mitchell 1967). The electron donor is hydrothermal hydrogen and charge
is split such that while electrons flow outward through a series of cryptocrystalline
conductors (mackinawite, Fe1+xS) in the membrane, attracted to, and reducing, ferric iron,
an equal number of protons translocate in the same direction through an aqueous
electrolyte held in pore space in the membrane at the same time to maintain charge balance.
We can imagine these protons collecting on the outer surface of the membrane, perhaps
trapped between this and a clay exterior, before focusing to a large pore and refluxing back
down gradient through the membrane toward the alkaline interior. On their way they
dimerize inorganic phosphate (equ. 8), which in turn polymerizes simple organic
molecules (Fig. 7).
More than this, the interfacing of an acidulous ocean (pH ~5 at ≤20°C) and
alkaline hydrothermal solution (pH ~10 at ~100°C) augments this proton flow with the
potential given by equation 13 for a pH contrast:
ΔEpH= - 2.3RT ΔpH
F
(15)
We can therefore take account, both of the chemiosmotic (redox) contribution, as well as
this ambient ΔpH contribution to Mitchell's protonmotive force. In this version of the
equation Δp (protonmotive force) is the overall 'protonic' potential:
Δp = Δψ + ΔEpH
(16)
The process is simplified electrochemically and represented in Figures 9 and 10a. In
Figure 9 the coupling between redox and hydrodehydration is made graphic with pH and
water activity coordinates (cf. equ. 8). The coupling was focused across the "precipitate
membrane" as a membrane potential. We can think of the overall electrochemical potential
as lying between relatively reduced alkaline hydrothermal solution and relatively oxidized
seawater. At the same time we must keep in mind that the maximum contribution to the
electron potential due to redox contrast results from the oxidation of hydrogen molecules
on the alkaline side of the membrane coupled to the reduction of ferric iron complexes on
the acidulous outside (Figs. 7, 10).
Although metabolism is difficult to reduce to a simple energetic requirement, we
can assume that the energy to generate ATP from ADP by oxidative phosphorylation is
the minimum needed today. This is because ATP is the driving force for, amongst other
processes, the generation of peptides from amino acids. We know from the work of
Thauer et al. (1977) that for two electrons (n = 2 in equation 13) to drive the synthesis of
one mole of ATP requires a total potential of 250 millivolts (-11.5 kcal per mole). The
same transformation by substrate level phosphorylation requires less energy but is
unlikely to have been the initial process (Thauer et al. 1977). But substrate level
phosphorylation can only be visualized in the abiotic world when computational water
activities are extrapolated to unattainable values (Russell and Hall 1997) (Fig. 9).
Wood (1985) demonstrates that energy required to generate inorganic
pyrophosphate (PPi) from monophosphate (Pi) is similar and comparably effective in
driving phosphorylations and polymerizations, at least in the fermenting bacteria (and see
Baltscheffsky et al. 1966). We have already suggested (Russell et al. 1994) that directional
transport of electrons and protons drove pyrophosphate synthesis through chemiosmosis
(cf. Mitchell 1976). Inspired by the experiments of Jagendorf (1967) we have assumed
that PPi was first regenerated through a natural acid bath phosphorylation of inorganic
monophosphate, though in reverse. Even without consideration of the redox contrast, the
pH difference alone, between the hydrothermal solution and seawater, probably exceeded
four pH units. This also amounts to a natural pmf of ~250 mV, theoretically quite enough
to drive ATP synthesis in the dark (Kell 1988, Van Walvren et al. 1997). Thus 250 mV
could be considered the critical value for the onset of chemosynthetic metabolism. Of
course, to get started in an ineffient chemiosmotic system we would expect a generous
over-voltage to surmount kinetic barriers, expenditure on 'side' reactions and uneconomic
leakages through the inorganic membrane. Reference to the Pourbaix diagrams depicted in
Figures 11 and 12, diagrams which idealise the thermodynamic potentials on proton
activity (pH) and electron activity (Eh) coordinates (see Pourbaix 1949), demonstrate that
there is indeed geochemical energy enough to engender metabolism across an inorganic
"precipitate membrane" on early Earth.
Fi
g. 9. Diagram using Geochemist's Workbench (GWB, Bethke 1996) illustrates how high energy
phosphoanhydride, stable at lower pH and water activity and higher T, forms from low energy
monophosphate (2PO3 OH2- + H+ ⇔ HOP2 O6 3- + H2 O). HOP2 O6 3- can drive dehydration
polymerisations on its hydration by the reverse reaction and is analogous to the ATP4-/ADP3-/or AMP2energy cycle of life which takes place in bacterial cells at a water activity of ~0.8 and pH ~7.5. In
oxidative phosphorylation the dehydrating power of ATP is renewed by pmf (acidification) whereas in
substrate level phophorylation ATP is renewed by removal of H+ and OH- by a NAD-associated enzyme.
6.4. EMERGENCE
We have seen that it is the hydrothermal convection cell allied with solar energy which
introduces the chemical disequilibria that brings about chemosynthetic life. The chemical
potentials are essentially those resulting from the interfacing of redox and pH contrasts.
Fig. 10. Diagram illustrating the basic drive from chemosynthesis through to oxygenic photosynthesis
The critical values for the onset of hydrothermal convection and the onset of metabolism
are 40 (dimensionless) and 250 millivolts respectively. For a treatment of how
cooperativity is effected in both convection and through a membrane by non-equilibrium
states the reader is referred to Glansdorff and Prigogine (1971). We content ourselves
here with drawing attention to the structural affinities between the two self-organizing
processes, specifically between medium enthalpy hydrothermal convection and
chemiosmosis (Fig. 13a & b). We can see that earliest metabolism is a partial, though
microcosmic, reversal of hydrothermal convection. Such convection involves the hydration
and oxidation of Mg-Fe silicates whereas metabolism involves the reduction of ferric
oxhydroxides and the hydrodehydration of phosphate. The down-draw zones in
hydrothermal convection are diffuse and some of the water is split to release hydrogen. In
turn this hydrogen is activated on the inside surface of the membrane (Fig. 14), the first
stage of metabolism. The resulting electrons and protons flow through to the membrane's
outer surface, the electrons along the iron lattice in mackinawite, and by hopping from one
mackinawite crystallite to the next; the protons by rotational/translational diffusion of
water/hydronium molecules adhering to the crystallite surfaces (da Silva and Williams
Fi
g. 11. Pourbaix (Eh/pH) diagrams comparing a) electrochemical energy potentiating the onset of life and the
first microbe, to b) the electrochemical energy available to modern iron reducing bacteria (Zachara et al. 2002).
Positions of natural waters and prokaryotic bacterial cytoplasm are approximate (Russell and Hall 1997).
Although in both cases the ultimate electron acceptor is FeIII on the outside of the membrane, the proton
acceptor is within the membrane, and is inorganic phosphate in a) and ADP + inorganic phosphate in b). We
emphasize that this and subsequent Pourbaix diagrams are used to make specific points about energetics.
They do not reflect the uncertainties which result from complex speciations and changing conditions.
Fi
g. 12. An Eh-pH diagram illustrating the stabilities of siderite, mackinawite (FeS), protoferredoxin,
greigite, pyrite, green rust and hematite, produced for activities of H2S(aq) = 10-3, and Fe2+ = 10-6, using
GWB (Bethke, 1996). The diagram illustrates the redox relationships of FeS and pyrite, FeS2. The inset
shows notional phase relations emphasising the intermediate oxidation state of the FeS component of
membrane protoferredoxins and is positioned to indicate the Eh-pH conditions pertaining to alkaline
hydrothermal fluid as it enters Priscoan seawater. Also illustrated is the influence of high CO2
atmospheric pressure which leads to a decrease, but not an elimination, of the stability field of FeS in
favour of siderite. The pH boundary of monophosphate/polyphosphate is shown to intersect the redox
boundary.
1991, p. 103). The electrons are 'received' by ferric iron and the protons flow across the
outer surface of the membrane toward larger pores where they reflux toward the alkaline
interior and a monophosphate sink. The sites of proton reflux are likely to be fairly evenly
spaced across the dilating inorganic membrane (cf. McConnell et al. 1984). In the
convective process the advective path of the heated water is drawn towards a highly
permeable fracture which focuses the up-draught. Up-draughts, and thereby the seepages,
are separated today by distances of about 7 kilometres (Anderson et al. 1977). Note that in
the case of open system free convection the heat stored in the crust which initially drives
the system is augmented by exothermic hydration. Likewise, in the case of
protometabolism the proton contrast between the acidulous ocean and the alkaline interior
of the inorganic membrane is augmented by chemiosmosis. Thus both systems can 'tick
over' even in the event of one of the drives' being suspended.
7. Energy driven transformations
As we have seen, Rayleigh-Bénard convection is the inevitable outcome of heat production
within the Earth. Chemical energy too uses metabolism as a mechanism for its own
dissipation (Black 2000). Energy seeks out a means of escape — leakage precedes full
scale dissipation. Amplification of particular minor perturbations to a full scale
megafluctuation is self-evident in the case of convection. We now consider in more detail
how the geochemical energy introduced via convection finds and exploits pathways to
dissipation before it too emerges as a self-contained regulated entity.
Fig. 13. Comparison between medium enthalpy hydrothermal convection and chemiosmosis. Water is
reduced and split in convection as the crust is oxidized and hydrated to release hydrothermal H2 (b) which
itself is oxidized and split to protons and electrons in chemiosmosis (a). The protons, perhaps contained
within a 'protoperiplasm' occupying space between clay superimposed on the precipitate membrane, reflux
through the membrane and 'dehydrate' and dimerize inorganic monophosphates (Heberle et al. 1994).
7.1. THE ENVIRONMENTS OF CHEMOSYNTHESIS
Carbon dioxide was the major component of the atmosphere in the Priscoan. Although
this carbon dioxide, dissolved in the ocean, was strongly out of equilibrium with
hydrothermal hydrogen and methane, the activation barrier to their reaction is
insurmountable in these conditions. So what other destination is there for electrons in
reduced compounds introduced to the early ocean? We have pointed out (section 4.1) that
medium temperature seepage waters emanating from the Earth's deep oceanic crust, having
reacted with ferrous iron, had a redox state close to the hydrogen potential. And it was this
hydrogen that is considered to have been indispensable to the emergence of the first
metabolising system, and ultimately, to a chemolithoautotrophic microbe (Russell and Hall
1997) (Fig. 10). At the same time about 20 mM/l or so of ferrous iron was transferred to
the ocean in high temperature (≥400°C) hot springs (von Damm 1990 and pers. comm.
2000). Although up to half this iron would have been precipitated as sulfide, a proportion
of the rest would have been photo-oxidized at the ocean surface to relatively insoluble
ferric oxyhydroxide (e.g., goethite, γ-FeOOH) — natural, though dispersed components
of a potential positive electrode (Braterman et al. 1983). It should not be overlooked that
hydrogen, the reducing equivalent, escaped to space (equ. 6). As we shall see in section 17,
one of life's major coups was to contrive a mechanism to trap such hydrogen as water was
photo-oxidized within a cell.
Cairns-Smith et al. (1992) suggested that this FeIII, dispersed in the ocean, was
life's first electron acceptor. As an analogy ferricyanide is used routinely as an electron
acceptor in experiments designed to show the simultaneous generation of ATP by protons
(e.g., Winget et al. 1965; Izawa and Hind 1967). And Geobacter metallireducens, as well
as many other bacteria in the lowest branches of the evolutionary tree can reduce FeIII with
facility (Liu et al. 1997; Vargas et al. 1998; Zachara et al. 2002). Thus we may consider
the Earth as a giant photoelectric cell (Fig. 5). And chemosynthesis worked, and works
still, off a chemical potential of one quarter of a volt, generated with potential to spare, by
one of other, or combinations, of the H2 /H+ and FeIII/Fe2 + redox couples produced in this
way at pH ~10 and ~5 respectively (Figs. 10, 11).
Fig. 14. Flow diagram illustrating the geochemical drive toward the emergence of life. There are two
pathways to consider — the provision of energy and the fixation of carbon. The chemical energy that fixes
carbon from the CO (later from CO2), ultimately derived from the mantle, is provided by the oxidation of
residual native iron and ferrous iron in minerals in the hot crust, such as olivine (Mg1.8Fe0.2SiO4) to
magnetite (Fe3O4), by convecting ocean waters of moderate temperature. Just as the water was split in the
convection cell, so the hydrogen evolved in that process is split in turn in two ways. While the electrons
are conducted to oxidize FeIII (produced by photolysis of oceanic FeOH+ ) on the outside of the
electrocatalytic mackinawite boundary, activated hydrogen and protons are generated. The protons
translocate chemiosmotically to the outside of the membrane where they contribute to the protonmotive
force (cf. Mitchell 1967). Carbon is fixed from the oxides in this diagram by a precursor to the acetylCoA pathway (Ljungdahl 1994) which involves activated hydrogen and a thiol (coenzyme A, not shown)
(Martin and Russell 2003): 2CO2 + 8[H] → CH3COSCoA + 3H2O (cf. Huber and Wächtershäuser 1997).
Apart from its central role in chemiosmosis, ferric iron is likely to have been
central to at least three other protometabolic processes:
i) the maintenance of homeostasis through the oxidation of thiols (Russell et al. 1994):
2RS- + 2Fe3+ ↔ RSSR + 2Fe2+
(16)
ii) the activation of hydrothermal H2 and possibly CH4 (Ragsdale and Kumar 1996):
H2 + 2Fe3+ ↔ H+ + H* + Fe2+ + Fe3+ ↔ 2H+ + 2Fe2+
(17)
iii) the Entner-Douderoff pathway of oxidation of hexose to glycerate through ferredoxins
(cf. Pyrococcus, Daniel and Danson 1995).
7.2. HYDROTHERMAL MOUNDS AND MEMBRANES
As the alkaline medium temperature hydrothermal solutions titrate into the relatively
oxidized carbonic ocean, metastable intermediaries, principally those embodying iron,
precipitate to form mounds and chimneys (Fig. 15) (Russell 1988; Marteinsson et al.
2001; Geptner et al. 2002). Four billion years ago the bulbous structures probably
comprised alternating layers of siderite (FeCO3 ), ferrous sulfide (FeS), clays and green
rust ([FeII,Mg)2 FeIII(OH)6 ]Cl). The mound would have the effect of restricting
hydrothermal flow to a seepage. Exhalations would be further attenuated by the deposition
of a semipermeable gel consisting principally of iron monosulfide at the geochemical
interface. If bisulfide concentrations were high such a barrier might have precipitated at the
surface (Russell et al. 1988,1989) (Fig. 15a,b). If not it would have been generated, and
supported, within the somewhat porous exhalative structure developed at the redox front
(Fig. 15c).
8. Origin of organic molecules
Core formation, bolide impacts and the nuclear fission of 235U, generated heat enough to
have melted much, if not all, of the early Earth (Ballhaus and Ellis 1996; Richter et al.
1997). Intrusion and latent heat from the rapidly crystallizing magma ocean would have
kept heat flow high near the surface. At a temperature of 1600°C most, though perhaps not
all, abiotic organic molecules delivered by comets and meteorites were destroyed. Carbon
survived in small amounts in elemental form and also as carbonate, soluble at ~1 wt% CO2
in mantle-derived magmas (Gerlach 1989). Thus a new set of abiotic organic molecules
'needed' to be acquired, either by local synthesis (e.g., Shock 1990), or in contingents of
interstellar dust particles and from constituents of carbonaceous chondrites during the late
bombardment (e.g., Oró 1960; Cooper et al. 2001).
Notwithstanding the seeming attractions of an extraterrestrial delivery of organic
molecules we argue that it is not only parsimonious to invoke a self-sufficient Earthly
origin but, because life's newly assembled motor would need a supply of appropriate
energy for its building and continued operation sufficient to outweigh catabolism, the
Earth offers the only sustainable source. Moreover, what may appear as an embarrassment
of extraterrestrial riches turns out to be a 'Beilsteinian catalogue' of organic molecules
delivered in a job lot of tholins or gunk (Cairns-Smith 1982). These epigenetic molecules
have been invoked as a means to 'kick-start' life (e.g., Sephton 2001) though motive power
has remained unspecified — what forced this multitude of organic molecules to
concentrate in a turbulent 10 km deep ocean, unaddressed (Bounama et al. 2001). With a
plethora of ill-assorted unwieldy large molecules (over one hundred different amino acids
and a myriad of polyaromatic hydrocarbons and sugars) how could the first organism
have sought out the functional from the dysfunctional? Better surely to start with a few
multi-purpose, simple, good quality organic molecules — minimal elements with a protean
combinatory potential — an alphabet, not a myriad of logograms.
An atmospheric origin is equally problematic for, as Cleland (2001) has pointed
out, although "the Miller-Urey experiments ... were touted as supporting that life on Earth
began in a primordial soup, (it) really supports the auxiliary assumption that some of the
building blocks of life (amino acids) can be produced by electrical discharges on a mixture
of methane, hydrogen, ammonia, and water". The main product is caramelised gunk 
"Beilstein" again (Urey in Shapiro 1986, p. 100). And we have known for some time that
the atmosphere, dominated as it was by carbon dioxide, was neutral rather than reduced
(Kasting 1993). Only formaldehyde, generated photochemically in the atmosphere, might
have been a factor in the emergence of life. Although this molecule is destroyed by solar
radiation, a fraction may have rained into the Priscoan ocean (Pinto 1980).
It has been our contention that alkaline hydrothermal fluids of medium temperature
supplied the first fuel and building blocks for life (Russell and Hall 1997). Hydrogen is
the fuel while methane, carbon monoxide and formaldehyde constitute the main sources of
carbon, and ammonia of nitrogen, to the seepage site (equations 2-4). These relatively cool
alkaline springs contrast with the 400+°C springs resulting from the generation of new
ocean floor, whether a response to whole mantle convection (Holmes 1931), mantle
plumes (Morgan 1971), or meteoritic impact (Whitehead et al. 1990). A particular
advantage of the relatively low temperature of alkaline hydrothermal solutions is that they
Fig. 15. a) Photomicrograph of cross-section through the botryoidal FeS bubbles that grew 350 Ma at a
submarine seepage site at one of the feeders to the Tynagh base metal deposit, Ireland. The FeS bubbles
have been oxidized to, and overgrown by, later pyrite (FeS2) (from Banks 1985). b) FeS sediments and
bubble generated as 250 mM/l of Na2S (representing a particularly concentrated alkaline hydrothermal
solution) is injected into a visijar containing a 25 mM/l solution of FeCl2 (representing the acidulous
early ocean). The visijar is 4 cm wide (photograph from Martin Beinhorn). c) Sketch of a notional
sequence of chemical sediments of ferric oxyhydroxide separated from divalent mixed layer expandable
clays by a thickening semipermeable FeS membrane (cf. Beutner 1913). In this case the FeS membrane
represents a diagenetic redox and pH front, and is supported by sedimentary smectite clays, clays that can
absorb organic molecules (not to scale) (cf. Geptner et al. 2002; Kelley et al. 2001).
would have the propensity to dissolve organic acids and bases, including the nucleic acid
bases (Barnes 1997). They also favour phosphate chemistry such as the Calvin cycle.
Intermolecular hydrogen bonds may form between such organic molecules when borne to
the cool interface (40°-70°C) which separates the hydrothermal solution from the
acidulous Priscoan ocean water. How our Earth-bound hypothesis for the emergence of
life envisages the source of the simplest organic molecules is tackled in the next section.
8.1. EARTHLY SOURCES OF FEEDSTOCK
8.1.1. General purpose molecules
Simple organic molecules may be generated as magmatic gases cool in the highly reducing
conditions obtaining in the Earth's crust, and by thermal contact metamorphism, as well as
from hydrothermal fluids. To distinguish between these three, oft interrelated, crustal
sources is not a simple matter. Gaseous magmatic emanations may be occluded in glasses
and newly crystallized rock (Harris and Anderson 1983; Kelley and Früh-Green 1999),
from where they may be stripped out and entrained when hydrothermal solutions of
medium temperature gain access to the crust. Alternatively volatiles could leak directly into
the base of such hydrothermal convection cells (Gerlach 1989). We have seen that
methane may be a product of present day serpentinization (equ. 4). And Voglesonger and
coworkers (2001) have demonstrated the synthesis of methanol in laboratory conditions
(300°-350°C) simulating degassing of a CO2 -H2 -H2 O mixture during the injection of
magmatic dykes in mafic crust. Methanol yield peaked at ~6 × 10-4% with respect to
carbon dioxide in a run time of one hour. This alcohol could rise from this zone of
generation to be entrained in cooler circulating medium temperature alkaline waters.
Carbon monoxide, reduced from magmatic carbon dioxide as it percolates through the
highly reduced oceanic crust, is another source of carbon to be considered.
Yet, according to McCollom and Seewald (2001) thermodynamically favoured
reduction reactions such as that of the carbon oxides with hydrogen, do not appear to
generate carbon-carbon bonds in aqueous phase in conditions simulating the oceanic crust
and require vapour (anhydrous head space) for the generation of abiotic hydrocarbons.
Although methane dominates both the hydrothermal delivery of abiotic
hydrocarbons and the biochemical metabolism of organisms occupying the lowest
branches of the evolutionary tree which can all use FeIII as an oxidant (Vargas et al. 1998),
we are wary of assuming an 'ideal' methanotrophy to have been the first form of
metabolism because methane is difficult to activate. A more likely one-carbon compound
is formaldehyde. In an industrial synthesis formaldehyde is generated from carbon
monoxide and hydrogen at moderate temperatures in the presence of metal catalysts. We
have seen that hydration (serpentinization) of the crust generates a hydrogenation catalyst,
awaruite (Ni3 Fe) (Horita and Berndt 1999). Also residual native iron and nickel left over
from meteoritic impacts at around 4.3 Ga could act as a catalyst and, with FeII, act to drive
oxygen fugacities to very low levels (Righter et al. 1997). Thus we speculate that yields of
formaldehyde in the early crust may, in places, have been high enough to feed the first
metabolist:
CO + H2 → HCHO
(18)
Ammonia, generated at high pressure and temperature in the crust (Brandes et al. 1998),
could contribute both to the generation of amino and nucleic acids. In theory, Strecker
syntheses at ~100°C in the presence of native nickel-iron also generates millimoles/litre of
cyanide (extrapolation from Schulte and Shock 1995, fig. 7):
CO + NH3 → HCN + H2 O
(19)
Thus the potential building blocks of the sugars and the nucleic acid bases respectively are
likely to have been delivered to the base of the seepage site. Other 'ready-made' organic
components generated, and/or delivered, in the hydrothermal solution emerging from the
crust in micro to millimole/litre concentrations were dimethyl ether, formate, methylformate and hydrosulfide (Cairns-Smith 1982; Ferris 1992; Russell et al. 1994; Chen and
Bahnemann 2000; McCollom and Seewald 2001; Schoonen and Barnes 1997). Further
additions to convecting, alkaline hydrothermal fluids from the mantle made en route
included CO2 , NH3 (and thereby urea), CO, and H2 S (e.g., Naughton et al. 1974).
The consolidating pile of chemical sediment acts as a molecular sieve, adsorbing
simple organic anions as well as ammonia, formaldehyde and cyanide from the fluctuating
hydrothermal feed (Ball and Rickard 1976; Leja 1982; Rickard et al. 2001). As we have
seen, carbon monoxide and hydrosulfide were other feedstocks (Hirsch et al. 1986;
Simakov 1998; Brandes et al. 1998). Trapped, adsorbed and concentrated in this bed the
C1 molecules oligermerize in alkaline solution to C2-C7 compounds (Reid and Orgel
1967; Ferris et al. 1978; Ferris 1992; Schulte and Shock 1995; cf. Oró and Kimball 1961,
1962). For example, as a first step in these circumstances, glycolaldehyde can be slowly
generated by the dimerization of formaldehyde:
2H2 CO → HCO.CH2 OH
(20)
It can be speeded up by the addition of Pb2 + and sugars (Zubay and Mui 2001), though it
must be said that, prior to the differentiation of the continents, lead is unlikely to have been
strongly enriched in Priscoan springs or ocean. Be that as it may, glyceraldehyde is then
generated from the glycolaldehyde by reaction with formaldehyde at pH 10.5, also
catalysed by a mixed valence double layer metal hydroxide (Krishnamurthy et al. 1999a),
though glycolaldehyde itself acts as an autocatalyst (Breslow 1959). In an alternative
approach again using lead nitrate as catalyst, Zubay and Mui (2001), found the first
aldopentose to be generated in 2.8% formaldehyde solution at 75°C and a pH of 10.3 to
be ribose. HCN also oligomerizes in alkaline solution (Oró 1960; Schwartz and Goverde
1982).
The chemical sediments described above can be thought of as comprising a natural
"flat-bed reactor" (section 11) (Anderson and Jackson 1968; El-Kaissy and Homsy 1976;
Couderc 1985), fed from the "complex natural flow reactor" beneath. Mackinawite,
greigite and violarite have been proposed as significant prebiotic catalysts (Russell et al.
1994,1998; cf. Huber and Wächtershäuser 1997). And the double layer hydroxides such
as the green rust are just the prebiotic catalysts favoured by Arrhenius (1986),
Eschenmoser (1994) and Krishnamurthy et al. (1999b) (see also Kassim et al. 1982).
Promising synthetic pathways to life's components are considered in more detail below.
8.1.2. Thiols
In conditions corresponding to such an environment and at these lower hydrothermal
temperatures (100°C) Heinen and Lauwers (1996,1997) have synthesized methane thiol at
a yield of ~0.25% with respect to H2 S with excess CO2 , in the presence of FeS and native
iron. Longer chained thiols were also generated in small amounts (and see Cole et al.
1994). In theory methane thiol activities would rise to as much as 1000 when generated
from CO rather than CO2 in the crust of the early Earth (Schulte and Rogers 2002).
8.1.3 Purines and pyrimidines
Continuing with this theme, in the hot, mildly alkaline solution coursing through the
sedimentary pile, HCN would have self-condensed to diaminomaleonitrile (Sanchez et al.
1967), an intermediate in the formation of adenine (Oró and Kimball 1961), a reaction
encouraged by formaldehyde (Ferris 1992). The other biotic purine, guanine, might be
synthesizable in hydrothermal conditions, but if so it would be at much lower
concentrations (Ferris et al. 1978).
Uracil and closely comparable pyrimidines are hydrolysis products of HCN
condensate (Voet and Schwartz 1982). Although cytosine itself has been synthesized from
guanidine ([NH2 ]2 CNH), another hydrolysis product of HCN oligomers, so far it has
only been shown to do so in the presence of cyanoacetaldehyde (Ferris 1974). Such an
unsaturated compound must be considered an unlikely, though not impossible, addition to
a highly reduced hydrothermal fluid from the mafic crust. Thus the apparent lack of
cytosine especially, must be flagged as one of the weak links in our hypothesis.
Nevertheless, the fact that facile syntheses of most the biotic nucleic acid bases have not
been demonstrated (Schwartz and Bakker 1989) should still be seen as a challenge rather
than a mortal blow to the hydrothermal hypothesis. Afterall these aromatic compounds
contain conjugate bonds, and their generation at very low oxygen fugacity has not yet been
attempted in rapidly oscillating pH conditions where acid-base catalysis and mineral
surfaces might be factors. Moreover, assuming the coevolutionary hypothesis of Wong
(1975), small concentrations are all that are required for a bound RNA 'mould'. It is the
amino acids that need to be well represented in the hydrothermal seepage waters so that
they may be polymerized to the 'casts' required as proteins. This modest requirement for
the nucleic acid bases stands in strong contrast to the relatively high concentrations
assumed for the "RNA World" (Gilbert 1986; Gesteland et al. 1999).
8.1.4. Amino acids
Hennet and his coworkers (1992) have demonstrated the syntheses of the 'vital' amino
acids in hydrothermal conditions. From their work we can imagine that the requisite acids
would be generated once carbon dioxide had gained access to the mound's interior, and in
the presence of FeS or illite at 150°C. Glycine, alanine, aspartate, serine, glutamate,
isoleucine, lysine and proline are produced at 150°C in the presence of hydrothermal
hydrogen (in sharply descending order of yield) (glycine yield ~2% with respect to KCN
+ NH4 Cl + HCHO with excess 3CO2 + H2 (Hennet et al. 1992 and see Marshall 1994))
(Fig. 16). Ornithine was not analysed for though we may surmise that it would be more
concentrated than lysine. Apart from the non-chiral glycine, all the acids were racemic, a
fact to be taken into account when considering the coevolution hypothesis favoured here.
And we should note too that isoleucine and threonine are doubly chiral.
8.2. INORGANIC MOLECULES
The remaining non-metallic constituents of life, sulfur and pyrophosphate, were exsolved
during crystallization of magma and exhaled through volcanoes (Yamagata et al. 1991;
Malyshev 2001; Varekamp et al. 2001). At the same time, carbon dioxide and hydrogen
chloride were emitted, to impose a relatively low pH on the Priscoan ocean (Maisonneuve
1982; Walker 1985; Macleod et al. 1994).
Fig. 16. The conditions employed by Hennet et al. (1992) in their abiotic synthesis of racemic amino
acids are projected upon a putative hydrothermal mound. The mound could be thought of as a natural
fluidized- or flat-bed reactor with dialytic capability (cf. Fig. 27).
8.2.1. Inorganic protoenzymes
A particular example of the power of iron and nickel sulfides to act as the abiotic precursor
to CO-dehydrogenase has been demonstrated by Huber and Wächtershäuser (1997).
These authors show that, assuming a natural source of CO and methane thiol (Heinen and
Lauwers 1996), a 40% yield of activated acetic acid is generated in a narrow pH range
around 6.5. Such a pH and mineralogical environment (i.e., mackinawite, FeS, and
violarite, FeNi2 S) would have been met in the hydrothermal sulfides comprising seepage
mounds on the floor of the early ocean (Russell et al. 1998). Note that in this reaction
CO2 is not a reactant and pyrite is not a product (cf. Wächtershäuser 1988). The same
authors have generated di- and tripeptides at yields of up to 0.6 and 3% respectively in
similar conditions at pH of between 8 and 9.5 (Huber and Wächtershäuser 1998).
9. Redox, pH, pmf and homeostasis
As discussed in section 5, all extant life relies on the generation of a protonmotive force
(pmf) as the fundamental energy transduction process leading to the production of
pyrophosphate or ATP (Mitchell 1961,1979) which in some cases is now known to
involve five [4Fe-4S] clusters (Jormakka et al. 2002). It is also responsible for the inward
transport of other nutrient solutes (Chakrabarti and Deamer 1994; Russell et al. 1994). In
all cases translocation results from the generation or existence of a pH contrast. Such a
prebiotic contrast has been predicted by Russell and coworkers (1994) to be the result of
medium temperature alkaline spring waters interfacing a cool acidulous Priscoan ocean
through an iron sulfide barrier, precipitated spontaneously at the alkaline seepage (Fig.
16b). As the alkaline reduced seepage waters meet with the acidulous Priscoan carbonic
ocean, iron precipitates out as hydroxide and siderite as well as sulfide. Of particular
significance to the development of metabolism is, we presume, the spontaneous
precipitation of a film of ferrous sulfide (mackinawite, Fe1+xS) and, with the photolytic
FeIII, the mixed valence sulfide Fe5 NiS8 (greigite) (Russell et al. 1988,1994,1998) (Fig. 6,
8). As discussed in section 6.3, this sulfide barrier either formed a direct interface with the
ocean, or it was supported within a clay matrix, though with the same function. Judging
form our laboratory experiments the mackinawite may comprise rosettes. At higher pH
and/or lower activities, green rust (~[(FeII,Mg)2 FeIII(OH)6 ]Cl) also forms a primitive,
though weaker, membrane. The superiority of the sulfide membrane is owed to the
readiness of sulfur to form cross-bonds whereas hydroxyl cannot (David Stone, pers.
comm. 2001). The sulfide membrane is demonstrably semipermeable though it can hold a
pH gradient of several units for ten hours or so (Russell et al. unpublished). And in the
membrane greigite clusters would contain the kind of cubane structures found in the core
of ferredoxins which are not only an essential component of living systems, but are the
electron transfer agents with the longest pedigree, a theme to be developed in a following
section (Eck and Dayhoff 1966; Hall et al. 1971; and see Coey et al. 1973).
Apart from constraining the hydrothermal seepage waters, the membranous FeS
compartments comprising the most active components of what is a self-organising
electrochemical reactor, would have two properties effecting catalysis. Firstly, although
immediate mixing and equilibration between the external acidulous mildly oxidized fluid
with the internal reduced alkaline fluid is inhibited, localized electron, as well as proton,
flow is permitted, the first development of "chemiosmosis" (cf. Mitchell 1961,1979) (Figs.
6, 7, 10a). As discussed in section 5.4, electrons would be conducted along the iron layer
(Fe-Fe is 2.6Å), hopping from one crystallite to the next, toward the external photolytic
FeIII receptor. At the same time the protons could also invade the membrane by
rotational/translational diffusion of water molecules along the "metallic" [001]
mackinawite surfaces (Russell et al. 1994,1998; da Silva and Williams 1991) (Figs. 6, 7).
Thus redox catalysis is augmented by acid-base catalysis.
Protons are also introduced to the system in two further ways. The spontaneous
precipitation of the iron sulfide membrane at the interface between the alkaline and
acidulous fluids generates protons in the film itself as shown in equation 2 (Russell and
Hall 1997; Rickard 1989):
Fe2+ + HS- → FeS + H+
(21)
The third mechanism for generating protons would be by charge splitting as discussed in
section 5. It is envisaged to take place on the inner surface of the membrane during the
activation of a fraction of the hydrothermal hydrogen as electrons are conducted through
the mackinawite (Figs. 6, 7, 13) to the photolytic ferric iron (Russell and Hall 1999)
(equations 10 and 17). In this case the protons are expected to be generated as a
compliment to the redox gradient, an antecedent to the way the protonmotive force is
generated in living systems. The forming or reforming of pyrophosphate and disulfide
bonds by protons also maintains homeostasis.
While hydrogen emanating via alkaline springs constitutes the low potential H2 /H+
couple, the positive potential is provided by Fe2+/Fe3+, brought about by the
photooxidation of ferrous iron introduced through the 400+°C springs in concentration of
25 millimoles/litre or more, perhaps with an addition from meteoritic dust. Though some
of the iron would be precipitated, we surmize that up to 20 millimoles/litre of ferrous iron
remained in solution in the acidulous ocean. Photolysis of the iron to insoluble ferric
oxyhydroxides provided a potential terminal electron acceptor as these particles were
eddy-pumped to oceanic depths (cf. Siegel et al. 1999).
It may be that methane in the alkaline solution could also be oxidized in this way,
first exothermically to methanol, and thence exergonically to formaldehyde, notionally:
CH4 + 2FeIII + OH- → HCHO + 2Fe2+ + H++ H2
(22)
An advantage of the high pH of the medium temperature hydrothermal solution is that it
favours phosphate interactions such as the ribulose monophosphate pathway, fed with
formaldehyde, as we shall see in the next section. The alkaline seepage also contains ≤20
mM/l of magnesium (Kelley et al 2001; and see Snow and Dick 1995; Russell et al. 1999;
Laverne et al. 2001). Magnesium is an important cofactor in both the Calvin Cycle and
RNA chemistry. Also the nucleic acids, as well as organic anions with metabolic potential,
are soluble in neutral to alkaline solutions. Furthermore, phosphorylations, esterifications
and peptide bond formation are encouraged in such conditions.
Pyrophosphate, soluble in the acidulous ocean (Russell and Hall 1997), would
precipitate in the same domain as an insoluble alkaline earth/phosphate matrix on meeting
the calcium- and magnesium-bearing alkaline solutions in the membrane (Neal and
Stanger 1984). And phosphorylated products will also form a precipitate with Ca2 + and
hydrated Mg2 + . Although the mineral canaphite, a polyphosphate of calcium and sodium,
(CaNa2 P2 O7 .4H2 O), might precipitate in such conditions (Rouse et al. 1988), the
membrane-bound substrate is more likely to have been MgPPi (Josse 1966) (Fig. 7).
10. The first cycle and maximum entropy
Many researchers have assumed that the reverse tri-carboxylic acid cycle was primal
(Hartman 1974; Wächtershäuser 1988; Russell et al. 1994). Yet its high energy
requirements, the necessity of enzymatic control for the reductive cycle as a whole (Keefe
et al. 1995; Orgel 2000), as well as the need for pre-existing, stereochemically appropriate
intermediates, all go to suggest that the forward TCA cycle preceded its reversal, and that
anyway, this was not the first metabolic cycle.
The two more likely possibilities for the fixation of carbon oxides are the pentose
monophosphate cycle and the acetyl-CoA (Wood-Ljungdahl) pathway. Perhaps they
emerged in tandem. The Huber-Wächtershäuser experiment (section 8.2.1) provides
support for the prebiotic emergence of the acetyl-CoA pathway (Fig. 14). This idea is
examined in more detail elsewhere (Russell et al. 1998; Martin and Russell 2003). Here,
given the likely delivery of formaldehyde to some of the millions of submarine seepages
(section 7.1.1), we revisit the pentose phosphate cycle, a variation on the formose reaction.
Assuming the pentose phosphate cycle was one of the first essays into metabolism
the question arises — what was the abiotic precursor pathway and autocatalytic cycle? The
formose reaction has been recognised as a fertile area of investigation since its publication
by Breslow in 1959, though Cairns-Smith and Walker (1974) have urged caution given
the plethora of possible products that may be generated in this "semi-chaotic" i.e., high
entropy, system (and see Shapiro 1988; Schwartz and De Graaf 1993). But the 'principle
of maximum entropy production' holds that informed new kinetic or dissipative structures
can only differentiate during an interim non-equilibrium phase transition of instability or
semi-chaos (Trincher 1965; Eigen and Schuster 1978). Information accumulates while
there is overall maximum entropy production during the phase change. Thus what at first
sight appears a strong argument against selection from products in the formose reaction
now appears as an expectation of the 'scramble for life'. Or to borrow a phrase from
Trincher, "information content ..... emerges and is retained ..... in the nonaqueous
structures" (Trincher 1965). Thus we may expect complex aperiodic ordering on the
surface of crystallites in the "precipitate membrane" to facilitate a surface chemistry with
the inherent advantages of stereoselection.
Prior to the emergence of life the fastest way to spend chemical energy at the
exhalative site was in individual saturation-supersaturation-nucleation-settling limit cycles
involving iron carbonate, sulfide and oxide precipitation as temperature, pH and Eh also
varied aperiodically (Fig. 12). Positive and negative feedbacks thus generated superdeposition cycles of contrasting mineral precipitates (cf. Lydon 1983; Letnikov 1997).
Emerging in these conditions, cellular life encapsulated feedback cycles. The first essay
into anabolism might have been the exploitation of the formose reaction.
10.1. THE PENTOSE PHOSPHATE CYCLE
Puzzling over the origin of autotrophy, Quayle and Ferenci (1978) considered a likely
template for the first carbon fixation cycle be found in the exergonic biosynthetic
sequences that started from formaldehyde, in particular, the ribulose monophosphate cycle
of formaldehyde fixation. In this vein, Ström, Ferenci and Quayle (1974) had
demonstrated how carbon is assimilated through the ribulose monophosphate cycle of
formaldehyde fixation (RuMP cycle). This is similar to the Calvin Cycle where
GAP + DHAP ↔ F(fructose)1,6PP → F6P + Pi
F6P + GAP → Rib-5-P + Erythrose-4P
(23)
(24)
Erythrose-4P + DHAP → Sedheptulose-1,7PP →
Sedheptulose-7P + Pi
Sedheptulose-7P + PGA → 2Ribulose-5P
(25)
(26)
The Calvin Cycle is catalysed by alkaline conditions and magnesium, both attributes of the
"Lost City" environment.
Mindful of the cautions of Orgel (2000) we speculate here on the potential of this
cycle to provide a cognitive map that might be used to prompt the imagination and to
provide routes for consideration and testing in the laboratory. Initial phosphorylations
could have been effected with amidotriphosphate (AmTP) in the presence of MgCl2 at
neutral pH and room temperature for, as we shall see below, Krishnamurthy et al. (1999a)
have successfully phosphorylated glyceraldehyde in this way. Amidotriphosphate itself
could have been synthesized for this reaction in the green rust film developing in the
neutral conditions at the interface between ammonia-bearing hydrothermal solution and
polyphosphate-bearing ocean (Yamagata et al. 1991; cf. Krishnamurthy et al. 1999a;
Quayle and Ferenci 1978, figure 3). Yamagata et al. (1995) have generated AMP in 10%
yield from adenosine and trimetaphosphate in aqueous solution.
Phosphate is the ideal leaving group for biological systems (Westheimer 1987)
and the charge on the phosphate retains the molecules in the environment. Moreover, the
inorganic membrane matrix we envisage would have been selective. Only alcohols would
be phosphorylated by the polyphosphate produced continually at the proton gradient.
Molecules with more than one functional group can also interact with each other to form
products that are biphosphates. Doubly bound, these will remain in the matrix for even
longer. Thus there is an evolving surface chemistry in and on the membrane. The effect of
all this is to select those molecules which can perform chemistry in this matrix, generating
products that are retained. Uncooperative and low energy molecules will simply remain in
the seepage waters and pass into the ocean.
Once the Cycle is established the tautomer of phosphoglyceraldehyde (PGA),
dihydroxyacetone phosphate (DHAP), will be generated in this environment (Weber
1992). Both GA2P (Müller et al. 1990) and, we speculate, GA3P would be present and
precipitated by calcium hydroxide from the alkaline hydrothermal solution (cf. Mizuno
and Weiss 1974) perhaps to produce 'poisoned' surfaces (e.g., 100 and 010) to a
mackinawite already dosed with Ca/Mg, developing in the 'a' and 'b' crystallographic
coordinates favoured for growth (cf. Pitsch et al. 1995; and see Morse and Arakaki 1993).
But the distance between any two phosphates would only favour reaction between GA3P
and DHAP. Phosphoglyceraldehyde is chiral. Each enantiomer will have an energy
minimum when the oxygen atoms of the aldehyde and hydroxyl, as well as the hydroxyl
and phosphate, are in anti-conformation. Then the aldehyde of the GA3P will attack the
DHAP to form fructose. Dextro-GA3P will yield D-fructose-6-phosphate and LevoGA3P will yield L-fructose-6-phosphate. Once fructose-6-phosphate (FMP) has been
formed, the stereochemistry is fixed for erythrose-4-phosphate and sedoheptulosephosphate formation. The cycle reconverges to ribulose-5-phosphate (RuMP). Under the
high partial pressure of carbon dioxide, and in the presence of activated hydrogen, much of
the ribulose monophosphate could assimilate it as HCO3 - and convert to 6phosphogluconate:
CH2 OH.CO.HCOH.HCOH.CH2 OPO3 2- + H* + CO2 →
COOH.HCOH.HOCH.HCOH.HCOH.CH2 OPO3 2-
(27)
Thus primed, the Cycle will continue to require a source of phosphorylation and reducing
power to generate GA3P. From that point the cycle is energetically neutral or downhill
until carbon dioxide is used to generate the triose again. Thus it is autocatalytic and it will
start to consume the huge reservoir of carbon dioxide in the atmosphere which itself is
continually supplied by volcanoes. If polyphosphate is available, the 6-phosphogluconate
decomposes to 1PGA and 1DHAP and the cycle would be unstoppable:
COOH.HCOH.HOCH.HCOH.HCOH.CH2 OPO3 2- + HP2O73- →
2HCO.HCOH.CH2 OPO3 2- + H2PO4-
(28)
But some of the ribulose-5-phosphate will isomerize to ribose-5-phosphate
(CHO.HCOH.HCOH.HCOH.CH2 OPO3 2-) which marks the stable end product of the
Calvin Cycle. This will then be retained in the system as an insoluble complex with Ca2 +
or other divalent cation. Thus thermal forces will repeat the 3'OH to a nearby phosphate
group and, since this is happening in an alkaline environment, it is reasonable to assume
that the 3'OH will be phosphorylated.
Each phosphate can accept a 5'OH and a 3'OH. Chains of polyribose phosphate
would be built up on the surface of mackinawite (Fig. 18), particularly in the presence of
acetate which has the effect of dehydrating the surface by the removal of the electrical
double layer (cf. Tessis et al. 1999; Pontes-Buarques et al. 2001). If a chain happened to
start with D-ribose, then stereochemistry would favour it continuing with a D-ribose as an
L-ribose would be sterically hindered — its 3'OH being on the wrong side for an attack on
the phosphate which is held by the attached ribose. As the 2'OH is sterically hindered by
the surface it cannot be phosphorylated. On the other hand the 1'OH is projected away
from the surface and may thus be activated by polyphosphate. We rejoin this discussion in
the next section.
10.2. CATABOLISM
While the generation of ribulose-5-phosphate marks the anabolic stage of metabolism in
the pentose phosphate cycle, the reappearance of phosphoglyceraldehyde and
dihydroxyacetone phosphate in the cycle is the result of catabolism. Of the two
enantiomers, dihydroxyacetone is structurally comparable to the active molecule pyruvate,
an intermediate in so much biochemistry. Pyruvate itself may have been first derived from
the oxidation of glucose with ferric iron acting as the final electron acceptor. Glucose is
another product of the formose reaction and pyruvate may have been produced via 2-keto3-deoxygluconate and glycerate, in what may have been a precursor to the EntnerDouderoff pathway. Protoferredoxins could have acted as the coenzymes in this cycle
prior to the evolutionary appearance of NADP+ (Daniel and Danson 1995) (section 12).
The protoferredoxins could have been recharged through a hydrogenase with the
production of dihydrogen (cf. Makund and Adams 1991).
10.3. FORMATION OF NUCLEOTIDES
We have seen how, for example, the 1'OH of D-ribose projects away from a surface and
could be activated by polyphosphate. How then could the base be presented to the to the
1'OH? Sowerby and Heckl (1998) have shown that bases spontaneously organize and
concentrate on sulfide surfaces from dilute solutions in arrays which place N7/N1 at
similar distances to the O1'. If such a surface covered in bases were opposed to a surface
covered with activated polyribose phosphate, as for example in the inorganic membrane,
then base addition could occur. The product, when all O1' had undergone base addition,
would be RNA. RNA has one negative charge per residue and is soluble in alkaline
solutions. It might be liberated from the surface of the crystallite in the exhalative
sedimentary pile and migrate toward the seepage. Once at the point of neutralisation of
charge, at around pH 6, met in the membranous barrier separating the alkaline
hydrothermal solution from the acidulous ocean, it would reprecipitate. How do these
assumptions sit with abiotic experimental syntheses?
Krishnamurthy and his coworkers (1999b) have induced the generation of ribose2,4-biphosphate at a yield of ~10% from glycolaldehyde phosphate and glyceraldehyde-2phosphate, optimal at 40°C, on mangalite (~[Mn2 Al(OH-)6 ]Cl), a mixed valence double
layer metal hydroxide. Mangalite and comparable hydroxides such as green rust, are the
kind of minerals that would comprise the chemical precipitates, the notional flat-bed
reactor, immediately beneath the submarine seepage site. Using another mineral to be
expected
in
this
environment,
the
"swelling"
clay
montmorillonite
(~[Na0.7][Al3.3Mg0.7]Si8 O2 0][OH]4.nH2O), Ferris and Ertem (1993) have condensed
the 5'-phosphorimidazole of adenosine which led to the preferential formation of 3',5'polyadenosine. We have argued (section 8) that a particular enantiomer of the 5'phosphorylated product might be favoured where the primers register to the high energy
[100] or [010] faces of mackinawite.
11. Genetic code
As we argue here that metabolism and the genetic code emerged in tandem  that a simple
code was an aspect of the first metabolism  we deconstruct the overall process to
consider the mechanism by which the code was erected and imparted. We then outline a
hypothesis which intimates how the iron-dominated mackinawite crystallites comprising
the first membrane could have acted as stereochemical templates to a linear array of ten or
so nucleic acids. Given that three nucleic acid triplets may have happened to act as
templates for two or three amino acids, these amino acids would have polymerized on an
'outer surface' before peeling off to take part in combinatorial chemosynthesis influenced
Fig. 17. The genetic code could have originated from the conformation of RNA attached to mackinawite.
Here three types of clefts are envisaged. In the first two types the bases are free to move around forming
different environments, each preferring a different amino acid. In the last cleft, inter-base interactions fix
bases so that no amino acid can enter, thus terminating the chain (Mellersh 1993).
Fig. 18. Sketch to show how the present mechanism for amino acid coding, polymerisation and release by
acid-base catalysis (Muth et al. 2000) might have originated in the "dry" mackinawitic membrane which
separated an acidulous ocean from warm alkaline seepage water. Note that N3' acts as the binding site for
the amino group on the purines whereas O2' fulfils the same role for the pyrimidines (Mellersh 1993).
by rapidly oscillating pH and redox fronts (Fig. 18). Thus we can consider genetic
regulation to have emerged as an unstable outer zone of amino acids was repeatedly
spalled from a mackinawite nanocrystal penultimately surfaced with the organophosphate,
RNA, as pH oscillated to low values.
In detail, the phosphate of ribose-phosphate nucleotides is likely to have
polymerized in the presence of protons as the nucleotides registered stereospecifically, in
the presence of acetate (Tessis et al. 1999), to surfaces of the mackinawites comprising the
membrane. We note that, to date, only purine nucleotides have been shown to oligomerize
onto a complementary template (Inoue and Orgel 1983) (Fig. 19). Mackinawite, like other
layered minerals, grows preferentially in the planes of the a and b crystallographic axes at
high energy faces such as [100], [110] and [010]. Because each crystallographic unit cell
is 5Å thick (Fig. 6), nucleotides are likely to have developed in linear arrays with the
phosphates bonded to sulfur in the sulfide layers (Pattrick, unpublished EXAFS). Thus
mackinawite faces such as [100], [010] or those between, acted as the stabilizing frame for
particles of RNA.
Stacking interactions of the bases effectively offered a variety of stable triplets,
arrayed as clefts, to the side chains of the simple amino acids (Mellersh 1993) (Fig. 17)
generated in chemical precipitates just beneath the surface of the hydrothermal mounds.
The evolutionary late-comer arginine offers the best example so far, experimented with,
and treated statistically, because of its significance in HIV research (Yarus 1988,1989;
Connell et al. 1993; Knight and Landweber 1998). Tyrosine also appears to have affinity
for its own triplet sites in RNA (Yarus 2000). Although we might expect 'proactive' amino
acids to be electrostatically attracted to that part of the genetic code table (Fig. 17) where
the purines comprise the middle bases, the fact that the 'hydrophobic' isoleucine also binds
to RNAs containing isoleucine codons, where the middle base is a pyrimidine, adds more
weight to this idea (Majerfeld and Yarus 1998).
Of course RNAs, whether messenger, transfer or ribosomal, are the result of
evolutionary complexification and their association, if any, with mineral surfaces is long
lost. Nevertheless, it is surprising that proteins do not feature in the decoding and active
'catalytic' centres of both subunits in ribosomal RNA: proteins merely provide the
superstructure (Ban et al. 2000; Nissen et al. 2000; Wimberley et al. 2000; Carter et al.
2000). Could it be that a mineral scaffold to a direct RNA processor of peptides was the
deep precursor to this structure (Mellersh 1993)?
Fi
g. 19. Table of the "universal" genetic code. Concentrations indicate amino acids that have been obtained
in "prebiotic" syntheses (Hennet et al. 1992; and see Marshall 1994) and are therefore assumed to be the
commonest on the early Earth. Ornithine, not analysed for in Hennet et al. (1992), has been tentatively
assigned to arginine codons as it is presumable more easily synthesized than lysine. The four starred
amino acids have been shown to attach to RNA strands which contain their codons.
A first step to addressing this idea is the demonstration that polyadenylic acid
bound to silica gel by drying, stereoselectively binds L-lysine from dilute aqueous solution
of L-amino acids (Mellersh and Wilkinson 2000). About half the amount of L-arginine
and L-ornithine also was found to bind with Poly A. Condensation to lysinamide was
effected by immersion in a reduced polar organic environment prior to the addition of
liquid ammonia (Mellersh and Wilkinson 2000). Polyguanylic acid immobilised on silica
gel in the same way did not bind to any of the amino acids in the pool. That glycine failed
to bind to its codon in these experiments was probably because of its low concentration
relative to likely values in the prebiotic conditions we have envisaged here. An added factor
is the lack of a side chain on glycine to interact with the third (auxiliary) base.
Stoichiometric calculation suggested that a maximum of eight-mer of polyadenylic acid
was associated with each lysine molecule. Whether the number was three (i.e., lysine's
codon, AAA) could not be gauged. Nevertheless, the clefts proposed by Mellersh (1993)
have just the right spacing and polarities to affiliate components of an alpha chain. N3' on
adenine, rendered unusually basic by its environment, could have accepted a proton
donated by the nucleophilic amino group of an amino acid when the pH oscillated to a low
value, thus acting as an acid-base catalyst (Mellersh 1993; and see Muth 2000). N3' on
guanine or O2' of pyrimidines would occupy the same space as N3' of adenine in the cleft
model and have a similar charge and function. The lone pair on the amino group now
attacks the electrophilic carbon of the carboxyl group of the amino acid in the adjacent
cleft, the carboxyl group already having protonated the 3'-O of the ribose (Fig. 18). The
carboxylate of a neighbouring amino acid can have electrons withdrawn by the 2'OH on
the third base (Mellersh 1993). This produces a delta-negative charge on the carbon. At
the same time the -NH3 + of the amine group of the amino acid in the next cleft donates a
proton to the phosphate between the two clefts, freeing up a valency on that phosphate.
The carboxylate of the first amino group can now form an anhydride with the phosphate
and a pseudorotation delivers it under the -NH2 of the second amino acid. The lone pair of
the NH2 can attack the carbon of the anhydride to form a peptide bond (Fig. 18). Since
there is now no charge relationship with the first base, the dipeptide can repeat the process
with the phosphate between the second and third clefts if it should happen to harbour
another amino acid. Again the lone pair on the amino group attacks the electrophilic
carbon of the carboxyl group of the amino acid in the adjacent cleft. But chain
terminations will generally occur after two or three polymerizations, when the process
comes across a cleft which does not contain an abiotic amino acid _ one of several
effective stop (non-sense) codon clefts (Fig. 17)  or because the mineral surface cannot
accommodate the tendency of RNA to coil beyond about 10-mer.
Fitful inflation of FeS bubbles with alkaline hydrothermal fluid, or pulsating
delivery of alkaline solution to an FeS layer would have caused rapid alternations of pH.
Periodically lower values within the iron sulfide membrane are to be expected because its
exterior interfaced the acidulous ocean. The effect of this 'proton shuttling' was to
polymerise the contiguous amino acids. Thereby, freed of their hydrogen bonds to the
nucleic acids, di- or tri-protopeptides could, depending on their sequence, react with other
molecules in this milieu as outlined below. Meanwhile the remaining nucleic acid mould
either attracted a new influx of similar amino acids to repeat the process, or as nucleic acid
concentrations built up, the antisense RNA particle could be generated, the duplex
unzipped by protons, and the information-bearing molecule transported elsewhere in the
membrane to act as a codon in its own right.
12. Synthesis of peptides and protoferredoxin
As we have seen, because only about ten of the amino acids were available for coding
before the onset of life, then perhaps a quarter of the present codons would have effected
termination (Fig. 19). Many of these are contiguous with the present stop or non-sense
codons, and are situated in that part of the table where pyrimidines are the first base and
the double ringed purines take up significant space as the middle base. Thus the average
length of the active proto-RNA 'reading frame' would have comprised three or so active
Fig. 20. Eck and Dayhoff (1966) suggested this evolutionary sequence of amino acid sequences for the
origin of ferredoxins. Independently Trifonov et al. (2001) came to similar conclusions for the first
complementary coding triplets (GGC and GCC) and their expansion by point mutation.
codons, short enough to allow coding and peptide bonding without deleterious distortion.
Thus protopeptides would have been only about three residues long. What would have
been the favoured sequences of the amino acids in these short protopeptides and how
would they have been incorporated into emerging life?
Eck and Dayhoff (1966) suggested that a deep ancestral protein was derived from
a repeated sequence which coded for alanine (GCN), aspartate (GAPy), serine (UCN) and
glycine (GGN). (These happen to be the most abundant of the abiotic amino acids
(Hennet et al. 1991)). Cysteine, valine, proline and glutamine were then incorporated to
generate a polypeptide which, on doubling, sequestered [Fe4S4]2+ to produce the first
ferredoxin (Fig. 20). Further doubling led to ferredoxins containing between two and
twelve [Fe4S4]2+/+ clusters (Steigerwald et al. 1990) (Fig. 21). The ferredoxins and related
iron-sulfur proteins served not only as electron transfer agents, hydrogenation enzymes
and redox catalysts, hydrogenases, dehydrogenases, nitrogenases, hydrolases,
endonuclease III, in cytochromes, as redox sensors (Allen 1993; Johnson 1996), but also
as structural components and stabilizers, particularly of protein dimers (Beinert et al.
1997). Thus they were well suited to take over control of electron and proton transport
from the iron sulfide films. Of the amino acids required in Eck and Dayhoff's scheme
only glutamine is unrepresented amongst the simple abiotic amino acids. Cysteine has
been detected in trace amounts (Hennet et al. 1992), though because of strong bonding to
sulfide catalysts, concentrations may have been underestimated.
While the suggestions of Eck and Dayhoff (1966) give us an early evolutionary
'target', one that is in concert with the analyses of Trifonov (2000), such an organizational
jump, without intermediate stages, is unimaginable. Instead we suggest here a
protoferredoxin in which the ligands consist of perhaps two amino acid trimers. Following
Trifonov's (2000) views of the nature of the first codons we suggest the first 'useful'
peptides were coded by (GGC)3 /(GCC)3 to give (gly)3 and (ala)3 . Though both of these
might have been able to sequester [Fe4 S4 ] clusters, a point mutation to favour an aspartate
moiety may have been more effective. The latter trimers could have sequestered
Fig. 21. [Fe4 S 4 ] centres as ferredoxin-like domains in a hyperthermophilic Archaeon, Methanothermus
farvidus. This polyferredoxin allows two electron transfer across the membrane (Steigerwald et al. 1990)
Fig. 22. Example of how a 'preformed' inorganic cubane [Fe4S 4] structure may have been chelated with
(gly2asp) and (ala)3 coded by (GGC)2AGC/(GCC)2GCU (cf. Bonomi et al. 1985; Trifonov 2000).
protoferredoxins as shown in Figure 22. Alternatively, were cysteine to have been available
(or mercaptopropanoic acid), then ligands such as ser2 cys/ala3 (coded by
[AGC]2 UGC/GCA[GCU]2 , or asp2 cys/ala,val2 (coded by [GAC]2 UGC/GCA[GUC]2 )
would have been possible. A precursor to CO-dehydrogenase could have been generated
in a similar way (cf. Fig. 8). Such peptides will precipitate near the RNA particles that
produced them, either because of inherent insolubility of the polyamides, or because they
contain serine which can be phosphorylated and precipitated with Ca2 + . One other role for
early peptides comprising the common abiotic amino acids has been emphasised by
Baltscheffsky and her coworkers (1999). They show that the active site motifs of enzymes
that generate pyrophosphate, the likely first central energy carrier, can consist exclusively
of glycine, alanine, aspartate and valine.
13. Organic takeover of membrane
An organic take-over of the iron sulfide/hydroxide membranes must have taken place at an
early stage of evolution but the nature of the first organic membrane is particularly
puzzling. Although lipids, as self-assembling membrane fillers and hydrophobic hosts,
might have been supplied from the hydrothermal system (McCollom et al. 1999; Holm
and Charlou 2001, and see Freund et al. 2001), they are produced in low yield, and
anyway, do not figure in Wächtershäuser's (1998) "canonical" gene cluster which bears
no trace of lipid chemistry. Wächtershäuser tentatively suggests that the presence of
proteins belonging to the secretory pathway in a gene cluster, conserved across 13
eubacteria and 6 archaebacteria, might indicate their role in building proteinaceous cell
envelopes for organisms preceding the last universal common ancestor (LUCA).
Genetically controlled proteinaceous cell envelopes comprised substantially of
hydrophobic polyalanine (section 12) would have the advantage of including metal
clusters, such as the [Fe4S4] centres, within their structure as stabilizers and electron
transfer agents (section 12 and Fig. 23). Indeed a polyferredoxin in the Methanothermus
farvidus (Steigerwald et al. 1990) allows two electron transfer from inside to the outside
of its membrane (Fig. 21). Excess thiols also could have been 'entropy driven' into this, the
first organic membrane. And non-coded peptides demonstrated to be generatable in
hydrothermal conditions by Huber and Wächtershäuser (1998) and Ferris et al. (1996)
also could have played an important role.
Fig. 23. Cartoon to illustrate how membranous FeS bubbles may have acted as (photo)electrochemical
reactors or chemiosmotic chambers for the synthesis of the next generation of membrane components,
possibly of phosphorylated proteins (cf. Wächtershäuser 1998). Distension is initially driven by hydraulic
pressure at the seepages. Osmotic pressure takes over as organic ions are generated. Individuation follows
the development of nucleic acid code for proteins. [Fe4 S 4 ] centres act as cross-links between, and so
stabilize, the peptides comprising the first organic membrane. They also act as ferredoxin-like domains.
14. Major evolutionary steps
The early organisms that emerged from the warm seepages would have had alternative
stereochemistries. Genetic mutations, gene swapping, doubling and rearrangements, gave
these first microbes the freedom to evolve rapidly and exploit other environments where
metabolism could be readily potentiated. In doing so new metabolic cycles could be
invented. At first, when supply of energy and material was in excess then organisms of
both chiralities would have flourished. The vanishingly small energetic inequivalence of
<10-14, or, more likely, <10-17 (MacDermott et al. 1992), between molecules such as DNA
would have been 'lost in the noise' at the energies available at the hydrothermal seepage
sites from which life emerged. But once microbes had expanded into all the easily
exploited niches, the competitive struggle for existence began in earnest. On our planet
organisms comprising D-amino acids and L-sugars lost this, the first world war. But such
a steric asymmetry is likely to obtain on other sunlit, wet rocky planets. Early incremental
vertical and horizontal evolutionary changes are areas of concern to the evolutionary
microbiologist. We concentrate here on those major early evolutionary jumps which may
have been driven by significant changes in the geochemical environment and/or been
facilitated by the sequestering of naturally occurring metal clusters by organisms —
clusters that otherwise would be incarcerated in minerals comprising submarine chemical
sediments.
Whatever the particular evolutionary paths followed or crossed, we know that
evolution itself is fundamentally and structurally conservative. Even the most
'revolutionary' of organisms are necessarily built on the foundations of their predecessors
(Jacob 1977). Major evolutionary jumps which allow a higher overall metabolic turnover
require an additional capability conferred by the acquisition of 'foreign' genes and/or the
capture of the kind of "ready-made" metal-bearing cluster mentioned above.
Given the likely nature of early geochemical environments, the evolutionary
metabolic tree is considered to have grown in the following sequence:
i) anaerobic chemolithotrophy a  microbes which use Earth's inorganic geochemicals,
mainly H2 , NH3 , CH4 , CH3 OH, HCHO and CH3 OOH as energy/electron, nitrogen and
carbon sources with ferric iron as the electron acceptor (ab intra; Russell and Hall 1997).
ii) anaerobic chemoorganotrophy (heterotrophy)  microbes that use the waste and
detritus of chemolithotrophs as energy and carbon sources (includes the fermenting
bacteria) and sulfate, nitrate and/or ferric iron as electron acceptors.
iii) anaerobic chemolithotrophy b  bacteria using CO as the sole source of carbon, H2 ,
H2 S, NH3 as energy and SO4 2-, NO3- and/or FeIII as electron acceptors (Pace 1997).
iv) anaerobic chemolithotrophy c  bacteria which use carbon dioxide as the sole source
of carbon, are able to assimilate nitrogen, use H2 , H2 S and/or Fe2+ for energy, and FeIII,
MnIV, S0 , NO3 -, CO2 and SO4 2- as electron acceptors (McFadden and Shively 1991;
Canfield et al. 2000),
v) anoxygenic photolithotrophs  bacteria using photons and Fe2 + and HS- as electron
sources and assimilating N2 and CO2 (Baymann et al. 2001),
vi) oxygenic phototrophy  cyanobacteria using photons, H2 0 and CO2 (Dismukes et al
(2001),
vii) aerobic chemolithotrophy  using CH4 , CH3 OH, HCHO and CH3 OOH as carbon
sources, Fe2+ and other reduced ions and complexes as electron sources and O2 as
electron acceptor,
viii) aerobic chemoorganotrophy (heterotrophy)  eukaryotic metabolism
We limit this contribution to the consideration of steps i, v and vi. Steps vii-viii are
considered in Martin and Russell (2003). Energetically we can note that in the generation
of a protonmotive force, inverse "acid bath" (cf. dark phase) phosphorylation preceded
photosynthesis (see Jagendorf 1967) (Fig. 9, 12).
15. Evolution to photosynthesis
On present knowledge it is not possible to discern whether photosynthesis evolved early
as an aspect of a random, though controlled, exploration of energetic potentials, or whether
it was forced by environmental change. Cockell and Knowland (1999) argue that it was an
opportunistic co-option of photons derived from protection proteins involving aromatic
conjugated bond structures. It is clear that a defence against high energy UV photos was a
prerequisite for photosynthesis (Mulkidjanian and Junge 1997). For such an adaptation
'time could be bought' in two ways. Firstly, where microbiolites develop in shallow water
moribund cells form an effective shield (Margulis et al. 1976). Secondly mineral
deposition could have played a role. For example, Rambler and Margulis (1980) have
demonstrated that some salts can strongly absorb UV. Moreover, direct bioprecipitation of
minerals mitigates the harmful effects of far UV (Phoenix et al. 2001).
The second idea, that an evolutionary jump from chemosynthesis to
photosynthesis was forced by changes in the environment, stems from a consideration of
the lowering of CO2 partial pressure with time. Although biotic methanogenesis probably
accounts for much of this change, a loss of a portion of atmospheric CO2 to the oceanic
crust is also likely, a consequence of hydrothermal alteration in the earliest Archaean as the
mantle cools (Alt and Teagle 1999). As sea-level dropped, the input of bases (Mg+ +>
Ca+ +> Na+ > K+ > Fe+ +>> NH4+ ) from protocontinents and submarine springs would
Fig. 24. a) Possible progress in mean Eh/pH of ocean water through time computed using GWB for:
activities of Fe2+ = 10-6 and SO42- = 10-10; fugacity of CO2 = 10-3.5 (present atmosphere); and hematite,
Fe2O3, suppressed to show goethite, FeOOH, which is taken to control Fe-solubility in near surface
environments. Fields of magnetite, Fe3O4 and siderite, FeCO3 shown. Pyrite, FeS2 is thermodynamically
stable but 'FeS' phases are favoured kinetically. Positions of natural waters and prokaryotic bacterial
cytoplasm are approximate. The redox plot is approximate as there are kinetic barriers between couples.
From 4.4 to 4.1 Ga there is an increase in pH resulting from ocean floor rock/water equilibration. Loss of
natural pmf encourages the evolution of anoxygenic photosynthesis. From 4 Ga the impact of oxygenic
photosynthesis led to oxidative weathering, gradual pH drop and the deposition of Banded Iron Formation.
b) Mn and Fe plots of species and phases in similar conditions. Activities of Mn2+ and Fe2+ = 10-6;
fugacity of CO2 = 1 (~3000 × present atmosphere). Pyrolusite is suppressed to favour hydrated and mixed
valence oxides and hydroxides such as birnessite [(Na,Ca,K)(Mg,Mn)Mn6O14.5H2O], stabilized by minor
elements. Birnessite is comparable to the thermodynamically uncharacterised ranciéite [CaMn4O9.3H2O].
have come to dominate the ocean, driving the pH toward 7 (Macleod et al. 1994) (Fig.
24a). At neutral pH the availability of Fe2+, and thereby of Fe(III) as an electron acceptor,
would have been more restricted. Thus the pmf (protonic potential) generated in this way,
as well as that resulting from ambient pH, could only operate at a much reduced level.
Moreover, a depletion of suitable electron donors would also have driven organisms to
compensate for the loss of a redox coupled pmf by the development of a dependency on
solar photons (Raven and Smith 1981). Thus, organisms could contrive a new way of
generating this all-important force (Michel and Deisenhofer 1988) (Fig. 25 ).
In the event of an increase in oceanic pH, some heterotrophic eubacteria may have
switched from FeOOH to MnO2 acceptance for their electrons. That this is feasible is
illustrated by the report of Myers and Nealson (1988) who showed that Alteromonas
putrefaciens reduced MnIV at an optimum temperature of 35°C at pH 6 to 7. That Mn is
exploited by bacteria in a submarine hydrothermal plume to this day has been
demonstrated by Cowen et al. (1986). The use of manganese may have helped to prepare a
structural site for this element in a bacterium during the development of oxygenic
photosynthesis. Indicative is the fact that the physiologically highly versatile green nonsulfur bacterium Chloroflexus aurantiacus can bind Mn in preference to Fe in the nonheme electron transfer site (Dimukes et al. 2001). Manganese (as Mn2 + ) remains soluble
in water to higher Eh and pH values than iron (Fig. 24b). Its solubility is theoretically
controlled by pyrolusite (MnO2 ), and, in the presence of bicarbonate, by rhodochrosite
(MnCO3 ). It could therefore have been available for photo-oxidation to an insoluble
complex oxide such as birnessite [(Na,Ca)(Mg,Mn)Mn6 O1 4.5H2 O] (Anbar and Holland
1992). Birnessite occurs widely today in seafloor Mn/Fe nodules as well as submarine
exhalites (Burns and Burns 1979).
15.1. FIRST PIGMENTS
15.1.1 Energetic expectations
Pratt (1993) has suggested that the macrocyclic corrin ligands, the tetrapyrroles, date from
4 Ga, and Eschenmoser (1988) has shown how the corrin ring can be induced to accept,
depending on "tuning", one atom from biophile metals such as Fe, Mg, Co, and Ni.
Magnesium in a uroporphinoid, confers a capability of receiving and being activated by
photons. A consideration of the management of solar radiation would suggest that the first
unsophisticated photosynthetic organisms could have only used the relatively long
wavelength photons, i.e., those with a voltage that could be tolerated by anaerobic
chemosynthetic bacteria with a developing propensity to absorb energy from photons. In
fact, the pigments chlorophyll 870, P840 and P798 (i.e., those excited by near-infrared
light and spanning energies from 1.42 to 1.53 volts) characterize the Purple/Green, Green
Sulfur Bacteria and Heliobacteria which occupy lower branches of the evolutionary tree.
Because there is sequence similarity between bacteriochlorophylls and nitrogenase
(section 5), they are presumed to have descended from nitrogen-reducing proteins, via
gene duplication and mutation (Armstrong 1998; Blankenship 2002).
15.2. SULFHYDRYL AND ANOXYGENIC PHOTOSYNTHESIS
Whatever the reason for the macroevolutionary jump from chemosynthesis to
photosynthesis, a reliance on sulfur metabolism and ferredoxins was maintained. With the
chemosynthetic model in mind, involving as it did, iron, HS- and simple thiols, it is no
surprise that within the chemosynthetic group of microbes, iron and then sulfur respiration
preceded methanogenesis (Brock et al. 1997; Vargas et al. 1998). In these early anoxic
times the role of the first photosynthetic reaction centre was in the generation of protonic
potential or protonmotive force, and thereby ATP, by cycling electrons from acceptor back
to donor via the cytochrome bc complex or its equivalent (Vermaas 2003; Blankenship
2002) (Fig. 25), just as both the purple and the green-sulfur and heliobacteria do today.
From a consideration of the energetics mentioned above, amongst the primitive anoxygenic
photosynthetic Eubacteria the two relevant kingdoms are the
Fi
g. 25. Electron pathways of oxygenic photosynthesis for cyanobacteria. Photosystems I and II are based
on Prescott et al. (1993) for pH = 7 but PSII is displaced, only for clarity, to a lower pH. In non-cyclic
photophosphorylation NADP+ is reduced by an electron from PSI to make NADPH; PSII provides an
electron to replenish PSI while dissociation of water to evolve oxygen provides the electron to replenish
PSII. In cyclic photophosphorylation only PSI is used and NADP+ does not receive an electron; protons
are transferred out of the cell, generating a pmf which produces ATP. Photosynthetic production of
NADPH, ATP and protons contribute to the synthesis of carbohydrate from CO2. Absorption of light
provides an alternative source of redox energy for hydrogen provision to chemical energy although FeS
remains at the core of the energy-transfer system (cf. Fig. 12 and with Blankenship 2002 fig. 11.7).
green sulfur and the purple bacteria. However, of the two, the purple bacteria only use
quinone-type reaction centres, whereas the green sulfur bacteria use electrons from sulfide
in combination with Fe/S clusters (Hauska et al. 2001; Vassiliev et al. 2001).
Thus, notwithstanding the 16S rRNA data, we presume, following Vermaas (1994),
that antecedents of green-sulfur-like bacteria evolved before the purple bacteria antecedents
because:
i) as we have seen, infrared radiation would not have been damaging to a metabolic system
already dealing with commensurate energies,
ii) it would have been a simpler evolutionary step to develop the Fe/S centres from those
most ancient of all biological catalysts, the ferredoxins, which, as in reaction centre 1, can
operate at the very low redox to be expected in the early ocean, where they could reduce
NADP and fix carbon from carbonate, with, for example, HS- as reductant.
iii) the green sulfur bacteria and the chloro-bacteria (Liebl et al., 1993) have homodimeric
reaction centres, whereas the purple bacteria, as well as the green filamentous and
cyanobacteria, have heterodimeric centres which resemble the less complex homodimer
(Hauska et al. 2001).
15.3. OXYGENIC PHOTOSYNTHESIS
Oxygenic photsynthesis is a much more demanding macroevolutionary development.
Nevertheless we assume it to have occurred early in the Archaean. Although the
accumulation of oxygen in the atmosphere began about 2.5 Ga (Farquhar et al. 2000),
mineralogical (hydrothermal-exhalative ferric iron) and rare earth element (negative Ce
anomaly) evidence for localized concentrations of oxygen in seawater, presumably
generated by proximal cyanobacterial colonies, date from at least 3.5 Ga (de Ronde et al.
1994), and probably from 3.8 Ga (Dymek and Klein 1988). Also Buick and Dunlop
(1990) have described 3,500 Ma marine sulfates from Western Australia and Runnegar
(2001) has shown that this barite (BaSO4) was primary. For sulfates to be stable traces of
free oxygen are necessary (Ohmoto et al. 1993). And stromatolites, presumably generated
by cyanobacteria, were also established by then (Walter 1983).
To evolve from non-oxygenic to oxygenic photosynthesis requires higher energies
(shorter wavelengths) and the processing of four protons and four electrons (Blankenship
2002). Water rather than H2 S is the electron donor in these circumstances at a midpoint
potential of 820 millivolts (equ. 28; Fig. 25).
2H2 O → O2 + 4H+ + 4e-
(28)
For carbon dioxide to be fixed requires the generation of NADPH for which two
photosystems (PSI and PSII) are used (Vermaas 2002). PSI of the cyanobacteria, similar
to RCI of the green sulfur bacteria (with Fe/S centres) discussed above, contains
chlorophyll 700 (700 nm), the oxidation of which gives a potential of 1.82 volts. PSII is
similar to RCII of the purple and green filamentous bacteria, and uses chlorophyll 680
(680 nm = 1.77 volts). It includes the CaMn4 centre responsible for water oxidation and
the entrie complex is designated PSII-WOC (Dismukes et al. 2001).
While evolution of PSII from a single RC ancestor belonging to the purple
bacteria can be explained by gene doubling and adaptation (Hansson and Wydrzynski
1990; Vermaas 2002), the introduction of the oxygen-evolving complex comprising the
CaMn4 core is such an extraordinary biological innovation that we have argued for the
cooption of a "ready-made" cluster as an explanation (Russell and Hall 2001; and see
Sauer and Yachandra 2002). This idea echoes our assumption that an [4Fe-4S] cubane
cluster could either be interred in the mineral greigite or sequestered by peptides into a
ferredoxin where it provided a "preformed" electron transfer site for the first metabolist.
Both the [4Fe-4S] cubane and the CaMn4 complex allow for loss and, in the case of the
iron sulfide, gain of (delocalized) electrons, from Fe2.5+ and Mn2.75+ respectively.
Sequestering of the [Fe4 S4 ] cubane with peptide both protects and allows the integrity of
the structure to survive, with minor distortion, the addition or subtraction of a single
electron (Beinert et al. 1997). Required to extract and accumulate four electrons and
protons from water, the conformational changes of the CaMn4 structure (ligated to the
tyrosine Yz) are much more extreme than the minor flexions of [Fe4 S4 ]+/2+, and are not
yet fully characterized (Fig. 26) (equ. 29).
[Mn4 13+ ~Yz] ↔ [Mn4 16+ ~Yz+] + 4e-
(29)
The original sequestering site of the "ready-made" CaMn4 complex may have been where
tyrosine and amines were already present in an ancestral type II reaction centre. Tyrosine
is conserved in all purple bacteria where it facilitates electron transfer between particular
Fig. 26. Model for the origin of a 'preformed' abiotic [CaMn4O9.3H2O] core cluster which, we suggest,
was enrolled in an antecedent of RCI to produce the water-oxidising complex in PSII (Russell and Hall
2001; Carrell et al. 2002; Sauer and Yachandra 2002).
pigments (Allen et al. 1988). We now revisit the experimental and geochemical evidence
that favours such a speculation.
Hot springs would have discharged Fe and Mn to the ocean in the early Archaean
(Appel, et al. 2001) just as they do today. Because iron is less soluble at higher pH, it
would have precipitated around the spring partly as sulfide (Walker and Brimblecombe
1985), leaving a putative cluster, [MnII2(HCO3 )4 ]n (Dismukes et al. 2001), to be photooxidized at extremely short wavelength beyond UV-C (λ ~225 nm (~5 volts) either to
birnessite (Anbar and Holland 1992), or possibly, in the presence of Ca, to colloidal
clusters of [3H2 O.CaMn4 O9 ], with the concomitant reduction of FeIII (Figs. 1, 26)
(Russell and Hall 2001). This putative cluster is similar to the naturally occurring mineral
ranciéite. Thus a CaMn4 species may have been a free cluster prior to sequestering by
RCI. A comparison between the mineral and the oxygen-evolving polymorphic complex is
instructive. Calcium is ligated to water in ranciéite (Post and Appelman 1988) (Fig. 26)
and the metal may also act as the water donor site in the oxygen evolving complex,
releasing it to the fully-accumulated positive charge state four (S4) of the tetra-manganese
cluster (Kok et al. 1970; Rutherford 1989). It is as a Lewis acid that calcium activates
water oxidation (Yocum 1991).
Calcium has several other roles: that of conducting electrons to tyrosine during
oxidation of the complex; preventing dissolution on reduction to state zero (S0) (cf.
Homann 1987), or, because of its low charge concentration, in preventing the formation
and locking of [Mn4 O4 ]4 + as a cubane (as in the hausmannite cluster
[(Mn2+)2 (Mn3+)4 O8 ], Fig. 26) during the reduction to the S0 phase in the precursor to
photosystem II. Indeed, the water oxidizing complex cannot function in the absence of
calcium (and chlorine) (Ghanotakis et al. 1984 Yocum 1991; Homann 1987).
Nevertheless, our choice of ranciéite as the precursor cluster structure to is not without its
difficulties. Based on their EXAFS studies Yachandra et al. (1996) conclude that the water
oxidising complex contains at least one Ca-O-Mn linkage at ~3.4Å. Two, or more
probably three, of the manganese pairs have non colinear di-µ-oxo bridges separated by
~2.75Å, and one, or perhaps two mono-µ-oxo bridges at about 3.3Å (Yachandra et al.
1996). Although the Mn-Mn vectors in ranciéite are all ~2.75Å we assume that, at the
scale of the cluster, oxobridges could have been mutable, i.e., one of the sp3 -type oxygens
could have reconformed to an sp2 -type. The calcium too would need to have a different
conformation to be closer in to the proximal manganese. Nevertheless, these differences
have led Sauer and Yachandra (2002) to identify and characterize hydrated manganate
minerals with tunnel structures with the oxo bridges directly comparable to those in the
water oxidizing complex. From this perspective the putative clusters that could comprise
hollandite [(Ba,K)1-2Mn8 O1 6.xH2 O] are best suited for enrolment in the first water
oxidizing complex (Sauer and Yachandra 2002).
The critical potential for the splitting of water (equ. 28) is 820 mV, although 200
mV activates individual proton transfer (Dau et al. 2001). This is easily exceeded by
relatively high energy photons and in the event the midpoint potential of P680 is 1.1 volts
(Fig. 25). The danger is more one of 'electrocution' of the first oxygenic photosynthesists
rather than a shortfall in energy supply (Fig. 1c & d). The four electrons from water are
used indirectly to reduce CO2 . Returning to the Nernst equation, it may be demonstrated
that the minimum potential requirement is therefore below that offered by the native and
excited states of P680 and P700, i.e., ≤2.4 mV (Figs 1 & 25).
We again stress that the iron-sulfur proteins remain a requirement in oxygenic
photosynthesis, as electron transfer agents and in the hydrogenase responsible for the
generation of ATP from four protons (Van Walraven et al. 1997; Vassiliev et al. 2001).
16. Proposed experimental reconstructions
Results of experimental work on the origin of life have not lived up to their early promise.
Experiential, rather than experimental, knowledge has been the more useful, i.e., that
gleaned from pertinent geological, geophysical, geochemical and biochemical discoveries.
Laboratory experiments have attempted to address particular steps along a critical path,
reducing the enterprise to, for example, a demonstration of the generation of pyruvate. But
interpretations and extrapolations of reactions from experiments with few reactants run to
equilibrium do not consider the electrical and protonic potentials that drove early life to
emerge, nor the separation of reactants by a semiconducting, semipermeable inorganic
membrane. With these factors in mind it is time to return to experiment. Below we
describe a nexus of chemical reactors suited to the reconstruction of how life could have
begun. The logic in our approach is to find experimental counterparts to what is, as yet, an
incomplete theory for the emergence of life (cf. Corliss 1986). Experimental assessments
of this type should help to reveal the weaknesses and any strengths of the alkaline
hydrothermal theory.
Although the descendence of photosystem II, which contains the CaMn4 cluster
that oxidizes water, is a biochemical issue (Bayman et al. 2001), the origin and enrolment
of the cluster itself is partly a photogeochemical problem. To this end we discuss possible
experimental approaches that may throw further light on its origins.
16.1 PREVIOUS EXPERIMENTS ON ORIGINS OF CHEMOSYNTHESIS
The "Catalytic Reactor Vessel" designed by Voglesonger et al. (2001) is the first flow
reactor to simulate a high temperature hydrothermal environment. This reactor, which
operates at up to 400°C and 30 MPa, was built to investigate an ephemeral H2 -CO2 -rich
vapour phase produced during the intrusion of magmatic dykes, and for this phase to react
with a magnetite catalyst in the presence of quartz to generate methanol. A low temperature
catalytic flow reactor has also been used by Weber (2001) to synthesise pyruvaldehyde
from triose catalyzed by poly-L-lysine. To the best of our knowledge origin of life
experiments have not been carried out using flat bed or electrochemical reactors. We
would emphasize that the reactor nexus we describe below will operate at the relatively low
temperatures obtaining in medium enthalpy hydrothermal systems feeding deep submarine
seepages (cf. Matsuno 1997).
16.2 THE NOTIONAL REACTOR NEXUS
The alkaline hydrothermal model for the emergence of life is depicted as a nexus of
chemical reactors. A submarine, medium temperature hydrothermal cell is modelled,
notionally, as a pressurized flow reactor packed with rock-wool partially impregnated with
native iron dosed with nickel and traces of the platinum group elements . An aqueous
solution approximating the chemistry of acidulous ocean water (1 in Fig. 27) as it was
~4.4 billion years ago is envisaged to flow through the reactor (2 in Fig. 27), simulating
the convective path. Carbon oxides, sulfide and ammonia (all derivable from a rocky
planet's mantle and crust) are variably introduced into the line operated at 100° to 200°C.
Primary production of hydrogen, methane, methanol, formaldehyde, and acetate is
expected. The now alkaline aqueous product from the flow reactor is introduced to the
base of a flat-bed reactor (3 in Fig. 27), kept at ~100°C, containing alternating layers of
freshly precipitated Fe>>Ni-Co sulfides, Fe>Mg hydroxides and Fe,Ca,Mg carbonates.
The flat bed reactor represents the metalliferous deposits generated at the submarine
hydrothermal seepage sites at a distance from oceanic spreading centres. As the fluids
percolate upwards we expect carbon and nitrogen compounds to be filtered out and
adsorbed, especially onto the sulfides. Simple amino acids will be generated in this milieu.
And once the critical concentrations for oligomerization reactions are attained, then other
C2 to C1 0 compounds could be generated. Thus enriched, the alkaline solutions are passed
through to an electrochemical reactor (4 in Fig. 27) with anode and cathode separated by a
furion membrane supporting freshly precipitated FeS. The anode is poised at the
hydrogen potential at the pH of the hydrothermal solution (pH ~10) whereas the cathode
is controlled by an Fe2+/FeIII couple at a putative oceanic pH of ~5.5. The anodic
compartment simulates bubbles of Fe>>Ni-Co sulfides, inflated at the seepages, and
previously considered to act as the hatcheries of life (Russell and Hall 1997). The
temperature of the electrochemical reactor would be held at ~40°C. In the geological
model, ferric oxyhydroxide has been derived from ferrous iron in the acidulous ocean by
photolysis of water. The exterior electrolyte, a simulacrum of this FeIII-bearing ocean, is
also a reservoir of pyrophosphate. We expect minor amounts of sugar phosphates and
purines to be synthesized in the electrochemical reactor, again by oligomerization. A
proportion of these liquors are refluxed to the flat bed reactor.
16.3. PREVIOUS EXPERIMENTS INTO OXYGENIC PHOTOSYNTHESIS
Although not concerned with the origins of the water oxidizing complex per se, Anbar and
Holland (1992) record birnessite [(Na,Ca,K)(Mg,Mn)Mn6O14.5H2O] in their
photochemical experiments, a structure broadly comparable to the inorganic cluster at the
heart of PSII. Using x-ray spectroscopy Sauer and Yachandra (2002) have provided a
number of candidate Mn4 clusters to consider in this regard.
16.4. EXPERIMENTAL APPROACHES TO THE ORIGIN OF THE WOC
The Anbar-Holland photooxidation experiment should be repeated but with the addition of
calcium bicarbonate. We expect a clusters to form, which on growth will prove to be
ranciéite [CaMn4 O9 .3H2 O] (Fig. 1c). If so a type I reaction complex from a
photosynthetic bacterium such as Chloroflexus aurantiacus could be introduced to the
aqueous solution immediately after radiation to investigate if the cluster could be
sequestered. If not it could be genetically modified in vitro to include four site-directed
histidines with appropriate spacings and the experiment repeated.
Fig. 27. Schematic figure to illustrate the envisaged reactor nexus.
17 Summary
We argue here that life emerged where warm alkaline waters seeped into the cool
acidulous ocean sometime within the first few hundred million years of Earth history.
Links can be assumed between the rather slow, low temperature reactions of geochemistry
and the quickened reactions of early biochemistry. The alkaline seepage waters contained
HS-, CH3SH, NH3, HCN, CO and CH2O. Dissolved or dispersed in the ocean were CO2,
P2O6OH3-, Fe2+ and photolytic FeIII. Mixing of the two fluids was frustrated by the
precipitation of a semipermeable FeS barrier at the seepage, possibly supported by an
iron- and magnesium-rich clay matrix comprising the hydrothermal mound. We attempt to
imagine the first eobiochemical pathways taken by the potential energy as it began to leak
through this barrier. Early metabolism probably comprised the Pentose Phosphate Cycle
and the Acetyl-CoA Pathway of CO2 fixation. Hydrogen in the hydrothermal fluid lost
electrons to FeIII on the exterior of the barrier by hopping from one mackinawite crystallite
to another. The 'leftover' protons were driven through aqueous films in the barrier to
maintain charge balance before grouping to return into the membrane to generate
pyrophosphate. Mackinawite (Fe1+xS) and greigite (as [SNiS][Fe4 S4 ][SFeS]) also acted
as prebiotic hydrogenases. The simple amino acids were generated within the
hydrothermal mound. Early proteins, including some of those comprising the
proteinaceous cell envelope that took over from the initial iron sulfide barrier, may have
been first coded for by up to 10-mer RNA adhering to mackinawite in the submarine
hydrothermal mound. Polymerization of these amino acids and their release as
constituents of protopetides was effected by rapid oscillations to low pH in the membrane.
Eventually, the metal sulfide clusters such as the [Fe4 S4 ] cubane, which otherwise would
be interred in metastable greigite, became enrolled in protoferredoxin ([Fe4 S4 ][SR]4 2-/3-),
where the ligands were other regulated peptide trimers. The addition of the peripheral
[SNiS] moiety to the greigite cubane may have composed an active centre to a primitive
CO-dehydrogenase ligated to similar short peptides.
Another "preformed" metal-bearing cluster lent itself to the other most remarkable
metabolic innovation — oxygenic photosynthesis. Oxygenic photosynthesis, with its
requirement to generate four protons and four electrons by the splitting of two water
molecules, may have been facilitated by a mutant Reaction Complex belonging to an
antecedent of a purple or green filamentous bacterium. This complex could have
sequestered an active [CaMn4 ] core in an enlarged manganese site, from a photolytic
[3H2 O.CaMn4 O9 ] cluster in the early ocean, a cluster that otherwise would be destined for
incarceration in the mineral ranciéite. Calcium has various functions in what became the
water-oxidizing complex, but its original role may have been in preventing the reduction of
the manganate to an inflexible [Mn4 O8 ] cubane. This is because its low charge
concentration with respect to a manganous ion is not conducive to the formation of a
spinel. While an [Fe4 S4 ] cubane is adequate to allow single electron transfer a [Mn4 O8 ]
cubane structure could not partake in the extraction of the four protons and electrons from
water necessary to effect oxygenic photosynthesis.
Critical values for the onset of hydrothermal convection, chemosynthetic
metabolism and oxygenic photosynthesis are given by the Rayleigh and Nernst equations.
They are a dimensionless 40, and 250 mV and 2.4 V respectively, quantities easily
exceeded in conditions obtaining on the early Earth. We aver that a experiments using a
reactor nexus which takes account of chemiosmosis at the final stages of moderate
temperature aqueous geochemical reaction will demonstrate the feasibility of this general
model for the onset of chemosynthesis. Photochemical and biological experiments
involving solutions of calcium and manganese chloride and carbonate may also throw light
on the origin of oxygenic photosynthesis.
Acknowledgements
We thank John Allen, Richard Cogdell, Chuck Dismukes, Rob Hengeveld, Max
McDowall, Bill Martin, Nick Platts, Laiq Rahman, John Raven, Woonsup Shin, Mike
Solomon, David Stone and Dugald Turner for discussions.
References
Abbott, D.H. and Hoffman, S.E. (1984) Archaean plate tectonics revisited 1. Heat flow, s
preading rate, and the age of subducting oceanic lithosphere and their effects on the o
rigin and evolution of continents, Tectonics 3, 429-448.
Abrajano, T.A., Sturchio. N.C., Kennedy, B.M., Lyon, G.L., Muehlenbachs, K. and Bohl
ke, J.K. (1990) Geochemistry of reduced gas related to serpentinization of the Zamba
les ophiolite, Philippines, Applied Geochemistry 5, 625-630.
Allen,
J.F.
(1993) Redox control of transcription: sensors, response regulators, activators and re
pressors, FEBS 332 203-207.
Allen, J.P., Feher, G., Yeates, T.O., Komiya, H. and Rees, D.C. (1988) Structure of the
reaction center from Rhodobacter sphaeroides R-26: Protein-cofactor (quinones and
Fe2 +) interactions, Proceedings of the National Academy of Science, USA 85, 84878491.
Alt, J.C. and Teagle, D.A.H. (1999) The uptake of carbon during alteration of the oceanic
crust, Geochimica et Cosmochimica Acta 63, 1527-1535.
Amend, J.P. and Shock, E.L. (2001) Energetics of overall metabolic reactions of thermop
hilic and hyperthermophilic Archaea and Bacteria, FEMS Microbiological Reviews 2
5, 175-243.
Ames, D.E., Watkinson, D.H. and Parrish, R.R. (1998) Dating of a regional
hydrothermal system induced by the 1850 Ma Sudbury impact event, Geology 26,
447-450.
Ananyev, G.M., Zaltsman, L., Vasko, C. and Dismukes, G.C. (2001) The inorganic
biochemistry of photosynthetic oxygen evolution/water oxidation, Biochimica et
Biophysica Acta, 1503, 52-68.
Anbar, A.D. and Holland, H.D. (1992) The photochemistry of manganese and the origin
of banded iron formations, Geochimica et Cosmochimica Acta 56, 2595-2603.
Anderson, R.B., Langseth, M.G. and Sclater, J.G. (1977) The mechanisms of heat transf
er through the floor of the Indian Ocean, Journal of Geophysical Research 82, 33913409.
Anderson, T.B. and Jackson, R. (1968) Fluid mechanical description of fluidized beds, I
ndustrial Engineering Chemical Fundamentals 7, 12-21.
Appel, P.W.U., Rollinson, H.R. and Touret, J.L.R. (2001) Remnants of an Early Archaea
n (>3.75 Ga) sea-floor, hydrothermal system in the Isua Greenstone Belt, Precambri
an Research 112, 27-49.
Armstrong, G.A. (1998) Greening in the dark: Light-indpendent chlorophyll
biosynthesis from anoxygenic photosynthetic bacteria to gymnosperms, Journal of
Photochemistry and Photobiology. B: Biology 43, 87-100.
Arrhenius, G. (1986) Dysoxic environments as models for primordial mineralisation, in
A.G. Cairns-Smith and H. Hartman, (eds.), Clay and Clay Minerals and the Origin
of Life, Cambridge University Press, pp. 97-104.
Avnir, D. (ed.) (1989) The Fractal Approach to Heterogeneous Chemistry, John Wiley
and Sons, New York.
Ball, B. and Rickard, R.S. (1976) The chemistry of pyrite flotation and depression, in M.
C. Fuerstenau (ed.), Flotation,
A.M.
Gaudin
Memorial
Volume vol 1, American Institute of Mining Metallurgical and Petroleum Engineers,
pp. 458-484.
Ballhaus, C. and Ellis, D.J. (1996) Mobility of core melts during Earth's accretion, Earth
and Planetary Science Letters 143, 137-145.
Baltscheffsky, H. (1996) Energy conversion leading to the origin and early evolution of l
ife: Did inorganic pyrophosphate precede adenosine triphosphate? in H. Baltscheffsk
y (ed.), Origin and Evolution of Biological Energy Conversion, VCH Publishers, Ca
mbridge, pp. 1-9.
Baltscheffsky, M., Schultz, A. and Baltscheffsky, H. (1999) H+ -PPases: a tightly
membrane-bound family. FEBS Letters 457, 527-533.
Ban, N., Nissen, P., Hansen, J., Moore, P.B. and Steitz, T.A. (2000) The complete atomic
structure of the large ribosomal subunit at 2.4 Å resolution, Science 289, 905-920.
Banks, D. (1985) A fossil hydrothermal worm assemblage from the Tynagh lead-zinc de
posit in Ireland, Nature 313, 128-131.
Baranov, S.V., Ananyev, G.M., Klimov, V.V. and Dismukes, G.C. (2000) Bicarbonate
accelerates assembly of the inorganic core of the water-oxidizing complex in
manganese-depleted photosystem II: A proposed biogeochemical role for
atmospheric carbon dioxide in oxygenic photosynthesis, Biochemistry 39, 60606065.
Barnes, H.L. (ed.) (1997) Geochemistry of Hydrothermal Ore Deposits, John Wiley an
d Sons, New York.
Barrie, T.T., Erendi, A, and Cathles, L. (2001) Paleosea-floor volcanic-associated massive
sulfide mineralization related to a cooling
komatiite
flow,
Abitibi
Province, Canada, Economic Geology 96, 1695-1700.
Baymann, F., Brugna, M., Mühlenhoff, U. and Nitschke, W. (2001) Daddy, where did (P
S)I come from? Biochimica et Biophysica Acta 1507, 291-310.
Beinert, H., Holm, R.H. and Münck, E. (1997) Iron-sulfur clusters: Nature's modular, m
ultipurpose structures, Science 277, 653-659.
Berg, J.M. and Holm, R.H. (1982) Structures and reactions of iron-sulfur protein cluster
s and their synthetic analogues, in T.G. Spiro (ed.), Iron-sulfur
proteins, Wiley-Interscience, New York, pp. 1-66.
Bernal, J.D. (1960) The problem of stages in biopoesis, in M. Florkin (ed.), Aspects of
the Origin of Life, Pergamon Press, New York, pp. 30-45.
Bernard, A. and Symonds, R.B. (1989) The significance of siderite in the sediments fro
m Lake Nyos, Cameroon. Journal of Volcanic and Geothermal Research, 39, 187-1
94.
Bethke, C. (1996) Geochemical Reaction Modeling, Oxford University Press.
Beutner, R. (1913) New electric properties of a semipermeable membrane of copper ferr
ocyanide, Journal of Physical Chemistry 17, 344-360.
Bischoff, J.L. and Rosenbauer, R.J. (1984) The critical point and two-phase boundary of
seawater, 200-500°C, Earth and Planetary Science Letters 68, 172-180.
Black, S, (2000) A Theory on the Origin of Life plus a Brief History of Biochemistry, Va
ntage Press, New York.
Blankenship, R.E. (2002) Molecular Mechanisms of Photosynthesis, Blackwell Science,
Oxford.
Blichert-Toft, J. and Albarède, F. (1994) Short-lived chemical heterogeneities in the Arch
ean mantle with implications for mantle convection, Science 263, 1593-1596.
Bonomi, F., Werth, M.T. and Kurtz, D.M. (1985) Assembly of FenSn(SR)2- (n=2,4) in
aqueous media from iron salts, thiols and sulfur, sulfide, thiosulfide plus rhodonase, I
norganic Chemistry, 24, 4331-4335.
Bounama, C., Franck, S. and von Bloh, W. (2001) The fate of the Earth's ocean, Hydrolo
gy and Earth System Sciences 5, 569-575.
Bourcier, W.L., Ulmer, G.C. and Barnes, H.L. (1987) Hydrothermal pH sensors of ZrO
2, Pd hydrides, and Ir oxides, in G.C. Ulmer and H.L. Barnes, (eds.), Hydrothermal
Experimental Techniques, John Wiley and Sons, New York, pp. 157-188.
Boyce, A.J., Coleman, M.L. and Russell, M.J. (1983) Formation of fossil hydrothermal c
himneys and mounds from Silvermines, Ireland, Nature 306, 545-550.
Brandes, J.A. Boctor, N.Z. Cody, G.D. Cooper, B.A. Hazen, R.M. and Yoder, H.S. (199
8) Abiotic nitrogen reduction on the early Earth, Nature 395, 365-367.
Braterman, P.S., Cairns-Smith, A.G. and Sloper, R.A. (1983) Photo-oxidation of hydrate
d Fe2 + — significance for banded iron formations, Nature 303, 163-164.
Breslow, R. (1959) On the mechanism of the formose reaction, Tetrahedron Letters 21,
22-26.
Brock, T.D., Madigan, M.T., Martinko, J.M. and Parker, J. (1997) Biology of Microorga
nisms, 8th Edition, Prentice Hall International, London.
Brünings, W. (1907) Beiträge zur Elektrophysiologie. III. Mitteilung. Zur Osmotischen
Theorie der Zellelektrizität, Pflüger Archiv für die Gesammte Physiologie 117, 409-4
60.
Buick, R. and Dunlop, J.S.R. (1990)
Evaporitic
sediments
of
early Archaean age from the Warrawoona Group, North Pole, Western Australia, Sed
imentology 37, 247-277.
Burns, R.G. and Burns, V.M. (1979) Manganese oxides, in R.G. Burns (ed.) Marine Mi
nerals, Reviews in Mineralogy vol. 6, Mineralogical Society of America, pp.1-46.
Cairns-Smith, A.G. (1982) Genetic Takeover and the Mineral Origins of Life, Cambridg
e University Press.
Cairns-Smith, A.G. and Walker, G.L. (1974) Primitive metabolism, Biosystems 5, 173-1
86.
Cairns-Smith, A.G. Hall, A.J. and Russell, M.J. (1992) Mineral theories of the origin of l
ife and an iron sulphide example. Origins Life and Evolution of the Biosphere 22, 16
1-180.
Canfield, D.E., Habicht, K.S. and Thamdrup, B. (2000) The Archean sulfur cycle and the
early history of atmospheric oxygen, Science 288, 658-661.
Carrell, T.G., Tyryshkin,
A.M.
and
Dismukes,
G.C.
(2002) A unified structural model for the photosynthetic water-oxidizing complex de
rived from spectroscopic signatures, Journal of BioInorganic Chemistry 7, 2-22.
Carter, A.P., Clemons, W.M., Broderson, D.E., Morgan-Warren, R.J., Wimberly, B.T. an
d Ramakrishnan, V. (2000) Functional insights from the structure of the 30S riboso
mal subunit and its interactions with antibiotics, Nature 407, 340-348.
Cathles,
L.M.
(1990)
Scales
and
effects of fluid flow in the upper crust, Science 248, 323-329.
Chakrabarti, A.C. and Deamer, D.W. (1994) Permeation of membranes by the neutral fo
rm of amino acids and peptides: Relevance to the origin of peptide translocation, Jour
nal of Molecular Evolution 39, 1-5.
Chen, Q.W. and Bahnemann, D.W. (2000) Reduction of carbon dioxide by magnetite: I
mplications for the primordial synthesis of organic molecules, Journal of the Americ
an Chemical Society 2000, 970-971.
Cleland, C.E. (2001) Historical science, experimental science, and the scientific method,
Geology 29, 987-990.
Cockell, C.S. and Knowland, J. (1999) UV radiation screening compounds, Biological R
eviews 74, 311-345.
Coey, J.M.D., Spender, M.R. and Morrish, A.H. (1973) The magnetic structure of spinel
Fe3S4, Solid State Communications 8, 1605-1608.
Cole, W.J., Kaschke, M., Sherringham, J.A., Curry, G.B., Turner, D. and Russell, M. J. (
1994) Can amino acids be synthesised by H2S in anoxic lakes? Marine Chemistry 4
5, 243-256.
Combarnous, M.A. and Bories, S.A. (1975) Hydrothermal convection in saturated porou
s media, Advances in Hydroscience 10, 231-307.
Connell, G.J., Illangasekare, M and Yarus, M. (1993) Three small ribooligonucleotides w
ith specific arginine sites, Biochemistry 32, 5497-5502.
Cooper, G., Kimmich, N., Belisle, W., Sarinana, J., Brabham, K. and Garrel, L. (2001) Ca
rbonaceous meteorites as a source of sugar-related compounds for early Earth, Natur
e 414, 879-883.
Corliss, J.B. (1986) On the creation of living cells in submarine hot spring flow reactors:
Attractors and bifurcations in the natural hierarchy dissipative systems, Origins of
Life and Evolution of the Biosphere 19, 381-382.
Couderc J-P. (1985) Incipient fluidization and particulate systems, in J.F. Davidson, R.
Clift and D. Harrison (eds.), Fluidization, Academic Press, New York, pp. 1-46.
Cowen, J.P., Massoth, G.J. and Baker, E.T. (1986) Bacterial scavenging of Mn and Fe in
a mid- to far-field hydrothermal particle plume, Nature 322, 169-171.
Daniel, R.M. and Danson, M.J. (1995) Did primitive microorganisms use nonheme iron
proteins in place of NAD/P? Journal of Molecular Evolution 40, 559-563.
da
Silva,
J.J.R.F. and Williams, R.J.P. (1991) The Biological Chemistry of the Elements, Clar
endon Press, Oxford.
Dau, H., Iuzzolino, L. and Dittmer, J. (2001) The tetra-manganese complex of photosyte
m II during its redox cycle
— X-ray absorption results and mechanistic implications, Biochimica et Biophysica
Acta 1503, 24-39.
Davis, E.E., Lister, C.R.B., Wade, U.S. and Hyndman, R.D. (1980) Detailed heat flow m
easurements over the Juan de Fuca Ridge system, Journal of Geophysical Research.
85B, 299-310.
Davis, R., Lehman, L., Petrovich, R., Shah, V.K., Roberts, G.P. and Ludden, P.W. (1996)
Purification and characterization of the alternative nitrogenase from the
photosynthetic bacterium Rhodspirillum rubrum, Journal of Bacteriology 178,
1445-1450.
de Ronde, de Wit, M.J. and Spooner, E.T.C. (1994) Early Archean (>3.2 Ga) Fe oxiderich, hydrothermal discharge vents in the Barberton greenstone belt, South Africa.
Geological Society of America Bulletin 106, 86-104.
Dimroth, E. and Kimberly, M.M. (1976) Precambrian atmospheric oxygen: evidence in t
he sedimentary distributions of carbon, sulfur, and iron, Canadian Journal of Earth
Science 13, 1161-1185.
Dismukes, G.C., Ruettinger, W., Boelrijk, A.E.M. and Ho, D. (1998) Structure of the M
n4Ca1 core of the PSII water oxidizing complex and the Mn4O4-cubane/Mn4O2butterfly
model
complexes, Proceedings XIth International Photosynthesis Congress, Vol. II, Kluwe
r Academic Publishers, Dordrecht, pp. 1259-1264.
Dismukes, G.C., Klimov, V.V., Baranov, S.V., Kozlov, Yu.N., DasGupta, J. and Tyryshki
n, A. (2001) The origin of atmospheric oxygen on Earth: The innovation of oxygenic
photosynthesis, Proceedings of the National Academy of Science, USA 99, 2170-21
75.
Dobbeck, H., Svetlitchnyi, V., Gremer, L., Huber, R. and Meyer, O. (2001) Crystal struct
ure of a carbon monoxide dehydrogenase reveals a [Ni-4Fe-5S] cluster, Science 293,
1281-1285.
Drennan, C.L., Heo, J., Sintchak, M.D., Schreiter, E. and Luddon, P.W. (2001) Life on c
arbon monoxide: X-ray structure of Rhodospirillium rubrum Ni-Fe-S carbon monox
ide dehydrogenase, Proceedings of the National Academy of Science, USA 98, 11973
-11978.
Dymek, R.F. and Klein, C (1988) Chemistry, petrology and origin of banded iron-format
ion lithologies from the 3800 Ma Isua Supracrustal Belt, West Greenland, Precambr
ian Research 39, 247-302.
Eck, R.V. and Dayhoff, M.O. (1966) Evolution of the structure of ferredoxin based on li
ving relics of primitive amino acid sequences, Science 152, 363-366.
Eigen, M. and Schuster, P. (1978) The hypercycle: a principle of natural self-organizatio
n: Part C: The realistic hypercycle. Naturwissenschaften 65, 347-369.
Elder, J. (1976) The Bowels of the Earth. Oxford University Press.
El-Kaissy, M.M. and Homsy, G.M. (1976) Instability waves and the origin of bubbles in
fluidized beds, International Journal of Multiphase Flow 13, 459-475.
Eschenmoser, A. (1988) Vitamin B12: Experiments concerning the origin of its molecula
r structure, Angewandte Chemie, International Edition in English, 27, 5-39.
Eschenmoser, A. (1994) Chemistry of potentially prebiological natural products, Origins
of Life and Evolution of the Biosphere 24, 389-423.
Farquhar, J., Bao, H. and Thiemens, M. (2000) Atmospheric influence of Earth's earliest
sulfur cycle, Science 289, 756-758.
Fehn, U. and Cathles, L.M. (1986) The influence of plate movement on the evolution of
hydrothermal convection cells in the oceanic crust, Tectonophysics 125, 289-312.
Feiler, U. and Hauska, G. (1995) The reaction center from green sulfur bacteria, in R.E.,
Blankenship, M.T. Madigan and C.E. Bauer (eds.), Advances in Photosynthesis: Ano
xygenic Photosynthetic Bacteria, Kluwer Academic Publishers, Dordrecht, pp. 665-6
85.
Ferris, F.G., Jack, T.R. and Bramhill, B.J. (1992) Corrosion products associated with atta
ched bacteria at an oil field water injection plant, Canadian Journal of Microbiology
38, 1320-1324.
Ferris, J.P, (1974) Chemical evolution XVIII. Synthesis of pyrimidines from guanidine a
nd cyanoacetaldehyde, Journal of Molecular Evolution 3, 301-309.
Ferris, J.P. (1992) Chemical markers of prebiotic chemistry in hydrothermal systems, Or
igins of Life and Evolution of the Biosphere 22, 109-134.
Ferris, J.P. and Ertem, G. (1993) Montmorillonite catalysis of RNA oligomer formation i
n aqueous solution. A model for the prebiotic formation of RNA, Journal of the Ame
rican Chemical Society 115, 12270-12275.
Ferris, J.P, Joshi, P.C., Edelson, E.H. and Lawless, J.G. (1978) HCN: A plausible source
of purines, pyrimidines and amino acids on the primitive Earth, Journal of Molecula
r Evolution 11, 293-311.
Ferris, J.P., Hill, A.R. Liu, R. and Orgel, L.E. (1996) Synthesis of long prebiotic oligome
rs on mineral surfaces, Nature 381, 59-61.
Fisher, A.T. and Becker, K. (2000) Channelized fluid flow in oceanic crust reconciles he
at-flow and permeability data, Nature 403, 71-74.
Forterre, P. and Philippe, H. (1999) Where is the root of the universal tree of life? Bioess
ays 21, 871-879.
Fournier, R.O. (1999) Hydrothermal processes related to movement of fluid from plastic
into brittle rock in the magmatic-epithermal environnent, Economic Geology 94, 119
3-1211.
Francis, D., Luddon, J., Johnstone, R. and Davis, W. (1999) Picrite evidence for more Fe
in Archean mantle reservoirs, Earth and Planetary Science Letters 167, 197-213.
Fuerstenau, M.C. (ed.) (1976) Flotation: A. M. Gaudin Memorial Volume, Vol. 1,
American Institute of Mining, Metallurgical and Petroleum Engineers, New York.
Fyfe, W.S. (1974) Heats of chemical reactions and submarine heat production, Geophysi
cal Journal of the Royal Astronomical Society 37, 213-215.
Gaffey, M.J.
(1997)
The
early
solar
system, Origins of Life and Evolution of the Biosphere 27, 185-203.
Garrels, R.M. and Christ, C.L., (1965) Minerals, Solutions and Equilibria, Harper Row,
New York.
Geptner, A., Kristmannsdöttir, H., Kristjánsson, J.K. and Marteinsson, V.M.
(2002) Biogenic saponite from an active submarine hot spring, Iceland, Clays and
Clay Minerals 50, 174-185.
Gerlach, T.M. (1989) CO2 from magma-chamber degassing, Nature 337, 124.
Gesteland, R.F., Cech, T.R. and Atkins, J.F. (eds.) (1999) The RNA World, Cold Spring
Harbor Laboratory Press, New York.
Ghanotakis, D.M., Babcock, G.T. and Yocum, C.F. (1984) Calcium reconstitutes high rat
es of oxygen evolution in polypeptide depleted Photosystem II preparations, FEBS 1
67, 127-130.
Gilbert, W. (1986) The RNA World, Nature 319, 618.
Glansdorff, P. and Prigogine, I. (1971) Thermodynamic Theory of Structure, Stability a
nbd Fluctuations, Wiley-Interscience, London.
Glasby, G.P. and Kasahara, J. (2001) Influence of tidal effects on the periodicity of earth
quake activity in diverse geological settings with particular emphasis on submarine sy
stems, Earth Science Reviews 52, 261-297.
Godderis, Y. and Veizer, J. (2000) Tectonic control of chemical and isotopic composition
of ancient oceans: The impact of continental growth, American Journal of Science
300, 434-461.
Goldschmidt, V. M. (1937) The principles of distribution of chemical elements in minera
ls and rocks, Journal of the Chemical Society 1937, 655-673.
Gonzalez, G., Brownlee, D, and Ward, P.D. (2001) The galactic habitable zone, Icarus 1
52, 185-200.
Gunter, W.D., Myers, J. and Girsperger, S. (1987) Hydrogen: Metal membranes, in G.C
. Ulmer and H.L. Barnes, (eds.), Hydrothermal Experimental Techniques, New York
, John Wiley and Sons, pp. 100-120.
Haack, U.K. and Zimmermann, H.D. (1996) Retrograde mineral reactions: a heat source
in the continental crust, Geologische Rundschau 85, 130-137.
Hall, D.O., Cammack, R. and Rao, K.K. (1971) Role for ferredoxins in the origin of life
and biological evolution, Nature 233, 136-138.
Hansson, Ö. and Wydrzynski, T. (1990) Current perceptions of Photosystem II, Photosy
nthesis Research 23, 131-162.
Harris, D.M. and Anderson, A.T. (1983) Concentrations, sources, and losses of H2O, C
O2, and S in Kilauean basalt, Geochimica Cosmochimica Acta 47, 1139-1150.
Hartman, H. (1975) Speculations on the origin and evolution of metabolism, Journal of
Molecular Evolution 4, 359-370.
Hauska, G., Schoedl, T., Remigy, H. and Tsiotis, G. (2001) The reaction center of green
sulfur bacteria, Biochimica et Biophysica Acta 1507, 260-277.
Heberle, J., Riesle, J., Thiedemann, G., Oesterhelt, D. and Dencher, N.A. (1994) Proton
migration along the membrane surface and retarded surface bulk transfer, Nature 370
, 379-382.
Heinen, W. and Lauwers, A.M. (1996) Organic sulfur compounds resulting from the int
eraction of iron sulfide, hydrogen sulfide and carbon dioxide in an anaerobic
aqueous environment, Origins of Life and Evolution of the Biosphere 26, 131-150.
Heinen, W. and Lauwers, A.M. (1997) The iron-sulfur world and the origins of life: Abi
otic synthesis from metallic iron, H2S and CO2: a comparison of the thiol generating
FeS/HCl(H2S)/CO2-system and its Fe0/H2S/CO2-counterpart, Proceedings Konin
klijke Nederlandse Akademie van Wetenschappen, Amsterdam, 100, 11-25.
Hemley, J.J., Cygan, G.L., Fein, J.B., Robinson, G.R. and D'Angelo, W.M. (1992) Hydr
othermal ore-forming processes in the light of studies in rock-buffered systems: I. Ir
on-copper-zinc-lead sulfide solubility relations, Economic Geology 87, 1-22.
Hennet, R.J-C, Holm, N.G. and Engel, M.H. (1992) Abiotic synthesis of amino acids un
der hydrothermal conditions and the origin of life: A perpetual phenomenon? Naturw
issenschaften 79, 361-365.
Hirsch, P.B., Hutchinson, J.L. and Tithmarsh, J.M. (1986) Voidites in diamond: evidence
for a crystalline phase containing nitrogen, Electron microscopy 11, 1703-1704.
Holme, N.G. and Charlou, J.L. (2001) Initial indications of abiotic formation of hydrocar
bons in the Rainbow ultramafic hydrothermal system, Mid-Atlantic Ridge, Earth and
Planetary Science Letters 191, 1-8.
Holmes, A. (1931) Radioactivity and earth movements, Transactions of the Geological S
ociety of Glasgow 18, 559-606.
Homann, P.H. (1987) The relations between the chloride, calcium, and polypeptide requir
ements of photosynthetic water oxidation, Journal of Bioenergetics and Biomembran
es 19, 105-123.
Horita, J. and Berndt, M.E. (1999) Abiogenic methane formation and isotopic fractionati
on under hydrothermal conditions, Science 285, 1055-1057.
Huber, C. and Wächtershäuser, G (1997) Activated acetic acid by carbon fixation on (Fe,
Ni)S under primordial conditions, Science 276, 245-247.
Huber, C. and Wächtershäuser, G (1998) Peptides by activation of amino acids with CO
on (Fe,Ni)S surfaces: Implications for the origin of life, Science 281, 670-672.
Inoue, T. and Orgel, L.E. (1983) A nonenzymatic RNA polymerase model,
Science 219, 859-862.
Ivanovsky, R.N., Krasilnikova, E.N. and Fal, Y.I. (1993) A pathway of the autotrophic
CO2 fixation in Chloroflexus aurantiacus, Archives of Microbiology 159, 257-264.
Izawa, S. and Hind, G. (1967) The kinetics of the pH rise in illuminated chloroplast susp
ensions, Biochimica et Biophysica Acta 143, 377-390.
Jacob, F. (1977) Evolution and tinkering, Science 196, 1161-1166.
Jagendorf, A.T. (1967) Acid-base transitions and phosphorylation by chloroplasts. FASE
B 26, 1361-1369.
Johnson, M.K. (1996) Iron-sulfur proteins, in R.B. King (ed.), Encyclopedia of Inorgani
c Chemistry, vol. 4, Wiley, Chichester, pp. 1896-1915.
Jormakka, M., Törnroth, S., Byrne, B. and Iwata, S. (2002) Molecular basis of proton mo
tive force: Structure of formate dehydrogenase-N, Science 295, 1863-1868.
Josse, J. (1966) Constititutive inorganic pyrophosphatase of Escherichia coli. (II) Nature
and binding of active substrate and the role of magnesium, Journal of Biological
Chemistry 241, 1948-1957.
Kamber, B.Z., Moorbath, S. and Whitehouse, M.J. (2001) The oldest rocks on Earth: tim
e constraints and geological controversies, in C.L.E. Lewis and S.J. Knell (eds.), The
Age of the
Earth:
from
4004
BC
to
AD
2002, Geological Society of London, Special Publications, 190, pp. 177-203.
Kassim, J., Baird, T. and Fryer, J.R. (1982) Electron microscope studies of iron corrosio
n products in water at room temperature, Corrosion Science 22, 147-158.
Kasting, J.F. (1993) Earth's earliest atmosphere, Science 259, 920-926.
Kasting, J.F. and Holm, N.G. (1992) What determines the volume of the oceans?. Earth
and Planetary Science Letters 109, 507-515.
Kasting, J.F., Whitmire, D.P. and Reynolds, R.T. (1993) Habitable zones around main s
equence stars, Icarus 101, 1-21.
Katsura, T. and Nagashima, S. (1974) Solubility of sulfur in some magmas at 1 atmosph
ere, Geochimica et Cosmochimica Acta 38, 517-531.
Keefe, A.D., Miller, S.L., McDonald, G. and Bada, J. (1995) Investigation of the prebioti
c synthesis of amino acids and RNA bases from CO2 using FeS/H2S as a reducing
agent, Proceedings of the National Academy of Science, USA, 92, 11904-11906.
Kell, D.B. (1988) Protonmotive energy-transducing mechanisms: some physical principl
es and experimental approaches, in C. Anthony (ed.), Bacterial Energy Transduction,
Academic Press, London, pp. 429-490.
Kelley, D.S and Früh-Green, G.L. (1999) Abiogenic methane in deep-seated mid-ocean r
idge environments: Insights from stable isotope analyses, Journal of Geophysical Re
search. 104B, 10,439-10,460.
Kelley, D.S., Karson, J.A.
et
al.
(2001) An off-axis hydrothermal vent field near the Mid-Atlantic Ridge at 30° N, Nat
ure 412, 145-149.
Klimov, V.V. Baranov, S.V. and Allakhverdiev, S.I. (1997) Bicarbonate protects the
donor side of photosytem II against photoinhibition and thermoinactivation, FEBS
Letters 418, 243-246.
Kling, G.W., Tuttle, M.L. and Evans, W.C. (1989) The evolution of thermal structure an
d water chemistry in Lake Nyos, Journal of Volcanology and Geothermal Research
39, 151-165.
Kok, B., Forbush, B. and McGloin, M. (1970) Cooperation of charges in photosynthetic
oxygen evolution — I. A linear four-step mechanism, Photochemistry and
Photobiology 11, 457-475.
Krishnamurthy, R., Arrhenius, G and Echenmoser, A. (1999a) Formation of glycolaldeh
yde phosphate from glyceraldehyde in aqueous solution, Origins of Life and Evoluti
on of the Biosphere 29, 333-354.
Krishnamurthy, R., Pitsch,
S
and
Arrhenius,
G. (1999b) Mineral induced formation of pentose-2,4-biphosphates, Origins of Life
and Evolution of the Biosphere 29, 139-152.
Lagabrielle, Y., Goslin, J., Martin, H., Thirot, J.-L. and Auzende, J.-M. (1997) Multiple ac
tive spreading centres in the hot North Fiji Basin (Southwest Pacific): a possible mod
el for Archaean seafloor dynamics? Earth and Planetary Science Letters 149, 1-13.
Laverne, C., Agrinier, P., Hermitte, D. and Bohn, M. (2001) Chemical fluxes during hydr
othermal alteration of a 1200-m long section of dykes in the oceanic crust, DSDP/O
DP hole 504B, Chemical Geology 181, 73-98.
Leja, J. (1982) Surface Chemistry of Froth Flotation, Plenum Press, New York.
Letnikov, F.A. (1997) Self-organization of formation of magmatic and hydrothermal ore
deposits, Geology of Ore Deposits 39, 261-274.
Liebl, U., Mockensturm-Wilson, M., Trost, J.T., Blankenship, R.E. and Vermaas, W. (19
93) Single core polypeptide in the reaction center of the photosynthetic bacterium He
liobacillus mobilis — structural implications and relations to other photosytems, Pro
ceedings of the National Academy of Science, USA, 90, 7124-7128.
Lister, C.R.B. (1975) On the penetration of water into hot rock, Geophysical Journal of t
he Royal Astronomical Society 39, 465-509.
Liu, S.V., Zhou, J., Zhang, C., Cole, D.R., Gajdarziska-Josifovska, M. and Phelps, T.J. (1
997) Thermophilic Fe(III)-reducing bacteria from the deep subsurface: the evolutiona
ry implications, Science 277, 1106-1109.
Ljungdahl, L.G. (1994) The acetyl-CoA pathway and the chemiosmotic generation of
ATP during acetogenesis, in H.L. Drake (ed.), Acetogenesis, Chapman and Hall,
New York, pp. 63-87.
Lydon, J.W. (1983) Chemical parameters controlling the origin and deposition of sedime
nt-hosted
stratiform
lead-zinc
deposits, Mineralogical Association of Canada, Short Course Handbook, vol. 8, pp.
175-250.
MacDermott, A.J., Tranter, G.E. and Tranter, S.J. (1992) The search for parity-violating e
nergy differences finds fruit in thiosubstituted DNA analogues, Chemical Physics Le
tters 194, 152-156.
Macleod, G., McKeown, C., Hall, A.J. and Russell, M.J. (1994) Hydrothermal and ocean
ic pH conditions of possible relevance to the origin of life, Origins
of
Life and Evolution of the Biosphere 23, 19-41.
Maisonneuve, J. (1982) The composition of the Precambrian ocean waters, Sedimentary
Geology 31, 1-11.
Majerfeld, I. and Yarus, M (1998) Isoleucine: RNA sites with essential coding sequences
, RNA 4, 471-478.
Makund, S. and Adams, M.W.W. (1991) The novel tungsten-iron-sulphur proteins of
the hyperthermophilic bacterium, Pyrococcus furiosus, Journal of Biological
Chemistry 266, 14208-14216.
Malyshev, A.I. (2001) Sulphur in high-tempeature natural processes, GSA Earth System
Processes, Global Meeting June 24-28, 2001, Programmes with Abstracts pp. 76-77.
Margulis, L., Walker, J.C.G. and Rambler, M. (1976) Reassessment of roles of oxygen a
nd ultraviolet light in Precambrian evolution, Nature 264, 620-624.
Marshall, W.L. (1994) Hydrothermal synthesis of amino acids. Geochimica et Cosmoch
imica Acta 58, 2099-2106.
Marteinsson, V.M., Kristjánsson, J.K. et al. (2001) Discovery of giant submarine
smectite cones on the seafloor in Eyjafjordur, Northern Iceland, and a novel thermal
microbial habitat, Applied and Environmental Microbiology 67, 827-833.
Martin, W. and Russell, M.J. 2003, On the origin of cells: An hypothesis for the
evolutionary transitions from abiotic geochemistry to chemoautorophic prokaryotes,
and from prokaryotes to nucleated cells. Philosophical Transactions of the Royal
Society of London 358B, in press.
Matsuno, K. (1997) A design principle of a flow reactor simulating prebiotic evolution, V
ivo Origino 25, 191-204.
McCollom, T.M. and Seewald, J.S. (2001) A reassessment of the potential for the reducti
on of dissolved CO2 to hydrocarbons during serpentinization of olivine, Geochimica
et Cosmochimica Acta 65, 3769-3778.
McCollom, T.M., Ritter, G and Simoneit, B.R.T. (1999) Lipid synthesis under hydrother
mal conditions by Fischer-Tropsch-Type reactions, Origins of Life and Evolution of
the Biosphere 29, 153-166.
McConnell, H.M., Lucas, K.T. and Weis, R.M. (1984) Periodic structures in lipid
monolayer
phase
transitions,
Proceedings of the National Academy of Science, USA, 81, 3249-3253.
McFadden, B.A. and Shively, J.M. (1991) Bacterial assimilation of carbon dioxide by th
e Calvin cycle, in J.M. Shively and L.L. Barton (eds.), Variation in Autotrophic
Life, Academic Press, New York, pp. 25-50.
Mellersh, A.R. (1993) A model for the prebiotic synthesis of peptides which throws light
on the origin of the genetic code and the observed chirality of life, Origins of Life an
d Evolution of the Biosphere 23, 261-274.
Mellersh, A.R. and Wilkinson, A-S. (2000) RNA bound to a solid phase can select an a
mino acid and facilitate subsequent amide bond formation, Origins of Life and
Evolution of the Biosphere 30, 3-7.
Michel, H. and Deisenhofer, J. (1988) Relevance of the photosynthetic reaction center fr
om purple bacteria to the structure of photosystem II, Biochemistry 27, 1-7.
Miller, S.A. and Nur, A. (2000) Permeability as a toggle switch in fluid-controlled crustal
processes, Earth and Planetary Science Letters 183, 133-146.
Mitchell, P. (1961) Coupling of phosphorylation to electron and hydrogen transfer by a
chemiosmotic mechanism, Nature 191, 144-148.
Mitchell, P. (1967) Proton-translocation phosphorylation in mitochondria, chloroplasts a
nd bacteria: natural fuel cells and solar cells, FASEB 26, 1370-1379.
Mitchell, P. (1976) Vectorial chemistry and the molecular mechanics of chemiosmotic co
upling. Power transmission by proticity, Biochemical Society Transactions 4, 399-43
0.
Mitchell, P. (1979) Keilin's respiratory chain concept and its chemiosmotic consequence
s, Science 206, 1148-1159.
Morgan, W.J. (1971) Convection plumes in the lower mantle, Nature 230, 42-43.
Morse, J.W. and Arakaki, T. (1993) Adsorption and coprecipitation of divalent metals wi
th mackinawite (FeS), Geochimica et Cosmochimica Acta 57, 3635-3640.
Mulkidjanian, A.Y. and Junge, W. (1997) On the origin of photosynthesis as inferred fro
m sequence analysis — a primordial UV-protector as common ancestor of reaction c
enters and antenna proteins, Photosynthesis Research 51, 27-42.
Müller, D., Pitsch, Kittaka, A., Wagner, E., Wintner, C.E. and Eschenmoser, A., (1990)
Mineral induced formation of sugar phosphates, Helvetica Chimica Acta 73, 1410-14
68.
Muth, G.W., Orteleva-Donnelly, L. and Strobel, S.A. (2000) A single adenosine with a n
eutral pKa in the ribosomal peptidyl transferase center, Science 289, 947-950.
Myers, C.R. and Nealson, K.H. (1988) Bacterial manganese reduction and growth with
manganese oxide as the sole electron acceptor, Science 240, 1319-1321.
Naughton, J.J., Lewis, V.A. Hammond, D. and Nishimoto, D. (1974) The chemistry of s
ublimates collected directly from lava fountains at Kilauea Volcano, Hawaii, Geochim
ica et Cosmochimica Acta 38, 1679-1690.
Neal, C. and Stanger, G. (1984) Calcium and magnesium hydroxide precipitation from al
kaline groundwater in Oman, and their significance to the process of serpentinization,
Mineralogical Magazine 48, 237-241.
Nernst,
W.
(1923) Theoretical Chemistry from the Standpoint of Avogadro's rule & Thermodyn
amics, MacMillan and Co, London.
Nissen, P., Hansen. J., Ban, N., Moore, P.B. and Steitz, T.A. (2000) The structural basis
of ribosome activity in peptide bond synthesis, Science 289, 920-930.
Ohmoto, H. Kakegawa, T. and Lowe, D.R. (1993) 3.4-billion-year-old biogenic pyrites f
rom Barberton, South Africa: sulfur isotope evidence, Science 262, 555-557.
Orgel, L.E. (2000) Self-organizing biochemical cycles, Proceedings of the National Acad
emy of Science, USA, 97, 12503-12507.
Oró, J. (1960) Synthesis of adenine from ammonium cyanide, Biochemical and Biophysi
cal Research Communications 2, 407-412.
Oró, J. and Kimball, A.P. (1961) Synthesis of purines under possible primitive Earth con
ditions 1. Adenine from hydrogen cyanide, Archives of
Biochemistry
and Biophysics 94, 217-227.
Pace, N.R. (1997) A molecular view of microbial diversity and the biosphere, Science 27
6, 734-740.
Parkes, R.J., Cragg, B.A., Bale, S.J., Getliff, J.M., Goodman, K., Rochelle, P.A., Fry, J.C.,
Weightman, A.J. and Harvey, S.M. (1994) Deep bacterial biosphere in Pacific Ocea
n sediments, Nature 371, 410-413.
Peters, J.W., Stowell, M.H.B., Soltis, S.M., Finnegan, M.G., Johnson, M.K. and Rees,
D.C. (1997) Redox-dependent structural changes in the nitogenase P-cluster,
Biochemistry 36, 1181-1187.
Phoenix, V.R., Konhauser, K.O., Adams, D.G. and Bottrell, S.H. (2001) Role of biomine
ralization as an ultraviolet shield: Implications for Archean life, Geology 29, 823-826.
Pinto, J.P., Gladstone, G.R. and Yung, Y.K. (1980) Photochemical production of formald
ehyde in Earth's primitive atmosphere, Science 210, 183-185.
Pitsch, S., Eschenmoser, A., Gedulin, B., Hui, S. and Arrhenius, G. (1995) Mineral induc
ed formation of sugar phosphates, Origins
of
Life
and
Evolution
of
the Biosphere 25, 297-334.
Pontes-Buarques, M., Tessis, A.C., Bonapace, J.A.P., Monte, M.B.M., Cortés-Lopez, G.,
de Souza-Barros, F. and Vieyra, A. (2001) Modulation of adenosine 5'-monophosph
ate adsorption onto aqueous resident pyrite: Potential mechanisms for prebiotic reacti
ons, Origins of Life and Evolution of the Biosphere 31, 343-362.
Post, J.E. and Appleman, D.E. (1988) Chalcophanite, ZnMn3O7.3H2O: New crystal-str
ucture determinations, American Mineralogist 73, 1401-1404.
Post, J.E. and Veblen, D.R. (1990) Crystal structure determinations of synthetic sodium,
magnesium, and potassium birnessite using TEM and the Rietveld method, American
Mineralogist 75, 477-489.
Pourbaix, M.J.N. (1949) Thermodynamics of Dilute Aqueous Solutions, Arnold, London
.
Pratt, J.M. (1993) Nature's design and use of catalysts based on Co and the macrocycle c
orrin ligand: 4 X 109 years of coordination chemistry, Pure and Applied Chemistry 6
5, 1513-1520.
Prescott, L.M., Harley, J.P. and Klein, D.A. (1993) Microbiology, 2nd Edition, Wm. C.
Brown Communications Inc., New York.
Price, N.J. (2001) Major Impacts and Plate Tectonics, Routledge, London.
Quayle, R.J. and Ferenci, T. (1978) Evolutionary aspects of autotrophy, Microbiological
Reviews 42, 251-273.
Ragsdale, S.W. and Kumar, M. (1996) Nickel-containing carbon monoxide dehydrogen
ase/acetyl-Co-A synthase, Chemical Reviews 96, 2515-2539.
Rahman, L. (2002) The geochemical modelling of emergent life from submarine
hydrothermal environments, Unpublished Ph.D Thesis, University of Glasgow.
Rambler, M., and Margulis, L. (1980) Bacterial resistance to ultraviolet irradiation under
anaerobiosis: Implications for pre-Phanerozoic evolution, Science 210, 638-640.
Raven, J.A. and Smith, F.A. (1981) H+ transport in the evolution of photosynthesis, Bio
Systems 14, 95-111.
Reid, C. and Orgel, L.E. (1967) Synthesis of sugars in potentially prebiotic conditions, N
ature 216, 455.
Reysenbach, A.-L. and Shock, E. L. (2002) Merging genomes with geochemistry in hydr
othermal ecosystems, Science 296, 1077-1082.
Rickard, D. (1989) Experimental concentration-time curves for the iron(II) sulphide preci
pitation process in aqueous solutions and their interpretation, Chemical Geology 78,
315-324.
Rickard, D., Butler, I.B. and Olroyd, A. (2001) A novel iron sulphide switch and its impli
cations for Earth and planetary science, Earth and Planetary Science Letters 189, 8591.
Righter, K. Drake, M.J. and Yaxley, G. (1997) Prediction of siderophile element metal-si
licate partition coefficients to 20 GPa and 2,800°C: the effects of pressure, temperatur
e, oxygen fugacity, and silicate and metallic melt compositions, Physics of the Earth a
nd Planetary Interiors 100, 115-134.
Riordan, M. and Schramm, D.N. (1991) The Shadows of creation, W.H. Freeman, New
York.
Rouse, R.C., Peacor, D.R. and Freed, R.L. (1988) Pyrophosphate groups in the structure
of canaphite, Ca2Na2PO7.4H2O: The first occurrence of a condensed phosphate mi
neral, American Mineralogist 73, 168-171.
Ruettinger, W., Yagi, M., Wolf, K., Bernasek, S. and Dismukes, G.C. (2000) O2 evolutio
n from the manganese-oxo cubane core Mn4O46 +: A molecular mimic of the photos
ynthetic water oxidation enzyme? Journal American Chemical Society 122, 10353-1
0357.
Runnegar, B. (2001) Archean sulfates from Western Australia, long thought to have been
replacements of gypsum evaporites were, in fact, originally barites, Eleventh Annual
V.M. Goldschmidt Conference, Hot Springs, Virginia, abstract.
Russell, M.J. (1973) Base-metal mineralization in Ireland and Scotland and the formatio
n of Rockall Trough, in D.H. Tarling and S.K. Runcorn (eds.), Implications of Conti
nental Drift to the Earth Sciences, Academic Press, London, vol. 1, pp. 581-597.
Russell, M.J. and Skauli, H. (1991) A history of theoretical developments in carbonate-h
osted base metal deposits and a new tri-level enthalpy classification, Economic Geolo
gy: Monograph 8, 96-116.
Russell, M.J. and Hall, A.J. (1997) The emergence of life from iron monosulphide bubbl
es at a submarine hydrothermal redox and pH front, Journal of the Geological Societ
y of London 154, 377-402.
Russell, M.J. and Hall, A.J. (1999) On the inevitable emergence of life on Mars, in J.A.
Hiscox (ed.), The search for life on Mars, Proceedings 1st UK Conference, British
Interplanetary Society, pp. 26-36.
Russell, M.J. and Hall, A.J. (2001) The onset of life and the dawn of oxygenic photosynt
hesis: Respective roles of cubane core structures [Fe4S4]2 + and transient [Mn4O4]
4 +[OCaO]2, Sixth International Conference on Carbon Dioxide Utilization, Septem
ber 9-14, 2001, Breckenridge, Colorado. Abstracts, p. 49.
Russell, M.J., Daia D.E. and Hall, A.J. (1998) The emergence of life from FeS bubbles a
t alkaline hot springs in an acid ocean, in J. Wiegel and M.W.W. Adams (eds.), Ther
mophiles: The Keys to Molecular Evolution and the Origin of Life, Taylor and Franc
is, Washington, pp. 77-125.
Russell, M.J., Hall, A.J., Cairns-Smith, A.G. and Braterman, P.S. (1988) Submarine hot
springs and the origin of life. -correspondence- Nature 336, 117.
Russell, M.J., Daniel, R.M., Hall, A.J. and Sherringham, J. (1994) A hydrothermally prec
ipitated catalytic iron sulphide membrane as a first step toward life, Journal of Molec
ular Evolution 39, 231-243.
Rutherford, A.W. (1989) Photosystem II, the water-splitting enzyme, Trends in Biochem
ical Science 14, 227-232.
Sanchez, R.A., Ferris J.P. and Orgel, L.E. (1967) Studies in prebiotic synthesis II. Synth
esis of purine precursors and amino acids
from
aqueous
hydrogen
cyanide, Journal of Molecular Biology 30, 223-253.
Sauer, K. and Yachandra, V.K. (2002) A possible evolutionary origin for the Mn4 cluster
of the photosynthetic water oxidation complex from natural Mn2 precipitates in the
early ocean, Proceedings of the National Academy of Sciences, USA, 99, 8631-8636.
Schoonen, M.A.A. and Barnes, H.L. (1997) Chemical and physical data for hydrotherma
l systems, in H.L. Barnes (ed.), Geochemistry of Hydrothermal Ore Deposits, John
Wiley and Sons, New York, pp. 937-962.
Schulte, M. D. and Shock, E. L. (1995) Thermodynamics of Strecker synthesis in hydrot
hermal systems, Origins of Life and Evolution of the Biosphere 25, 161-173.
Schulte, M. D. and Rogers, K.L. (in press) Thiols in hydrothermal solution: Standard pa
rtial molal properties and their role in the organic geochemistry of hydrothermal envir
onments, Geochimica et Cosmochimica Acta.
Schwartz, A.W. and Bakker, C.G. (1989) Was adenine the first purine? Science 245, 110
2-1104.
Schwartz, A.W. and De Graaf, R.M. (1993) The prebiotic synthesis of carbohydrates: a r
eassessment, Journal of Molecular Evolution 36, 101-106.
Schwartz, A.W. and Goverde, M. (1982) Acceleration of HCN oligomerization by forma
ldehyde and related compounds: Implications for prebiotic synthesis, Journal of Mol
ecular Evolution 18, 351-353.
Sephton, M.A. (2001) Life's sweet beginnings? Nature 414, 857-858.
Seward, T.M. and Barnes, H.L. (1997) Metal transport by hydrothermal ore fluids,
in H.L. Barnes (ed.) Geochemistry of Hydrothermal Ore Deposits, John Wiley and
Sons, New York, pp. 435-486.
Seyfried, W.M. and Bischoff, J.L. (1981) Experimental seawater-basalt interaction at 30
0°C, 500 bars: Chemical exchange, secondary mineral formation, and implications for
transport of heavy metals, Geochimica et Cosmochimica Acta 45, 135-147.
Shapiro, R. (1986) Origins: A Skeptic's guide to the Creation of Life on Earth, Heinema
nn, London.
Shock, E.L. (1990) Geochemical constraints on the origin of organic compounds in hydr
othermal systems, Origins of Life and Evolution of the Biosphere 20, 331-367.
Shock, E.L. (1992) Chemical environments of submarine hydrothermal systems, Origins
of Life and Evolution of the Biosphere 22, 67-107.
Shock, E.L. (1996) Hydrothermal systems as environments for the
emergence of life, in Evolution of Hydrothermal Ecosystems on
Earth (and Mars?), CIBA Foundation Symposium, London, No. 2
02, pp. 40-52.
Siegel, D.A., McGillicuddy, D.J. and Fields, E. (1999) Mesoscale eddies, satellite altimet
ry, and new production in the Sargasso Sea, Journal of Geophysical Research 104C,
13,359-13,379.
Sigurdsson, H., Devine, J.D., Tchoua, F.M., Presser, T.S., Pringle, M.K.W. and Evans,
W.C. (1987) Origin of the lethal gas burst from Lake Monoun, Cameroon, Journal o
f Volcanology and Geothermal Research 31, 1-16.
Simakov, S.K. (1998) Redox state of Earth's upper mantle peridotites under the ancient c
ratons and its connection with diamond genesis, Geochimica et Cosmochimica Acta
62, 1811-1820.
Smith, J.V. (1981) The first 800 million years of the Earth's history, Royal Society of Lon
don Philosophical Transactions 301A, 401-422.
Snow, J.E. and Dick, H.J.B. (1995) Pervasive magnesium loss by marine weathering of
peridotite, Geochimica et Cosmochimica Acta 59, 4219-4235.
Sowerby, S.J. and Heckl, W.M. (1998) The role of self-assembled monolayers of the pu
rine and pyridine bases in the emergence of life,Origins of Life and Evolution of
the Biosphere 28, 283-310.
Steigerwald, V.J., Beckler, G.S. and Reeve, J.N. (1990) Conservation of hydrogenase an
d polyferredoxin structures in the hyperthermophilic Archaebacterium Methanother
mus fervidus, Journal of Bacteriology 172, 4715-4718.
Ström, T., Ferenci, T. and Quayle, R.J. (1974) The carbon assimilation pathways of Meth
ylococcus capsulatus, Pseudomonas methanica and Methylosinus trichosporium (O
B3B) during growth on methane, Biochemical Journal 144, 465-476.
Summit, M. and Baross, J.A. (2001) A novel microbial habitat in the mid-ocean ridge su
bseafloor, Proceedings of the National Academy of Sciences, USA, 98, 2158-2163.
Tessis, A.C., Penteado-Fava, A., Pontes-Buarques, M., de Amorim, H.S., Bonapace, J.A.
P., de Souza-Barros, F., Monte, M.B.M. and Vieyra, A. (1999) Pyrite suspended in a
rtificial sea water catalyzes hydrolysis of adsorbed ATP: Enhancing effect of acetate,
Origins of Life and Evolution of the Biosphere 29, 361-374.
Thauer, R.K., Jungermann, K. and Decker, K. (1977) Energy conservation in chemotrop
hic anaerobic bacteria, Bacteriological Reviews 41, 100-180.
Trifonov, E.N. (2000) Concensus temporal order of amino acids and evolution of the trip
let code, Gene 261, 139-151.
Trifonov, E.N., Kirzhner, A., Kirzhner, V.M., and Berezovsky, I.N. (2001) Distinct stage
s of protein evolution as suggested by protein sequence analysis, Journal of Molecul
ar Evolution 53, 394-401.
Trincher, K.S. (1965) Biology and Information: Elements of Biological Thermodynamic
s, Consultants Bureau, New York.
Turcotte D.L. (1980) On the thermal evolution of the Earth, Earth and Planetary Science
Letters 48, 53-58.
Van Walraven, H.S., Hollander, E.E., Scholts, M.J.C. and Kraayenhof, R. (1997) The H
+ /ATP ratio of the ATP synthetase from the cyanobacterium Synechoccus 6716 varie
s with growth temperature and light intensity, Biochimica et Biophysica Acta 1318, 2
17-224.
Vargas, M., Kashefi, K., Blunt-Harris, E.L. and Lovley, D.R. (1998) Microbial evidence f
or Fe(III) reduction on early Earth, Nature 395, 65-67.
Vassiliev, I.R., Antonkine, M.L. and Golbeck, J.H. (2001) Iron-sulfur clusters in type I r
eaction centers, Biochimica et Biophysica Acta 1507, 139-160.
Vaughan, D.J. and Craig, J.R. (1978) Mineral Chemistry of Natural Sulfides, Cambridge
University Press.
Vermaas, W.F.J. (1994) Evolution of heliobacteria: Implications for photosynthetic
reaction center complexes, Photosynthesis Research 41, 285-294.
Vermaas, W.F.J. (2003) Photosynthetic reaction centers, antenna complexes, chlorophyll
-binding proteins, gene duplication and divergence, sequence alignment. Encyclopedi
a of Life Sciences, Nature Publishing Co., in press and http://www.els.net.
Voet, A.B. and Schwartz, A.W. (1982) Uracil synthesis via HCN oligomerization, Origin
s of Life 12, 45-49.
Vogelsonger, K.M., Holloway, J,R., Dunn, E.E., Dalla-Betta, P.J. and O'Day, P.A. (2001)
Experimental abiotic synthesis of methanol in seafloor hydrothermal systems during
dyking events, Chemical Geology 180, 129-139.
Volbeda, A., Charon, MH., Piras, C., Hatchikian, E.C., Frey, M. and Fontecilla-Camps, J.C. (1995) Crystal st
ructure of the nickel-iron hydrogenase from Desulfovibrio gigas, Nature 373, 580-5
87.
Von Damm, K.L. (1990) Sea floor hydrothermal activity: Black smoker chemistry and c
himneys, Annual Review of Earth and Planetary Sciences 18, 173-204.
Von Damm, K.L. (2000) Chemistry of hydrothermal vent fluids from 9°-10°N, East Paci
fic Rise: "Time zero", the immediate posteruptive period, Journal of Geophysical Res
earch 105B, 11,203-11,222.
Wächtershäuser, G. (1988) Pyrite formation, the first energy source for life: A hypothesi
s, Systematic Applied Microbiology 10, 207-210.
Wächtershäuser, G. (1998) Towards a reconstruction of ancestral genomes by gene clust
er alignment, Systematic Applied Microbiology 21, 473-477.
Walker, J.C.G. (1985) Carbon dioxide on the early Earth, Origins of Life and Evolution
of the Biosphere 16, 117-127.
Walker, J.C.G. and Brimblecombe, P. (1985) Iron and sulfur in the pre-biological ocean,
Precambrian Research 28, 205-222.
Walter, M. (1983) Archaean stromatolites: Evidence for the Earth’s earliest benthos, in J.
W. Schopf (ed.), Earth’s Earliest
Biosphere:
Its Origin and Evolution, Princeton University Press, New Jersey, pp. 187-213.
Weber, A.L. (1992) Prebiotic sugar synthesis:
Hexose
and
hydroxy
acid
synthesis from glyceraldehyde catalyzed by iron(III) hydroxide oxide, Journal of Mo
lecular Evolution 35, 1-6.
Weber, A.L. (2001) The sugar model: Catalytic flow reactor dynamics of pyruvaldehyde
synthesis from triose catalyzed by poly-L-lysine contained in a dialyzer, Origins of L
ife and Evolution of the Biosphere 31, 231-240.
Westheimer, F.H. (1987) Why nature chose phosphates, Science 235, 1173-1178.
Whitehead, R.E.S., Davies, J.F. and Goodfellow, W.D. (1990) Isotopic evidence for hyd
rothermal discharge into anoxic seawater, Sudbury basin, Ontario, Canada, Chemical
Geology (Isotope Science Section) 86, 49-63.
Wilde, S.A., Valley, J.W., Peck, W.H. and Graham, C.M. (2001) Evidence from detrital z
ircons for the existence of continental crust and oceans on the Earth 4.4 Gyr ago, Nat
ure 409, 175-178.
Williams, R.J.P. (1961) Functions of chains of catalysts, Journal of Theoretical Biology
1, 1-13.
Wimberly, B.T., Broderson, D.E., Clemons, W.M., Morgan-Warren, R.J., Carter, A.P., V
onrheln, C., Hartsch, T. and Ramakrishnan, V. (2000) Structure of the 30S ribosomal
subunit, Nature 407, 327-339.
Winget, G.D., Izawa, S. and Good, N.E. (1965) The stoichiometry of photophosphorylat
ion, Biochemical and Biophysical Research Communications 21, 438-443.
Wong, J.T. (1975) A co-evolution theory of the genetic code, Proceedings of the Nationa
l Academy of Science, USA, 72, 1909-1912.
Wood, H.G. (1985) Inorganic pyrophosphate and pyrophosphates as sources of energy,
Current Topics in Cellular Regulation 26, 355-369.
Woods, R. (1976) Electrochemistry of sulfide flotation, in M.C. Furstenau (ed.) Flotatio
n: A.M. Gaudin Memorial Volume, American Institute of Mining, Metallurgical, and
Petroleum Engineers, Inc. New York, vol. 1, pp. 298-333.
Yachandra, V.K., Sauer, K. and Klein, M.P. (1996) Manganese cluster in photosynthesis
: Where plants oxidize water to dioxygen, Chemical Reviews 96, 2927-2950.
Yamagata, Y., Wanatabe, H., Saitoh, M. and Namba, T. (1991) Volcanic production of po
lyphosphates and its relevance to prebiotic evolution, Nature 352, 516-519.
Yamagata, Y., Inoue,
H.,
and
Inomata,
K. (1995) Specific effect of magnesium ion on 2',3'-cyclic AMP synthesis from aden
osine and trimetaphosphate in aqueous solution, Origins of Life and Evolution of the
Biosphere 25, 47-52.
Yarus, M. (1988) A specific amino acid binding site composed of RNA, Science 240, 17
51-1758.
Yarus, M. (1989) Specificity of arginine binding by the Tetrahymena intron, Journal of
Molecular Evolution 28, 980-988.
Yarus, M. (2000) RNA-ligand chemistry: A testable source for the genetic code, RNA 6,
474-484.
Yocum, C.F. (1991) Calcium activation of photosynthetic water oxidation, Biochimica
et Biophysica Acta 1059, 1-15.
Zachara, J.M., Kukkadapu, R.K., Frederickson, J.M., Gorby, Y.A. and Smith, S.C. (2002
) Biomineralization of poorly crystalline Fe(III) oxides by dissimilatory
metal
reducing bacteria (DMRB), Geomicrobiology Journal 19, 179-207.
Zubay, G. and Mui, T. (2001) Prebiotic synthesis of nucleotides, Origins of Life and Evo
lution of the Biosphere 31, 87-102.