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Geochemical Connections
to Primitive Metabolism
Deep hydrothermal
“black smokers” may
promote chemical
reactions that were
important in
life’s origins.
George D. Cody 1
M
any microorganisms make extensive use of transition metal sulfide
clusters in their metabolic chemistry. Similarly, transition metal
sulfide minerals, e.g., pyrrhotite and pyrite, have the potential to
provide the essential catalytic chemistry for Earth’s earliest life. Experiments
reveal that transition metal sulfides have the capacity to both catalyze and,
in some cases, participate in organosynthetic reactions that bear similarity
to modern biosynthetic pathways. These experiments are buttressed by
recognition of natural cases of extensive abiotic organosynthesis in the
Earth’s crust—reactions that could have provided the first life with a large
complement of functionally useful protobiological organic compounds.
KEYWORDS: metabolism, biosynthesis, biocatalysis, origin of life, biogenesis
INTRODUCTION
At present there is no completely satisfactory theory for the
origin of life. Several origins hypotheses focus on the identifiable qualities of life, e.g., information and replication, as
in the case of the RNA world hypothesis, and early biological energy conversion, as in the case of the “metabolic”
theories of life. The metabolic perspective rests on the fact
that all life requires a source of energy. In the absence of
light energy, life must use the natural chemical potential
derived from chemical disequilibrium in the environment.
Kinetic barriers that inhibit thermodynamic equilibrium
endow the natural environment with ample sources of
chemical potential energy that could be exploited for
organosynthesis, provided that catalysts exist to promote
such reactions. It is intriguing to consider whether certain
minerals may have provided catalytic function for Earth’s
earliest life.
TRANSITION METAL SULFIDES
AND METABOLISM
In the metabolism-first scenario of life’s origins, the first
cells were “chemoautotrophs” (see Table 1). It is worthwhile to consider how these microorganisms survive based
on simple chemical disequilibria alone. In hydrogen-based
subsurface microbial ecosystems, certain anaerobic
microorganisms, e.g., the methanogens, extract energy and
synthesize biomolecules by exploiting the natural thermodynamic disequilibrium of coexisting CO2 and H2
(Gottschalk 1986). Methanogenic microorganisms utilize a
complex array of metallo-enzymes to catalyze the reduction of CO2 selectively towards the formation of useful
biochemical products. The primary carbon-fixing pathway
involves the production of the energy-rich molecule acetylcoA (Lengeler et al. 1999).
TABLE 1
SOME
TERMS RELATED TO THE METABOLISM
OF MICROBES
Metabolism
The network of chemical reactions by which
cells process matter and energy from their
environment
Autotroph
A cell that manufactures its own biomolecules
from small molecules
Chemoautotroph
An autotroph that harvests the chemical energy
of rocks and other chemicals in disequilibrium in
the environment
Methanogen
A cell that generates methane as a byproduct
of metabolism
Enzyme
A chemical (usually a protein) that catalyzes
a biochemical reaction
Synthase
An enzyme that helps to assemble two smaller
molecules into a larger molecule
Co-enzyme
An organic molecule (not a protein) that helps
a protein enzyme
Acetyl-coA
An important metabolic coenzyme
(gram formula weight ~ 800)
Organosynthesis
Natural reactions that produce organic molecules
Biosynthesis
Biological reactions that produce bio-organic
molecules
Prokaryote
A generic name for single-celled organisms
that do not have a nucleus
Mitochondria
The energy generating element in eukaryotic cells
1 Geophysical Laboratory, Carnegie Institution of Washington,
5251 Broad Branch Rd NW, Washington, DC 20015, USA
E-mail: [email protected]
ELEMENTS, VOL. 1,
PP
139–143
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According to these hypotheses, Earth’s earliest life was
derived from abiotic reactions catalyzed by transition metal
sulfide minerals. The vestiges of this non-enzymatic stage
of biology are preserved today in multitudes of critical
metabolic metallo-enzymes. Two notable hypotheses
include Wächtershäuser’s iron-sulfur world (Wächtershäuser 1988, 1990, 1992) and Russell and Hall’s iron-sulfur membrane model (Russell et al. 1988, Russell and Hall
1997). Both proposals predict that life emerged as a direct
consequence of chemical reactions derived from the interaction of reduced fluids (crustal and/or mantle-derived)
with reactive and catalytic transition metal sulfides. One of
the essential differences between these hypotheses and
those that preceded them is the idea that Earth’s first
organism was an autotroph, i.e., a life form capable of synthesizing all of its biomolecular constituents from simple
inorganic compounds such as CO2, NH3, H2S, and PO4-3.
In 1988 German chemist and patent lawyer Günter
Wächtershäuser proposed that pyrite formation provided a
viable energy source for Earth’s first life, via the reaction of
iron monosulfide and hydrogen sulfide to produce pyrite
and hydrogen:
FeS + H2S à FeS2 + H2
A simplified representation of catalytic pathways of the
acetyl-coA synthase complex. The left reaction pathway
sequentially reduces CO2 to a tetrahydrofolate (THF) bound methyl
group. This methyl group is transferred to a cobalt cobalamin cofactor
and then to a Ni-X-Fe4S4 cluster (where X = sulfur and possibly a second transition metal). The right reaction pathway first promotes the
water-gas shift reaction reducing CO2 to CO by utilizing a second NiX-Fe4S4 cluster. Carbonyl migration and insertion between the Ni-CH3
bond yields the acetyl group. Transfer of the acetyl group first to the
thiol end of cofactor A yields acetyl-coA.
FIGURE 1
This exergonic (energy-releasing) reaction has the
potential to drive otherwise endergonic (energy-consuming) reactions, such as the biologically important reduction of CO2 to form formic acid:
CO2(aq) + FeS + H2S à HCOOH + FeS2 + H2O
Catalytic transition metal sulfide clusters such as Fe4S4 are
essential to the chemistry required for acetyl-coA synthesis.
One key reaction pathway towards acetyl-coA synthesis
(FIG. 1) leads to the progressive reduction of CO2, ultimately
to a transferable methyl group (CH3), while the second
pathway promotes the reduction of CO2 to CO. The two
reaction pathways join at the point where a methyl group
is transferred, first to a cobalt atom and ultimately to a
nickel atom in a Ni-X-Fe4S4 cluster, where X indicates sulfur and possibly a second transition metal (e.g., Qiu et al.
1994; Doukov et al. 2002).
One reason why transition metals play such a prominent
role in acetyl-coA synthase is the high bonding affinity of
CO for transition metals (Fe, Co, and Ni in particular). The
electronic configuration of CO and transition metals allows
for considerable sharing of charge, hence the formation of
a weak metal–carbon bond. Vibrational spectroscopy
reveals that the bond of CO to Fe is stronger than to that of
Co or Ni. That extant life chooses to use Fe, Co, and Ni (and
Cu) in acetyl-coA may thus reflect a fine tuning of the catalytic function of the enzyme complex.
Transition metals such as Fe, Co, and Ni play a critical role
in numerous metabolic strategies in all chemoautotrophic
microbes. Other examples of enzymes that rely on transition metals and sulfur include (1) nitrogenases, which use
Mo, Fe, and S to reduce N2 to NH3; (2) hydrogenases, which
employ Fe, Ni, and S to derive electrons from H2 to H+; and
(3) aldehyde oxidoreductase enzymes, which use W and
Mo to interconvert organic aldehydes and acids via electron transfer.
TRANSITION METAL SULFIDES
AND THE ORIGIN OF LIFE
The ubiquitous role of transition metals and sulfur in key
microbial enzymes has led to hypotheses proposing that
sulfide minerals act as catalysts in organosynthesis.
ELEMENTS
(1)
(2)
Wächtershäuser postulated that the formation of pyrite
would provide a catalyst to drive a broad range of essential
protobiochemical reactions (Wächtershäuser 1992).
Perhaps the most imaginative aspect of Wächtershäuser’s
iron-sulfur world hypothesis was the proposal that Earth’s
first organism existed not encapsulated in a roughly spherical cellular membrane, but rather protected from the environment by a half membrane on the surface of pyrite. He
proposed that such an organism—the progenitor of all
modern cells—eventually detached from the pyrite surface,
taking with it the metabolic functionality it “learned” on
the pyrite surface.
British geochemists Michael Russell and Allan Hall (1997)
have developed an alternative hypothesis regarding the
role of transition metal sulfides in the origin of life. Their
theory postulates that the early Hadean oceans were warm,
mildly acidic, and relatively rich in dissolved Fe2+ and Ni2+.
They propose that hydrothermal fluids generated within
the ancient Hadean oceanic crust would have been highly
alkaline, hot, rich in bisulfide, and reduced. Where these
hydrothermal exhalations mixed with ocean water at the
sea floor, reaction of the bisulfide with dissolved base
metals would have resulted in the rapid precipitation of
transition metal sulfides. Russell and Hall propose that iron
sulfide bubbles formed at the sites of mixing, and that these
bubbles might have served as primitive membranes. The
purported advantage afforded by the FeS-membrane theory
is that the membrane naturally separates a low pH exterior
fluid from a high pH reduced interior fluid. Appealing to
the comparison of cell membrane function in mitochondria and certain prokaryotes, Russell and Hall note that the
presence of both pH gradients and Eh gradients would have
allowed these membranes to support processes akin to
electron-transport mediated chemistry in modern cells.
One significant difference between Wächtershäuser’s
model and that of Russell and Hall is that the latter does
not utilize oxidation of FeS as an energy source, nor does it
invoke pyrite as a catalytic agent for organosynthetic
reaction. Rather, Russell and Hall propose that the FeS
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membrane served a function similar to the hydrogenase
and acetyl-coA enzymes, by catalytically converting the
chemical potential of H2 + CO2 into biological energy generation and biochemical synthesis.
MINERAL-CATALYZED ORGANIC SYNTHESIS
Does mineral-catalyzed organic synthesis occur in nature?
Barbara Sherwood Lollar and coworkers (2002) presented
perhaps the most convincing evidence for locally extensive
abiotic organosynthesis with their observations of hydrocarbon-rich gases, including methane, ethane, propane,
and butane. These gases, collected from hard-rock terrains
of the Canadian Shield in close proximity to the ancient
Kidd Creek volcanogenic massive sulfide deposits, were
unambiguously identified as abiotic based on their distinctive distribution of stable carbon and hydrogen isotopes.
Deep-sea hydrothermal vents also are known to emit large
quantities of methane derived from abiotic reduction of
CO2 during the aqueous alteration of basalt and related
rocks (Kelley et al. 2001). This so-called serpentinization
reaction, wherein anhydrous olivine [(Mg,Fe)2SiO4] is converted to the hydrous mineral serpentine [Mg3Si2O5(OH)4]
and magnetite (Fe3O4), has the capacity to generate copious
quantities of hydrogen as a by-product (Berndt et al. 1996).
The reactions most likely responsible for these natural
hydrocarbon syntheses are Fischer-Tropsch Type reactions
(FTT), by which carbon atoms in CO groups sequentially
bind to a catalytic surface, are reduced by hydrogen, and
are added to an elongating hydrocarbon chain (FIG. 2). The
concentrations of hydrocarbons measured naturally by
Sherwood Lollar et al. (2002) and generated experimentally
by Berndt et al. (1996) are plotted against carbon number
(1 = methane, 2 = ethane, 3 = propane, etc.) in FIGURE 3. The
power law relationships exhibited in both cases are characteristic of FTT synthesis, suggesting that surface catalysis is
responsible for the observed hydrocarbons.
The log of the concentration of chain-like aliphatic
hydrocarbons and alkane thiols as a function of the number and carbon atoms. Note that the data of Berndt et al. (1996) and
Heinen and Lauwers (1996) are in log nanomoles, whereas the data of
Sherwood-Lollar et al. (2002) are in log %.
FIGURE 3
Also plotted in Figure 3 is an intriguing series of chain-like
organic molecules called alkane thiols, which were generated in a very different experiment. To test one of
Wächtershäuser’s central postulates, Heinen and Lauwers
(1996) performed a series of reactions using FeS, H2S, and
water, blanketed by an atmosphere of N2/CO2 or pure CO2,
and demonstrated the apparently facile reduction of CO2 to
form alkane thiols coincident with the formation of pyrite.
The predominant product was methane thiol (CH3SH), followed by a series of alkane thiols up to the 5-carbon pentane thiol. Heinen and Lauwers reported that, following
the reaction, a “silvery” floating layer, predominantly
pyrite, formed. It is intriguing that the relationship
between yield of alkane thiol and carbon number shown in
Figure 3 is also consistent with a surface-catalyzed FTT
process. The most likely site of the reaction was on the
newly formed pyrite. Thus, iron sulfides are apparently also
capable of promoting FTT synthesis reactions.
The FTT reaction, however, is not immediately obvious as a
useful starting point for chemistry that may have benefited
the origins of life. Indeed, the facile conversion of CO2 and
H2 to form methane leaves one in a difficult predicament
for subsequent organosynthetic reactions because methane
is not particularly useful in jump-starting metabolism. The
formation of partially oxidized carbon species like alkane
thiols, on the other hand, leaves open the possibility for
much more interesting prebiotic chemistry.
EXPERIMENTAL EXPLORATION OF METAL
SULFIDE-PROMOTED REACTIONS
A schematic representation of the catalytic, FischerTropsch Type (FTT) reduction of CO on a hypothetical
transition metal solid, where the transition metal atoms are shown in
purple and non-metal atoms are shown in green. A sequence of carbonyl insertion followed by reduction by H2 leads to progressive hydrocarbon chain growth.
FIGURE 2
ELEMENTS
Wächtershäuser’s groundbreaking hypothesis has inspired
numerous experiments. Blöchl et al. (1992) and Kaschke et
al. (1994), for example, tested the reducing power of the
pyrite-forming reaction on a number of oxidized organic
molecules and convincingly demonstrated the capacity of
iron sulfide minerals to promote interesting organic reduction reactions. In order for transition metal sulfide-mediated
chemistry to have true significance to prebiotic chemistry,
however, it remained to demonstrate that these minerals
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could promote reactions that link functionalized molecules, i.e., to form macromolecules, not just aid chemical
reductions.
Keller et al. (1994) tested this aspect of Wächtershäuser’s
hypothesis by demonstrating the formation of nitrogencontaining amide bonds, which are critical to life’s biochemistry. What made Keller et al.’s reaction especially
interesting is that they relied on a reactive intermediate
molecule called a thioacid; but one cannot start with a
thioacid because such compounds are unstable in hot water
and rapidly react to form other compounds. Consequently,
thioacids must be formed “on the fly,” as reaction intermediates. To accomplish this goal, they linked reactions
wherein FeS was sulfidized with H2S in the presence of
other reactants and produced a satisfying 2% yield of
acetanilide in a matter of days.
Notwithstanding the incremental progress demonstrated
by these experimental results, the abiotic reaction that has
received the most attention was that reported by Huber and
Wächtershäuser (1997). They conceived a series of experiments designed to test whether transition metal sulfides are
capable of mimicking the CO-insertion reaction that is promoted in cells by the acetyl-coA synthase enzyme complex
(FIG. 4). Remarkably in one case, using an unidentified
mixed (Ni,Fe)S compound synthesized during the experiment, they measured a 41% conversion of methane thiol to
acetic acid, where the synthesis of acetic acid in particular
was important in that it served to demonstrate a carbonyl
inserting reaction. Huber and Wächtershäuser interpreted
this unusual catalytic enhancement by the mixed (Fe,Ni)S
phase as a consequence of CO having a greater affinity for
iron, while CH3 has a greater affinity for nickel—an interpretation similar to that proposed for the acetyl-coA synthase enzyme, itself (FIG. 4).
Other intriguing reactions are also attributed to this
(Ni,Fe)S phase, notably the formation of so-called “peptide”
bonds, by which amino acids link together to form proteins
(Huber and Wächtershäuser 1998). This formation of peptide bonds is obviously important, but is surprising because
the spontaneous condensation of amino acids to form pep-
A schematic representation of the reaction between
methane thiol (CH3SH) and carbon monoxide on a highly ordered surface of (Ni,Fe)S as proposed by Huber and
Wächtershäuser (1997). It has been proposed that this (Ni,Fe)S phase
catalyzes a carbonyl insertion reaction as follows: first, a methyl group
derived from methane thiol is transferred to a nickel atom (green). An
adjacent iron atom (blue) is carbonylated with carbon monoxide.
Carbonyl insertion leads to the formation of the nickel-bound acetyl
group. Nucleophilic attack by either hydoxyl, bisulfide, or methane
thiol yields acetic acid, thioacetic acid, or methyl thioacetate, respectively.
FIGURE 4
ELEMENTS
tides is both thermodynamically and kinetically inhibited.
Consequently, the reaction must have been coupled to
another exergonic reaction. The likely mechanism was discovered recently by Leman et al. (2004), who found that
carbonyl sulfide (COS) readily promotes the formation of
peptides from free amino acids in the absence of any transition metal sulfide species. These results appear to suggest
that the addition of CO to an aqueous solution containing
the (Ni,Fe)S phase yields COS and some carbonylated Ni-Fe
phase. As we will see, carbonylated transition metal complexes derived from metal sulfide minerals may have other
prebiotic utility.
Organometallic transition metal sulfide complexes are
readily synthesized from monosulfides, e.g., NiS, CoS, and
FeS. This fact, coupled with the successful demonstration of
(Ni,Fe)S-catalyzed carbonyl insertion reactions (Huber and
Wächtershäuser 1997), suggests another route to the formation of key metabolic molecules, such as pyruvic acid
and other so-called “alpha ketoacids”. Thus, Cody et al.
(2000) explored whether, under high pressure, reactions of
alkane thiols, carbon monoxide, and FeS might provide a
source of alpha ketoacids. Their experiments were run with
pure FeS, aqueous formic acid (HCOOH), and the volatile
9-carbon molecule, nonane thiol, at 250°C and pressures
up to 2000 atmospheres for six hours. After reaction, the
product solutions had turned a brilliant red color, and UVvisible light and Raman spectroscopy of the solutions
revealed the presence of carbonylated iron–sulfur species.
The intensity of absorption, furthermore, increased substantially with increased pressure. Analysis of the products
revealed substantial quantities of sulfur-containing organic
molecules, as well as the ten-carbon molecule, decanoic acid.
The synthesis of decanoic acid from a nine-carbon reactant
is analogous to the formation of two-carbon acetate from
one-carbon precursors by Huber and Wächtershäuser
(1997). However, in the earlier experiments, FeS did not
promote acetate synthesis. In the Cody et al. experiment, it
is likely that the site of reaction was the carbonylated
iron–sulfur clusters. Of particular interest to early, protometabolic chemistry was the detection of traces of the
alpha ketoacids, pyruvic acid, and 2-oxo undecanoic acid.
Pyruvic acid must have formed from methane thiol derived
from CO reduction. Given the severe conditions of Cody et
al.’s experiment, it is possible that the alpha ketoacids
formed via double carbonylation followed by hydrolysis.
These results taken in context with those of Huber et al.
(2003) and Leman et al. (2004) point to the possibility that
at least some transition metal sulfides react in the presence
of CO to produce new phases that either directly or indirectly afford extremely useful protometabolic reactions.
These results naturally also raise the question as to whether
any of the transition metal sulfides are actually acting as
surface catalysts. Certainly this appears to be the case for
the FTT synthesis of alkane thiols by Heinen and Lauwers
(1996). However, in the case of the carbonyl insertion reactions, the evidence is not as robust. This question has been
addressed in a pair of papers that focused on targeted carbonyl insertion reactions for the purpose of (1) identifying
a plausible protometabolic pathway to formation of familiar biological metabolic intermediates, e.g., citric acid, and
(2) assaying a broader range of transition metal sulfide minerals for their capacity to promote carbonyl insertion reactions in general.
In 2001, Cody et al. set out to test whether the transition
metal sulfides have the capacity to convert simple olefins
like propene (as are formed in Heinen and Lauwers’ 1996
experiment) to biologically important mono-, di-, and tricarboxylic acids. At each step, reactions run in the presence
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of NiS yielded the targeted product. Particularly interesting,
however, was the fact that while numerous different structural modifications, or isomers, of these products would be
expected, a high degree of isomeric selectivity was
observed. For example, while one would predict that two
different 5-carbon dicarboxylic acids would be formed,
reactions in the presence of NiS produced only one. This
high degree of selectivity is consistent with these reactions
being surface catalyzed.
Another surprising result of these experiments was that in
addition to the product carboxylic acids, partially oxidized
compound products (thiol derivatives of methyl succinic
acid) were also formed. The identity of the electron acceptor that promoted this reaction has not been determined,
but it is certainly possible that a redox coupling reaction, in
which NiS was reduced to Ni3S2, was involved. The formation of these organothiols provides support for the idea
that a protometabolic path from CO2 up to citric acid catalyzed by transition metal sulfides is plausible.
Expanding on these results, Cody et al. (2004) recently
assayed the catalytic qualities of a broad range of transition
metal sulfides for organosynthesis. This study revealed that
many transition metal sulfides, including such common
copper sulfides as chalcopyrite, bornite, and chalcocite,
provide some catalytic function. Only FeS appears to suffer
significant CO-derived dissolution; all the other transition
metal sulfides are apparently stable under the reaction
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ELEMENTS
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Natural transition metal sulfide minerals can promote a
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reaction participants. Whether and how this chemistry
may have aided the emergence of life remains a mystery. It
is clear, however, that organosynthetic reactions would
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access to a broad range of molecular building blocks by
virtue of the natural world’s capacity for abiotic organosynthesis.
ACKNOWLEDGMENTS
I gratefully acknowledge my collaborators in this area of
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Hazen, J. Scott, and the late H. Yoder. Some of the research
discussed in this paper was supported by a grant from NASA
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