Download Life in the lithosphere, kinetics and the prospects for life elsewhere

Phil. Trans. R. Soc. A (2011) 369, 516–537
doi:10.1098/rsta.2010.0232
REVIEW
Life in the lithosphere, kinetics and the
prospects for life elsewhere
B Y C HARLES S. C OCKELL*
Planetary and Space Sciences Research Institute, The Open University,
Milton Keynes MK7 6AA, UK
The global contiguity of life on the Earth today is a result of the high flux of carbon and
oxygen from oxygenic photosynthesis over the planetary surface and its use in aerobic
respiration. Life’s ability to directly use redox couples from components of the planetary
lithosphere in a pre-oxygenic photosynthetic world can be investigated by studying
the distribution of organisms that use energy sources normally bound within rocks,
such as iron. Microbiological data from Iceland and the deep oceans show the kinetic
limitations of living directly off igneous rocks in the lithosphere. Using energy directly
extracted from rocks the lithosphere will support about six orders of magnitude less
productivity than the present-day Earth, and it would be highly localized. Paradoxically,
the biologically extreme conditions of the interior of a planet and the inimical conditions
of outer space, between which life is trapped, are the locations from which volcanism
and impact events, respectively, originate. These processes facilitate the release of redox
couples from the planetary lithosphere and might enable it to achieve planetary-scale
productivity approximately one to two orders of magnitude lower than that produced
by oxygenic photosynthesis. The significance of the detection of extra-terrestrial life is
that it will allow us to test these observations elsewhere and establish an understanding
of universal relationships between lithospheres and life. These data also show that the
search for extra-terrestrial life must be accomplished by ‘following the kinetics’, which is
different from following the water or energy.
Keywords: lithosphere; iron-oxidizing bacteria; kinetics; bacteria
1. Introduction
The detection of life on other planetary bodies would provide the opportunity to
test hypotheses about the relationship between life and planetary lithospheres. It
may even be possible to find common principles that govern these relationships
and thus develop a coherent synthetic picture of the way in which life coevolves
with planetary lithospheres throughout the Universe. To achieve this, however,
*[email protected]
One contribution of 17 to a Discussion Meeting Issue ‘The detection of extra-terrestrial life and
the consequences for science and society’.
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This journal is © 2011 The Royal Society
Review. Life in the lithosphere
517
Figure 1. The extent of life on the Earth. Diagram depicting the thickness of the region in which
there is a biota in relation to the diameter of the Earth. The thickness of the Biofilm has been
increased by five times to enhance its visibility in the diagram.
requires that we first establish an understanding of the relationship between the
terrestrial lithosphere and its associated life—at the time of writing our only
known example of life in the Universe [1].
Despite the abundance of life on the Earth, its extent can hardly be described
as a ‘biosphere’ (figure 1). In the sense that a thin-walled beach ball or a classroom
geographical globe can be described as a sphere, then the term is mathematically
correct. However, from a biological perspective, the biosphere is more properly
termed a ‘biofilm’, which more accurately conveys the nature of the microbially
dominated layer of life that covers the Earth and interacts with the lithosphere.
It is consistent with the same term used to describe a layer of organisms living
on or within the surface and interacting with the mineral matrices of rocks and
even buildings (e.g. [2–14]). In this paper, I describe the totality of life on the
Earth as the Biofilm. I have capitalized it to emphasize its application to the
planetary-scale phenomenon of life. The term Biofilm also captures more exactly
the phenomenon that we seek on other planetary bodies—Biofilms within the
surface of planetary bodies interacting with their lithospheres and the planetary
atmospheres above them.
The planetary-wide diffusion of oxygen and the distribution of carbon
compounds, both produced from photosynthesis, facilitate planetary-wide
heterotrophy (the use of organic carbon compounds as an energy source), and
in large part account for the global contiguity and productivity of the Biofilm
on the Earth today. For the present-day Earth, net productivity is estimated as
approximately 1 × 1016 mol C yr−1 [15,16]. The organic acids and other metabolic
products that result from this productivity contribute to the dissolution of
Phil. Trans. R. Soc. A (2011)
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C. S. Cockell
the lithosphere, which provides nutrients, including bioessential cations, to the
Biofilm. The planetary-scale contiguity of a Biofilm is likely to be the case on any
planet where oxygenic photosynthesis has evolved. This state of affairs is not my
focus here.
Important questions are what productivity is achievable prior to the evolution
of oxygenic photosynthesis; what kinetic barriers exist to the extraction of redox
couples from the lithosphere; and what processes might facilitate the release of
biologically important redox couples?
To address these questions, this paper will focus on a group of
chemolithotrophs, that is, micro-organisms that use inorganic compounds as a
source of electron donors for growth, called the iron-oxidizing bacteria. Ironoxidizing bacteria are capable of using reduced iron, coupled with electron
acceptors (such as oxygen in the case of aerobic iron oxidation and nitrate in the
case of anaerobic iron oxidation) to conserve energy for growth. They are also
capable of carrying out iron oxidation using light ([17–28]; equations (1.1)–(1.3)).
Aerobic iron oxidation
4Fe2+ + O2 + 4H+ → 4Fe3+ + 2H2 O.
(1.1)
Anaerobic iron oxidation
+
3+
+ N2 + 6H2 O.
10Fe2+ + 2NO−
3 + 12H → 10Fe
(1.2)
Phototrophic iron oxidation
4FeCO3 + 7H2 O → CH2 O + 4Fe(OH)3 + 3CO2 .
(1.3)
Iron within rocks and life originates from stellar evolution as the last stable
product of exothermic stellar nucleosynthesis [29]. As iron is readily incorporated
at high concentrations into materials from which rocky terrestrial-type planets
are formed, and it is a product of fundamental cosmological constants [30],
then the use of iron as a source of electrons to drive energy acquisition in
planetary lithospheres is plausibly a universal process (if life exists elsewhere).
Other elements are also incorporated into rocks and can be used in energyyielding reactions, such as sulphur, although their contribution to productivity is
generally less important than iron [31]. Here attention will be given to aerobic iron
oxidation. Although this reaction (equation (1.1)) requires oxygen as the terminal
electron acceptor, and this would not be available (or it would be very localized)
on a planet where the gross atmospheric composition remains largely unaffected
by oxygenic photosynthesis, the focus here is to investigate the interactions of the
organisms with the lithosphere. Thus, the choice of iron-oxidizing micro-organism
does not influence the qualitative conclusions about the kinetic challenges that
present themselves to the use of iron bound within planetary lithospheres.
2. Biological iron oxidation: limits of the Biofilm–lithosphere interaction
(a) Continental land environments
The first hypothesis to address is that iron within rocks provides a readily
accessible source of energy for iron-oxidizing bacteria in all of the Earth’s
environments.
Phil. Trans. R. Soc. A (2011)
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Volcanic rocks (the primary igneous minerals from which the Earth
is constructed, most other minerals being formed from metamorphosis or
sedimentary processes; [32]) usually contain between 7% and 15% iron, and
most of this is available as reduced iron, either homogeneously distributed, as
in volcanic glass, or localized to specific minerals, such as pyroxenes and olivines
in crystalline rocks.
Studies of the microbial diversity of volcanic rocks by molecular methods
yield insights into the prevalence of different groups of organisms, including
iron-oxidizing bacteria. A diversity of surface volcanic rocks in Iceland have
been investigated [33–37]. Analyses of the microbial diversity of these rocks
(using 16S rRNA gene sequences) show that most of the organisms are related
to heterotrophs. For example, in basaltic glass, Actinobacteria dominated the
microbial community, which are a primarily heterotrophic phylum of bacteria
common in soils [34].
These data are consistent with those reported by others. Gomez-Alvarez
et al. [38] investigated microbial communities in volcanic deposits in Hawaii,
USA. Acidobacteria and Actinobacteria were recovered at all sites. No sequences
associated with iron-oxidizing bacteria were reported in their work. Similarly,
Ibekwe et al. [39], in studying microbial communities associated with the ash
deposits at Mount St Helens, USA, did not identify iron-oxidizing bacteria.
Despite these results, in none of these studies can one rule out iron-oxidizing taxa
among the large number of novel, uncultured and functionally uncharacterized
organisms that are found in these environments.
The difficulty in identifying micro-organisms by molecular methods is
compounded by incomplete sampling. The high number of microbial taxa in
the rocks makes it difficult to achieve complete sampling of their diversity. This
limitation can be partly overcome by direct attempts to culture iron-oxidizing
bacteria from the rocks using gradient tube methods (e.g. [40]). Attempts to
culture iron-oxidizing bacteria from many Icelandic volcanic rocks have so far
been unsuccessful (P. Wilkinson 2010, unpublished data).
Neither the lack of molecular evidence for iron-oxidizing bacteria nor
the lack of cultured organisms definitively shows the absence of these
organisms within the rocks, but it does establish adequately the qualitative
observation that the rocks are not a habitat for an abundant community of
iron-oxidizing bacteria.
(b) Continental riverine environments
Two explanations for the lack of iron-oxidizing bacteria in the volcanic rocks
might be a lack of these organisms generally in surficial materials in Iceland or the
low temperatures experienced there. Iron-oxidizing bacteria have been described
in a number of environments around the world, but most of these are deep-sea,
temperate or tropical environments [41–51].
These hypotheses can be tested by searching for the presence of iron-oxidizing
bacteria in potentially more favourable surface environments. Throughout Iceland
small streams dissect the terrain and run through basaltic watersheds carrying
the products of volcanic rock weathering. Many of them contain rocks with a
conspicuous red/orange surface coloration with evident biofilms formed on their
surfaces (C. S. Cockell 2009, unpublished data).
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C. S. Cockell
Analysis of the biofilms by scanning electron microscopy (SEM) shows
them to contain abundant iron oxide spiral-shaped stalks (figure 2) and hollow
iron oxide tubes associated with the iron-oxidizing genera Gallionella and
Leptothrix, respectively (figure 2a–c; [52–56]). The structures are produced
by the bacteria as a means to control the secretion of oxidized iron
that results from iron oxidation (equation (1.1)) and prevent bacterial selfentombment [27,28,57]. Molecular analysis of the biofilms confirms the presence
of 16S rRNA gene sequences belonging to Gallionella (figure 2d), a member of
the b-proteobacteria.
Measurements of the annual temperature regimen in a typical stream ranged
from 0.1 to 15.6◦ C during 2008. The stream did not freeze. These data support
the hypothesis that abundant iron-oxidizing bacteria can persist in cold Icelandic
environments and that physical environmental conditions or the lack of organisms
on the island are not reasons for the lack of iron-oxidizing bacteria within the
Icelandic rocks.
(c) Marine environments
The data from Icelandic streams raise the hypothesis that the presence
of abundant liquid water (compared with the interior of rocks, which
receives intermittent precipitation and snowmelt) is sufficient to generate a
favourable environment for iron-oxidizing bacteria. This hypothesis can be
further tested by examining the abundance of iron-oxidizing bacteria within
basaltic rocks in the ocean environment, where the rocks are also surrounded by
abundant water.
We examined young basalts (<200 000 yr) from the Axial Volcanic Ridge
at an ocean depth of approximately 3 km in the median valley of the MidAtlantic Ridge. The basaltic glass was a composite sample of glass that had
spalled off the rims of pillow basalt samples, collected by the Isis remotely
operated vehicle (National Oceanography Centre, Southampton, UK) during
cruise JC24 [58].
The samples exhibit a surface-weathered zone, which is composed of many
small fractures that are filled with the alteration products of volcanic glass
(figure 3) and other detritus originating from the sediments near the rocks and
the photic zone. Micro-organisms inhabit the fractures and in some cases form
biofilms on the fracture-filling material, which were clearly visualized in slices
prepared for transmission electron microscopy (TEM; figure 3c,d).
To date, we have been unable to culture iron-oxidizing bacteria from within the
rocks. Organisms we have cultured are heterotrophs associated with the ocean
environments such as Halomonas and Sulfitobacter [59]. Previous studies of the
microbial diversity of oceanic basalts have not revealed abundant sequences of
known iron-oxidizing bacteria [60–62].
Another way to assess the presence of iron-oxidizing bacteria in this
environment is to search for the depletion of iron in the basaltic glasses along
fractures. If iron-oxidizing bacteria are abundant and obtaining energy from the
rocks, then large iron depletions should be evident. Small samples of glass from
the edge of fractures were removed by focused ion beam (FIB) milling and their
elements mapped in TEM. However, there was no evidence for pervasive removal
Phil. Trans. R. Soc. A (2011)
Phil. Trans. R. Soc. A (2011)
(d)
0.05
79
65 uncultured bacterium EU801480
62 uncultured b-proteobacterium EF111171
River3-1
biofilm50
biofilm65
89
biofilm63
uncultured
bacterium
EU801838
60
River2-34
70 River2-79
99 River3-29
b-proteobacterium AB452981
83 biofilm71
River2-46
66 uncultured Comamonadaceae DQ628931
biofilm3-26
81 100 biofilm3-5
81 uncultured bacterium FJ694633
66 uncultured b-proteobacterium AJ421913
biofilm51
84 glacier bacterium AY315177
62 uncultured bacterium EU978781
63
River2-43
uncultured bacterium EF014656
98
River2-83
78 River3-4
61 River2-73
River2-9
River2-44
River2-75
86 Methylibium fulvum AB245357
100 uncultured Aquabacterium sp. EF664070
River3-5
90 uncultured bacterium FM872569
River2-4
79 71
81 River2-15
River2-61
99
92 uncultured bacterium AB240512
89 uncultured bacterium FJ612163
77 biofilm3-23
100 uncultured bacterium EU340165
River3-64
83
100 uncultured bacterium EU978769
uncultured b-proteobacterium EF612410
100 River8
88 uncultured b-proteobacterium EF663684
River2-45
75
54
biofilm56
97 uncultured bacterium EU937950
67
uncultured bacterium AB240483
100
River2-38
97 uncultured b-proteobacterium DQ450774
79
uncultured b-proteobacterium AF351236
River3-31
100 uncultured Gallionella sp. GQ390163
Gallionella ferruginea subsp. capsife...
Gallionella
98 uncultured Gallionella sp. GQ390161
biofilm10
biofilm36
100 biofilm59
biofilm42
100 biofilm62
Aquifex sp. 10H85-7C-S AB304892
sp.
Figure 2. Iron oxidizers in an Icelandic stream at Skorradalur, Western Iceland. SEM secondary electron images. (a) Image of biofilm on stream
rock surfaces showing detritus mixed with frustules of diatoms and spiral stalks of the iron-oxidizing bacterium, Gallionella sp. (scale bar, 2 mm).
(b) Close-up image of spiral stalks of iron oxides produced as waste products by Gallionella spp. (scale bar, 2 mm). (c) Tubes of iron oxides produced
by the iron-oxidizing bacterium, Leptothrix sp. (scale bar, 2 mm). (d) Phylogenetic tree (16S rDNA) showing position of Gallionella sp. in a stream
on a b-proteobacteria tree (scale bar represents number of changes per nucleotide position); Aquifex sp. (accession no. AB304892) was used as an
outgroup. ‘River’ and ‘biofilm’ refer to two sets of sequences obtained from rock surfaces.
(c)
(b)
(a)
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C. S. Cockell
(a)
(b)
(c)
(d)
Figure 3. Biofilms of organisms inhabiting Mid-Atlantic Ridge basaltic glass fractures. SEM
secondary electron images. (a) Fracture-filling material (scale bar, 20 mm) showing coccoid
organisms on the surface of material (close-up in b; scale bar, 2 mm). Transmission electron
microscopy (TEM) images. (c) TEM of biofilm on fracture-filling material (scale bar, 2 mm) shown
in close-up below. Cells are marked with arrows. (d) Close-up of representative cell in (a) within
fracture-filling material (scale bar, 200 nm).
of iron [63]. These data are consistent with the observed association of bacteria
with ferromanganese crusts on otherwise unaltered basaltic glass in the Loihi
seamount, Hawaii, reported by Templeton et al. [64].
These data do not preclude an involvement of bacteria in basaltic glass
alteration; indeed, considerable evidence exists that micro-organisms do interact
with, and alter, basaltic glass [65–74]. However, the data provide convincing
evidence that the freshly available basaltic glass does not provide a source of
iron for an abundant and thriving community of chemolithotrophs.
(d) The kinetic explanation for the data
How can these three sets of data be reconciled into a synthetic view of the
interactions of iron-oxidizing bacteria with the planetary lithosphere?
The contrast between the lack of iron-oxidizing bacteria in Icelandic basaltic
glass and their presence in Icelandic streams can be understood as a simple
kinetic problem. The basaltic glass has an iron content of approximately 13 per
cent. Assuming that aerobic iron oxidation occurs with a yield whereby 0.15
moles of reduced carbon is generated from every mole of Fe2+ oxidized [46,75]
and that a bacterium contains 3.6 × 10−14 mol C [76], then every 1 m3 of basaltic
glass can theoretically sustain approximately 2.5 × 1016 iron-oxidizing bacteria.
By contrast, the iron concentrations of typical Icelandic streams and rivers are
sub-micromolar [77,78]. Taking an optimistic upper value of 1 mM, a stream would
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sustain approximately 4 × 109 iron-oxidizing bacteria in every 1 m3 of water,
approximately seven orders of magnitude less biomass per unit volume than
basaltic glass.
However, there are two important differences between these two environments.
In the case of the basaltic glass (and all other volcanic rocks), the iron is locked
up in a silicate matrix and its release rate is very low. The release rate will
depend, inter alia, upon the hydrological regimen through the rocks, the presence
of conditions that accelerate rock weathering, such as high or low pH, and the
formation of secondary products [78–85].
Wolff-Boenisch et al. [86] calculated the release rate of major cations from
igneous glasses as a function of silica content at 25◦ C and pH 4.0. They
calculated the release rate of iron as approximately 0.003 mol m−3 yr−1 . They
assumed that the material is embedded within a soil horizon of given porosity
and glass composition. This release rate would correspond to the production
of 2.8 × 1010 cells m−3 yr−1 , if all the iron was available, or the equivalent
of approximately 2.5 × 104 cells g−1 of material. However, the low water flow
rate through surface rocks in Iceland and thus near-equilibrium conditions
that might exist in volcanic rock pore spaces coupled with the formation
of secondary products, such as palagonite in basaltic glass [80,84], account
for the lack of readily available iron to sustain iron-oxidizing bacteria over
long time periods. By contrast, although per unit volume the stream has less
available energy for the biota, the ferrous iron is readily accessible and is
constantly replenished.
These two sets of data show how the energy in the lithosphere is
generally kinetically unavailable to life, despite the thermodynamically favourable
characteristics of many rocks.
A distinction should be made here between access to iron as a nutrient and
access to iron as an energy supply. Some micro-organisms produce organic acids
and iron-chelating compounds such as siderophores that can be used to sequester
small amounts of iron from the environment for their nutrient requirements,
i.e. iron for enzymes, cytochromes, etc. (e.g. [87–92]) and it is likely that these
processes for deriving nutrients from the lithosphere evolved very early in the
history of life [16]. However, the concentrations required for these needs are much
less than those required for energy production.
It should also be observed that these data represent end-member examples and
that there are environments, other than streams, where iron-oxidizing bacteria
have been observed. Examples are acidic environments, where Fe2+ is maintained
in a reduced condition against oxidation in the present-day atmosphere
(e.g. [93–98]), neutral wetlands [46,99] and the rock–soil interface [76].
Although the data from the Icelandic streams would suggest that the presence
of water is a critical factor in enabling the kinetic limits to iron oxidation
to be overcome, the mere presence of water in contact with rocks is not
sufficient to release iron for energy production. The data from the Mid-Atlantic
Ridge shows that voluminous water in contact with basaltic glass does not
necessarily allow iron-oxidizing bacteria to derive energy from the rocks. There
are two explanations for these deep-sea observations. Firstly, although iron
released from the rocks might have the potential to become concentrated
and useful for iron oxidation reactions, in any fractures near the surface, the
iron will become diluted in ocean water within which iron is typically at
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C. S. Cockell
sub-nanomolar concentrations (e.g. [100,101]). Secondly, the flow of water may
be insufficient to drive the surface of the rocks, particularly within enclosed
fractures, far from chemical equilibrium conditions to favour further iron leaching
from the rock matrix. This latter problem would also be the case for the
terrestrial volcanic rocks in Iceland. These data must be reconciled with the
enrichment and culture of iron-oxidizing bacteria from deep ocean basalts
reported by others (e.g. [44,102–104]). Previous observations of iron-oxidizing
micro-organisms in deep ocean basaltic rocks have generally been made where
active circulation through rocks and hydrothermal systems generates sufficient
reduced iron to sustain these communities, demonstrating the importance of an
active hydrological cycle in overcoming the kinetic limitations to iron oxidation
in the deep ocean.
In summary, these data illustrate the principle that the Biofilm is limited,
often in many locations to the point of being unable to achieve productivity, in
its ability to derive energy from the lithosphere. These limitations can only be
overcome when appropriate mechanisms exist to overwhelm the kinetic barriers
to the acquisition of ferrous iron from rocks. As the data presented here show,
one mechanism to overcome the kinetic barrier is an active hydrological cycle,
which is indirectly linked to the presence of tectonism and active volcanism.
These processes can be regarded as ‘internal’ mechanisms for overcoming the
kinetic barrier. An important ‘external’ mechanism is asteroid and comet
impacts. To what extent can these processes overcome the kinetic barriers on
a planetary scale?
3. Overcoming the kinetic barrier to lithospherically derived energy
(a) Volcanic activity and tectonism
Redox couples produced by volcanic and active geochemical and hydrological
processes would have provided a diversity of energy sources on the pre-oxygenic
photosynthetic Earth [31,105–107].
The primary net productivity of the present-day Biofilm has been calculated
by a number of authors and is estimated to be approximately 1 ×
1016 mol C yr−1 [15,107] with a gross productivity around twice this [107]. The
potential productivity of the Biofilm without photosynthesis, and when iron
is derived by a direct interaction between life and the lithosphere (i.e. direct
microbe–mineral interactions), can be calculated by determining the rate of the
new formation of ocean crust each year. Bach & Edwards [108] provided an
estimate of the oceanic crust production of approximately 4 × 109 tonnes based on
the production of approximately 3 km3 yr−1 . They calculated the biomass of ironoxidizing micro-organisms (both aerobic and anaerobic) that could be generated
by this quantity of rock as approximately 1.6 × 1010 mol C yr−1 . If the assumption
of 7 per cent Fe in the rocks, as in Bach & Edwards [108], is used and the
same conversion metrics as those used for the Icelandic case above are used, a
total potential productivity of aerobic iron-oxidizing bacteria using iron directly
extracted from the rocks would be approximately 1.5 × 1012 mol C. Overall, the
productivity of the Biofilm using Fe directly extracted from rocks would be at
least six orders of magnitude less than the present-day Biofilm. This calculation
assumes that all of the ferrous iron is eventually used by a biota.
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Although this paper focuses on the iron-oxidizing bacteria, there are other
micro-organisms that can acquire energy directly from rocks. Sulphide associated
with newly formed igneous rocks can drive microbial sulphide oxidation.
Bach & Edwards calculate, based on new crust formation and average sulphide
concentrations, that these reactions may contribute a similar biomass as iron
oxidation [108]. A variety of metal-reducing micro-organisms can use metals
with multiple oxidation states to conserve energy for growth, e.g. chromium and
uranium [109–111]. However, in the case of the most abundant metal available
for reduction, Fe3+ , its contribution to iron in newly formed igneous rocks is
typically less than or equal to 7 per cent [112]. Although these groups of organisms
will, collectively, increase the productivity of the Biofilm, the productivity of
these modes of metabolism will be no greater than iron oxidation because these
substrates, like iron, must be extracted from the rock matrix; in many cases
these substrates are the secondary products of the oxidation of elements originally
released from the lithosphere anyway.
The effects of active volcanism and geochemical cycling on productivity can
be derived by calculating the productivity of a pre-oxygenic photosynthetic
Biofilm in toto, when these processes can contribute to the total productivity,
a task attempted by Canfield et al. [31]. They calculated the productivity of the
Earth approximately 3.8 Ga in the absence of oxygenic photosynthesis, deriving
separate estimates for productivity from H2 -based and S◦ -based ecosystems
and N-based anammox (anaerobic ammonium oxidation). They derived a total
productivity of 2.8 × 1014 mol C yr−1 . Some of the reactions considered are based
on the use of atmospheric gases, e.g. nitrogen, rather than direct extraction
of energy from rocks, but Canfield’s calculations give a productivity based on
Fe-based anoxygenic photosynthesis of 4 × 1015 mol C yr−1 , i.e. iron oxidation
constitutes the majority of the total global productivity that they calculate.
It should be noted that their total productivity value also includes H2 -based
ecosystems, which includes H2 generated from serpentinization reactions with
ultramafic rocks, which can be considered as an indirect lithospherically derived
energy source. However, this energy source does not yield large productivities
globally, consistent with the calculations of Sleep & Bird [106]. Canfield
et al. [31] derived their calculation of Fe-based productivity from estimates of
the Archean Fe2+ oceanic concentration and the availability of phosphorus to
support productivity. The difference between their value and the value based
only on new rock production in this paper and that by Bach & Edwards [108]
is probably accounted for by ocean circulation through the deep crust, and
by association the tectonic and volcanic activity which contributes to active
geochemical turnover and circulation in regions other than only places of new
rock formation. Circulation weathers deep rocks and makes iron available which
is then circulated into the oceans to allow for Fe-based ecosystems [113]. However,
it should be noted that the production of new crust might have been greater
on the younger hotter early Earth, which might contribute to some of the
discrepancy between the biomass calculated based on new crust formation ([108];
this paper) and the estimates based on the concentration of ferrous iron in the
Archean oceans [31].
Thus, in the presence of active tectonism and volcanism, which contributes
to geochemical turnover and an active hydrological cycle, the productivity of the
Biofilm might achieve within one or two orders of magnitude of the productivity of
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C. S. Cockell
the oxygenic photosynthetic Biofilm using just iron derived from the lithosphere
in iron phototrophy, once the kinetic barrier to the biological use of iron has been
overcome by the release of Fe2+ into the oceans.
(b) Asteroid and comet impact events
Asteroids and comets are the only extra-terrestrial phenomena capable of
delivering a localized pulse of energy into the lithosphere. They are one
of many catastrophes to which the microbial world has proven itself to be
resilient over geological time periods [114]. Impact events might therefore be
an important externally derived agent contributing to improving accessibility of
lithospherically derived redox couples. To test this hypothesis, the effects of an
asteroid or comet that has intersected with the deeper regions of the Biofilm can
be investigated.
The Chesapeake Bay Impact Structure (CBIS) is a buried 85–90 km diameter
impact structure formed approximately 35.4 Ma in the late Eocene [115–118].
It was formed in a shallow marine environment (water depth less than 350 m)
underlain by a few hundred metres of lower Tertiary and Cretaceous sediments on
top of Neoproterozoic and Paleozoic crystalline basement. The joint International
Continental Scientific Drilling Programme–United States Geological Survey
drilling project into the CBIS on the Eastern seaboard of the USA in 2005 offered
an opportunity for the first time to investigate the influence of an impact on the
Biofilm. During the drilling project, three drill cores were recovered to a depth
of 1.76 km.
The recovered core reveals a sequence of events which occurred within
approximately 15 minutes after the impact [119]. They include the formation of
a crater cavity, the deposition of impact breccias that include suevites and airfall deposits, the displacement of a large granite megablock from the edge of the
crater overlaid by avalanched sediments and ocean-resurge (tsunami) deposits
formed during the impact, and the subsequent deposition of marine sediments
over the 35 Myr since impact (figure 4). We used robust contamination control to
investigate the microbial communities through the impact structure [120].
The decline in microbial abundance through the top of the structure follows
a logarithmic function, broadly common to, but exhibiting some important
differences from, other deep subsurface sites [121]. However, from the point of
view of the discussion here, the most important feature is the effect of the impact
on the deeper microbial community (figure 4).
There is an increase in cell abundance below a granite megablock (below
1096 m) in a region of increased porosity, where the rocks contain fracture
networks caused by the impact. Following local heating to as high as 390◦ C [122],
micro-organisms must have recolonized the deeper fractured region of the
structure after temperatures dropped below the upper temperature limit for
microbial growth at 121◦ C [123]. Although we were not able to enrich ironoxidizing bacteria, molecular methods indicated the presence of the iron-reducing
genus, Geobacter, as members of the community. These micro-organisms perform
the opposite reaction to the iron oxidizers and reduce iron with organic
carbon or other electron donors. The Fe2+ concentrations at these depths,
which exceeded 5 mmol g−1 sediment [124], suggest the occurrence of microbial
iron reduction.
Phil. Trans. R. Soc. A (2011)
527
Review. Life in the lithosphere
(a)
38°
77°
76°
Maryland
Map
area
Ra
p
pa
ha
nn
oc
k
River
Chesapeake
Chesapeake Bay
impact structure
Bay
rk
Ja
Eyreville
coreholes
m
37°
es
r
ve
Ri
Annular
trough
150
300
200
250
350
400
450
300
550
600
700
750
depth below land surface (m)
450
Eocene
400
Chickahominy
650
350
diamicton
500
Calvert
250
sediment
blocks
and
diamicton
250
500
25 miles
25 km
enumerations
0
post-impact
sediments
(late
Eocene
to
Pleistocene)
post-impact
200
50
100
stratigraphy
crater
150
Miocene
100
0
0
Yorktown
50
0
Eastover
0
Virginia
North Carolina
St Mary’s
(b)
Pliocene
Norfolk
ATLA
NTIC OC
EAN
Yo
Cape
Charles
Central
crater
River
750
800
850
900
950
sediment
blocks
1000
1000
1050
1100
1150
granite
block
1200
1250
1250
1300
1350
1400
1450
1500
1550
1600
sediment
impact
breccia
(suevite
etc.)
Schist/
pegmatite
1500
1650
1700
1750
1750
0
105
106
107
microbial abudance
(per gram sediment dry weight)
108
Figure 4. (a) Location of CBIS. (b) Microbial enumerations (log abundance per gram dry weight)
through the core retrieved from the impact structure (adapted from Cockell et al. [121]). Cell
numbers shown as ‘0’ are samples with cell numbers below detection limits (less than 104 cells g−1 ).
Phil. Trans. R. Soc. A (2011)
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C. S. Cockell
Although the deep regions of the impact structure did not yield iron-oxidizing
bacteria, the data from the Chesapeake crater show how, by deeply fracturing
rocks, impact events can enhance the flow of nutrients and redox couples through
and from rocks that are otherwise inaccessible to the deeper regions of the Biofilm.
Similar impacts into basaltic targets could enhance the release of ferrous iron from
crustal rocks and the hydrological circulation to subsurface life.
Quantifying the effect of impacts on global productivity is difficult on account
of the fact that it will depend on the scale of the impactor and it is made
more uncertain by the indiscriminate target locations of impacts (unlike volcanic
regions, which can be more readily constrained). Known craters on the Earth
today probably cover an area of about 50 000 km2 [125]. Even taking into account
undiscovered craters and an impact flux 100–1000 times higher on the early
Earth than today [126], the surface area directly affected by impacts at any
given time on early Earth would not have been large. It would have been much
less than the areas affected directly or indirectly by volcanism, tectonism and the
hydrological circulation caused by these processes, particularly as higher Archean
heat flow [127,128] might imply volcanism, or the influence of volcanically
driven circulation, over more of the planetary surface than today. This might be
different on a planet with much higher impact fluxes than those experienced on
Archean Earth. Nevertheless, impacts perform an analogous process to volcanism
and tectonism in the relationship between life and its lithosphere, acting to
delocalize the availability of redox couples from the lithosphere, increasing
planetary-scale productivity.
4. A synthetic view of the Biofilm–lithosphere interaction
On a pre-oxygenic photosynthetic planet, overcoming the kinetic barrier to the
acquisition of iron as an electron donor from rocks is energetically prohibitively
costly. Any process that can drive a vigorous hydrological circulation can increase
the rock-weathering rate and release reduced iron from rocks, which can be
coupled with electron acceptors to conserve energy for growth.
The interior of the planet, where volcanism and tectonism originates, is at
too high a temperature for life. The low temperatures, desiccating conditions
and high radiation levels prevent the environment of interplanetary space from
hosting active micro-organisms [129], yet beneficial impactors originate from this
environment. Thus, the extreme environments that define the lower and upper
boundaries of the Biofilm are also the environments from which catastrophic
disturbances arise that allow the Biofilm to acquire energy from the lithosphere
more easily and to achieve greater planetary-scale productivity. The locations
of the Biofilm’s worst threats are also the source of its enhanced productivity
(summarized in figure 5).
5. The significance of extra-terrestrial life
This view of the Biofilm has implications for both the search for extra-terrestrial
life and the significance of its detection.
Phil. Trans. R. Soc. A (2011)
529
Review. Life in the lithosphere
the freezing
abyss
lithospheric austerity
searing
hades
asteroid and
comet impacts
enhanced productivity
the Biofilm
tectonism/volcanism
Figure 5. The pre-oxygenic photosynthetic Biofilm. Trapped between severe heat in the planetary
interior and the freezing temperatures of outer space, it is from the former that volcanism and
tectonic activity derive and from the latter that asteroids and comets originate, both of which
generate the circulation to release redox couples from rocks. The Biofilm’s greatest threats are also
its greatest beneficiaries.
Data show that the search for extra-terrestrial life must be guided by following
the kinetics. The data from the Mid-Atlantic Ridge show that this is not the
same as the strategy of following the water [130,131]. The basaltic glasses of the
Mid-Atlantic Rift are surrounded by an ocean of liquid water, but the release of
ferrous iron from the rocks is not sufficient to support abundant iron-oxidizing
bacteria within their fractures.
Data from the Icelandic basaltic glass show that following the kinetics is not
the same as the strategy of following the energy [132]. The rocks contain abundant
ferrous iron in contact with atmospheric oxygen and yet the kinetic barrier makes
them poor locations for iron-oxidizing bacteria.
A ‘follow the kinetics’ approach underlines the observation that habitability
may not be a matter of degree, i.e. one environment is better than another or
can support higher biomass. An Icelandic-like rock environment on Mars, for
instance, that possessed electron donors in the form of basaltic ferrous iron,
transient liquid water and electron acceptors, for example hydrogen peroxide
or perchlorate in the Martian case [133,134] and a range of other required
nutrients, may nevertheless be unable to support chemolithotrophic life deriving
energy from crustal materials, but a river or stream may be able to do so.
There can be a categorical difference between two thermodynamically favourable
environments, but only one exceeds a kinetic threshold to support a particular
metabolic niche.
The significance of the data for the detection of extra-terrestrial life is that
an opportunity will exist to test our views of the interactions of a biota
with lithospheres on another planetary body. Have other ‘life forms’ developed
hitherto unimagined means for dissolving lithospheres and acquiring energy from
rocks? Or is it the case that all pre-oxygenic photosynthetic planets suffer
lithospheric austerity alleviated by such processes as volcanism/tectonism and
impact events? Are there convergent evolutionary patterns in the mechanisms
by which life extracts energy from planetary lithospheres, as is proposed for
planetary megafauna [135]? What are the productivities of these other Biofilms
and do these productivities follow the same quantitative trends that we observe on
Phil. Trans. R. Soc. A (2011)
530
C. S. Cockell
the Earth? The detection of life on another planetary body would provide another
datum point to begin to develop a catalogue, if you will, of the variations of biotic
interactions with rocks, and thus to unravel universal relationships between life
and lithospheres.
I would like to thank the discussion meeting organizers for the opportunity to present these data.
This work was made possible by funding from the Leverhulme Trust (project no. F/00 269/N)
and the Royal Society. I thank my research group for contribution of data to this paper and John
Raven for valuable comments on the manuscript.
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