Serpentinites,
Hydrogen, and Life
Chrysotile serpentine
fibers growing on olivine
Thomas M. McCollom1 and Jeffrey S. Seewald2
1811-5209/13/0009-129$2.50
T
DOI: 10.2113/gselements.9.2.129
he process of serpentinization creates strongly reducing conditions and
produces fl uids that are highly enriched in molecular hydrogen and
methane. Some microorganisms are able to exploit these compounds
to gain metabolic energy and to generate biomass, leading to the development of biological communities based on chemical energy rather than
photosynthesis. The abundance of chemical energy and favorable conditions
for organic synthesis make serpentinites a strong candidate for the site of
the origin of life on Earth, as well as a prime target in the search for life
elsewhere in our Solar System.
SERPENTINIZATION AND
HYDROGEN GENERATION
The presence of fluids containing
high levels of H2 and CH4 is one
of the most distinctive characteristics of rocks undergoing active
serpentinization (Abrajano et al.
1988; Charlou et al. 2002; Kelley
et al. 2005). Serpentinites form
through the aqueous alteration
and hydration of rocks composed
predominantly of the minerals
KEYWORDS : chemosynthesis, hydrogen metabolism, abiotic organic synthesis,
olivine and pyroxene (i.e. ultraearly Earth, origin of life, methane
mafic rocks), and H2 and CH4 are
generated through the reduction
of water and dissolved CO2 as the
INTRODUCTION
reaction proceeds. The overall process of serpentinization
The last two decades have seen a steep increase in scientific (FIG. 1) can be portrayed by the general reaction:
research focused on serpentinites. One of the key reasons
olivine + pyroxene + H 2O → serpentine ± brucite ±
for this growing interest has been the realization that
magnetite + H2 ,
molecular hydrogen (H 2 ) and methane (CH4 ) produced
where
the
term
serpentine
represents
one
or more members
during serpentinization can be utilized by many types of
of a mineral group that includes lizardite, antigorite, and
microorganisms to gain metabolic energy. By converting
the energy into biomass, these organisms have the capacity chrysotile. Common accessory minerals found in serpentito support entire biological communities based on chemical nites include Fe- and Ni-bearing sulfides, oxides, and native
energy rather than photosynthesis. The prospect that these metal alloys. While these phases are typically present in
only small amounts, they can play critical roles in the
biological communities exist with little or no photosynthetic input suggests that they might be modern analogs of formation of CH4 and other organic compounds (Horita
and Berndt 1999) and are especially useful as indicators
communities that existed on early Earth. It is also possible
of chemical conditions during alteration (Klein and Bach
that such communities exist on other planetary bodies in
2009). Because olivine is stable in the presence of water at
our Solar System, such as Mars and Jupiter’s moon Europa,
whose surfaces appear too hostile to allow the presence of higher temperatures, serpentinization is largely restricted
to temperatures below about 330–400 ºC, depending on
photosynthetic organisms. In recent years, these ideas have
pressure (McCollom and Bach 2009).
stimulated ongoing efforts by geomicrobiologists, astrobiologists, and others to characterize the microbial populations of serpentinites and to understand their relationship
with the geochemical environment in which they live.
Here, we provide a brief overview of the geochemical
context for serpentinite-hosted biological communities,
and we summarize the results of recent investigations into
the function and composition of those biological communities. We conclude with a discussion of the potential
relationship between serpentinites and the origin and
early development of life on Earth, and the possibility
that serpentinite-hosted biological ecosystems might exist
elsewhere in our Solar System.
1 CU Center for Astrobiology & Laboratory
for Atmospheric and Space Physics
Campus Box 600, University of Colorado, Boulder
CO 80309-0600, USA
E-mail: [email protected]
2 Dept. of Marine Chemistry & Geochemistry
Woods Hole Oceanographic Institution
Woods Hole, MA 02543, USA
E LEMENTS , V OL . 9,
PP.
129–134
Olivine
mgt
brucite
serpentine
ȝP
Serpentinization of olivine in a laboratory experiment,
showing dissolution features in olivine and conversion
to fibrous serpentine (chrysotile), platy brucite, and octahedral
magnetite (mgt). Bright areas are due to charging by the electron
beam in this electron microscope image.
FIGURE 1
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A PR IL 2013
The generation of H 2 during serpentinization is a consequence of the coupling of H 2O reduction to the oxidation
of ferrous iron (FeII), derived from olivine and pyroxene,
to ferric iron (FeIII) that precipitates in mineral products, a
process that can be summarized by the expression:
2(FeIIO)
rock
+ H 2O →
(FeIII
2O3 ) rock
+ H2 .
Magnetite is often portrayed as the principal sink for FeIII
among the reaction products, but serpentine minerals
can also be a significant reservoir for oxidized Fe in many
circumstances (Evans 2008). Owing to the link between Fe
oxidation and H 2 generation, the rates and amounts of H 2
produced by rocks undergoing serpentinization is strongly
influenced by the manner in which Fe is distributed among
the mineral products (McCollom and Bach 2009).
In many serpentinites, a significant fraction of the Fe
released during the dissolution of olivine and pyroxene
is incorporated into serpentine and brucite as FeII (Evans
2008). Since any iron sequestered into these minerals as
FeII does not undergo oxidation, this reduces the overall
amount of H 2 generated. Conversely, the amount of H 2
produced is directly proportional to the fraction of iron
that is converted to Fe III and precipitates in magnetite,
serpentine, or other phases during alteration. In some
cases, FeII initially sequestered into brucite and serpentine
can subsequently become unstable as conditions change
and undergo oxidation, leading to generation of additional
H2 during later stages of alteration (Bach et al. 2006). In
natural serpentinites, there is considerable variability in
the partitioning of Fe among secondary mineral products
and in the oxidation state of Fe in the products (Evans
2008), indicating significant variability in the amounts
of H 2 generated during serpentinization under different
circumstances. Several factors may contribute to how the
distribution of Fe is regulated during serpentinization,
including equilibrium distribution of Fe among product
phases, variation in the relative thermodynamic stabilities of product minerals as a function of temperature and
pressure, reaction kinetics, and silica activity (Frost and
Beard 2007; Evans 2008; McCollom and Bach 2009).
The high H 2 concentrations that develop during serpentinization are conducive to the formation of methane and
other organic compounds from the reduction of inorganic
carbon (McCollom and Seewald 2007). The synthesis of
methane, for example, can be represented by the reaction:
CO2 + 4H2 → CH4 + 2H2O ,
which is increasingly favored by thermodynamics to form
CH4 as the abundance of H2 increases. Nevertheless, even
though the reaction is increasingly favored to proceed as
H2 accumulates during serpentinization, laboratory experiments and observations from natural systems indicate
that there are strong kinetic inhibitions to the reaction
at temperatures below about 350 °C under hydrothermal
conditions, resulting in sluggish reaction rates (Seewald
et al. 2006). As a consequence, substantial conversion of
CO2 to CH4 in serpentinites appears to require either very
long residence times, catalysis of the reaction by minerals,
or the intervention of biological organisms to promote the
reaction. Awaruite, a Ni–Fe alloy found in trace amounts
in some serpentinites, has been found to be a particularly
effective catalyst for the reduction of dissolved CO2 to CH4
(Horita and Berndt 1999), suggesting it may be a critical
contributor to CH4 generation. Other minerals found in
serpentinites, including magnetite, chromite, and Fe–Ni
sulfides, have been explored as possible catalysts in laboratory experiments, but so far, experimental simulations that
include these minerals have produced only small amounts
E LEMENTS
of CH4 and other organic compounds, indicating that their
capacity to promote carbon reduction is probably limited
(McCollom and Seewald 2007; McCollom 2013).
In addition to CH4, the formation of more complex organic
compounds is similarly favored by thermodynamics at the
elevated H2 concentrations attained during serpentinization. As with CH4, however, reaction pathways to form
these compounds require catalysts to overcome substantial
kinetic barriers, especially where the reactions involve the
formation of carbon–carbon bonds. If suitable catalysts are
present, however, the high H2 abundances in serpentinites
could lead to the abiotic synthesis of many types of organic
compounds by Fischer-Tropsch-type reactions or other
processes (McCollom and Seewald 2007; McCollom 2013).
Another distinguishing characteristic of many serpentinites is the strongly alkaline conditions that develop when
serpentinization takes place at temperatures below about
200 °C. Indeed, fluids discharged from active, low-temperature serpentinites have some of the highest pH values ever
recorded in natural systems on Earth (Mottl et al. 2003).
However, the pH of fluids during serpentinization decreases
sharply with increasing temperature, and moderately acidic
conditions can prevail at higher temperatures.
HYDROGEN AND METHANE
IN NATURAL SERPENTINITES
The close association of reducing, strongly alkaline fluids
with serpentinization fi rst came to the attention of most
scientists through the research of Barnes and coworkers,
who studied the composition of alkaline springwater
discharged from serpentinized ophiolites in California
(Barnes et al. 1967). Ophiolites represent sections of ocean
crust and upper mantle that have been thrust onto the
continents by tectonic forces, and ultramafic rocks present
within these units undergo serpentinization when exposed
to circulating groundwater. Since the original work of
Barnes, alkaline springs containing elevated H 2 and CH4
have been studied in numerous other locations around the
world, including sites in Oman, the Philippines, Turkey,
Portugal, and Canada (Schrenk et al. 2013). Springwaters
discharged from rocks undergoing active serpentinization typically have pH values well above 10 and elevated
concentrations of dissolved Ca in addition to H 2 and CH4.
As a consequence, the springs are often surrounded by
calcite (CaCO3) mineral deposits that precipitate, as CO2
from the atmosphere is absorbed into the alkaline fluids.
Groundwater flowing through rocks that have already been
completely serpentinized are also alkaline, but the fluids
typically have a pH of 9 or below and Mg replaces Ca as
a major cation.
At the relatively low pressures prevailing in subaerial
environments, the abundance of H 2 and CH4 in the fluids
often exceeds their aqueous solubility, so that groundwater discharged in alkaline springs is typically accompanied by H 2 - and CH4 -rich gas, which either bubbles
out of the springs or vents from fractures as a separate
phase (Etiope et al. 2011). In many serpentinites, there
may also be a diffusive flux of H2 and CH4 over a broad
area surrounding springs and vents, but these fluxes have
only been studied in a few locations (Etiope et al. 2011).
The relative abundance of H2 and CH4 in the gas phase
is highly variable among different sites. For example, at
the Zambales ophiolite in the Phillipines, serpentiniteassociated gases contain near equimolar abundances of H 2
(41–46 vol%) and CH4 (53–55 vol%) (Abrajano et al. 1988),
while gases from the Tekirova ophiolite, Turkey, contain
up to 93 vol% CH4 and ≤10 vol% H 2 (Etiope et al. 2011).
Relative to methane derived from other processes, such
130
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concentrations (Charlou et al. 2002; Proskurowksi et al.
2008; Lang et al. 2010). The isotopic compositions of CH4
from these systems are characterized by enrichments in the
heavy isotopes of C and H that are similar to those observed
in serpentinite-associated gases from ophiolites, supporting
an abiotic origin for the CH4 from carbon reduction during
serpentinization. In addition, the isotopic composition of
the light hydrocarbons and formate at Lost City are consistent with an abiotic source (Proskurowski et al. 2008; Lang
et al. 2010). The lack of detectable 14C in the CH4 and
other hydrocarbons indicates that the ultimate source of
carbon for these compounds is probably the mantle rather
than circulating seawater, suggesting that bicarbonate from
seawater is removed from the fluids by the precipitation
of carbonate minerals before the fluids reach the environments where CH4 formation occurs.
Hydrogen-rich fluids discharging from a deep-sea
hydrothermal system hosted in ultramafic rocks on the
Mid-Cayman Rise. The hydrothermal fluids vent through chimneylike structures composed primarily of metal sulfide minerals such as
pyrite (FeS2) and chalcopyrite (CuFeS2). Note the presence of
shrimp, which live by consuming biomass produced by the chemosynthetic microbial community. PHOTO CREDIT: NOAA O KEANOS E XPLORER
PROGRAM, M ID -C AYMAN R ISE E XPEDITION 2011
FIGURE 2
SERPENTINITE-HOSTED
MICROBIAL COMMUNITIES
as microbial metabolism and the thermal decomposition
of biogenic organic matter, CH4 observed in serpentinitehosted alkaline springs tends to be highly enriched in the
heavy stable isotopes of C and H (13C and 2H), suggesting
the CH4 is derived primarily from abiotic reduction of
inorganic carbon during serpentinization. Potential sources
of inorganic carbon in these systems include dissolved CO2
in circulating groundwater, magmatic gases, and carbonate
minerals. Serpentinite-associated gases also contain trace
quantities of low-molecular-weight hydrocarbons that may
be produced abiotically (Abrajano et al. 1988), although
in some cases their carbon isotope composition suggests a
contribution from the thermal decomposition of biogenic
organic matter (Etiope et al. 2011).
Serpentinization also occurs in submarine environments
in several different settings, including (1) areas along
the mid-ocean ridge where circulating hydrothermal
fluids interact with ultramafic rocks exposed by seafloor
spreading (FIG. 2); (2) sites distal from the ridge crest, where
ultramafic rocks from the mantle are tectonically displaced
to the near surface and interact with seawater; and (3) broad
areas along subduction zones, where fluids discharging
from the subducting slab can cause the serpentinization
of overlying ultramafic rocks in the mantle (Charlou et al.
2002; Mottl et al. 2003; Kelley et al. 2005). Despite variations in temperature, fluid flow regimes, and other physicochemical factors among these different settings, the same
basic serpentinization reactions occur in all these environments, resulting in rocks composed primarily of serpentine,
brucite, and magnetite as well as fluids enriched in H 2
and CH4. In submarine environments, however, elevated
pressures substantially increase the aqueous solubilities
of H 2 and CH4, and these compounds typically exist as
aqueous species dissolved in the fluids rather than as a
separate gas phase.
Hydrogen concentrations up to 16 mmol/kg have been
reported in hydrothermal fluids discharging at the seafloor
from serpentinizing systems, including the high-temperature (>365 ºC), acidic fluids at the Rainbow site on the
Mid-Atlantic Ridge (Charlou et al. 2002) and the more
moderate-temperature (to ~90 ºC), strongly alkaline fluids
at Lost City (Kelley et al. 2005). At both sites, aqueous
H 2 is accompanied by elevated methane concentrations
of 1–3 mmol/kg, as well as light hydrocarbons (ethane,
propane, and butane) and formate at substantially lower
E LEMENTS
The H2 and CH4 generated within serpentinites have the
capacity to provide an abundant source of metabolic energy
for microbial communities living in these systems. Many
microorganisms can extract metabolic energy from H 2
or CH4 by transferring electrons from these compounds
to external sources of electron acceptors, such as O2 and
SO 4 2- (TABLE 1). Consequently, when fluids circulating
through serpentinites are exposed to electron acceptors
present in the atmosphere or in seawater, an abundant
source of chemical energy becomes available to support
microbial communities (FIG. 3) (McCollom 2007). Other
organisms in these environments are able to make a living
by consuming H2 and CO2 already present in the fluids as
they cool from higher temperatures, allowing the organisms to occupy environments where no external source
of electron acceptors exist. Most of these organisms are
capable of using the metabolic energy gained from H2 and
CH4 to synthesize new biomass from CO2, and are referred
to as chemosynthetic microorganisms or, more formally by
biologists, chemolithoautotrophs. The biomass produced by
these chemolithoautotrophs is consumed by other organisms, which can lead to the establishment of food webs
based on chemical energy, with little or no input of organic
matter from photosynthesis.
Oxic habitats
Meso- & psychrophilic
aerobes
(H2 oxidizers,
methanotrophs, etc.)
Anoxic habitats
Chimney wall
Seawater
2°
O2
Thermophilic
anaerobes
(methanogens,
2SO4 reducers)
SO42CO2
2050°
100° 200° 300°
CH4
H2
Vent
Fluid
350°
Schematic cross section of a deep-sea hydrothermal
vent chimney, showing habitats for chemosynthetic
microorganisms produced by the mixing of H2- and CH4 -rich hydrothermal fluid with oxidized seawater (see McCollom 2007). The
thick black lines indicate the walls of a hydrothermal chimney, with
temperature zones across the wall indicated on the figure. Anoxic
habitats (those lacking dissolved O2) predominate at temperatures
above ~50 ºC, while oxic (and microoxic) habitats predominate at
lower temperatures.
131
FIGURE 3
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TABLE 1
reduction, using H 2 or CH4 from the vent fluids as a source
of electrons, also appears to be occurring in some chimneys
at Lost City (Schrenk et al. 2013).
Primary sources of chemical energy for chemosynthetic microorganisms in serpentinite environments
M ETABOLIC
ENERGY SOURCE
O VERALL
CHEMICAL REACTION
Hydrogen oxidation
H2 + ½O2 → H2O
Methanotrophy
CH4 + 2O2 → HCO3 - + H + + H2O
Methanogenesis
CO2 + 4H2 → CH4 + 2H2O
Sulfate reduction
SO 42- + 2H + + 4H2 → H2S + 4H2O
Anaerobic methane
oxidation (AMO)
SO 42- + 2H + + CH4 → CO2 + H2S + 2H2O
Investigations of the microbial communities living within
sulfide mineral chimneys formed at Rainbow and other
high-temperature (>350 ºC) deep-sea hydrothermal
systems hosted in ultramafic rocks (FIG. 2) have revealed
taxonomically diverse microbial populations that include
both biomass producers and consumers, with representatives from many different groups of bacteria and archaea
(a class of microorganisms distinct from the bacteria)
(Takai et al. 2004; Flores et al. 2011; Schrenk et al. 2013).
Chemosynthetic organisms capable of metabolizing H 2
and CH4 are prominent members of these communities,
including hydrogen oxidizers, methane-oxidizers, methanogens, and sulfate reducers (TABLE 1). Many of these organisms, particularly the methanogens, are thermophilic, with
optimal growth temperatures above 50 ºC, indicating that
they live within the interiors of the chimney structures.
Intriguingly, classes of chemosynthetic organisms such as
the methanogens are often represented by many different
species at individual hydrothermal vents, suggesting
that multiple organisms with similar metabolic requirements may be occupying slightly different microhabitats
within these systems. In addition to microbial consumers,
the chemosynthetic organisms at these sites support the
growth of macrofauna, such as shrimp and mussels, who
either graze on the microbial biomass or host symbiotic
chemosynthetic microorganisms that utilize H 2 and CH4
within their tissues (FIG. 2) (Petersen et al. 2011).
The composition of the microbial communities at ultramafic-hosted hydrothermal systems is distinctly different
from that of deep-sea hydrothermal systems hosted by
basaltic rocks, where organisms that oxidize hydrogen
sulfide (H 2 S) dominate the chemosynthetic population
(Flores et al. 2011). These differences reflect the relative
abundance of electron donors at the sites, with fluids at
basalt-hosted systems containing substantially higher levels
of H2 S and lower levels of H 2 and CH4 than at ultramafichosted sites (McCollom 2007). Nevertheless, the lower
amounts of H 2 and CH4 present in basalt-hosted systems
still support chemosynthetic organisms capable of utilizing
these compounds, and there is considerable overlap in the
microbial groups that utilize these compounds in the two
types of systems.
In stark contrast to the high-temperature systems, the
moderately hot (<90 ºC) vents at Lost City support a
much less diverse microbial community, with some sites
dominated by a single species of archaea from the methanosarcinales (Schrenk et al. 2004, 2013). The extremely
low diversity of the microbial communities at Lost City is
probably attributable to the strongly alkaline pH and very
low inorganic carbon levels caused by the precipitation of
carbonate minerals throughout the system. The dominant
organisms in these communities appear to be involved
in either methanogenesis or methane oxidation, but their
metabolic abilities remain uncertain because they have
not yet been cultured in the laboratory. Microbial sulfate
E LEMENTS
Serpentinite-hosted alkaline springs on land likely support
microbial communities as well, but the microbiology
of these systems is just now beginning to be explored.
Recent metagenomic analyses indicate that chemosynthetic Betaproteobacteria that oxidize H 2 as their source
of metabolic energy are prominent members of serpentinite-hosted alkaline springs in Canada, and closely
related species appear to be present, though less prominent, in other sites of serpentinization, including Lost City
(Brazelton et al. 2012; Schrenk et al. 2013). Another group
of organisms present in the Canadian springs and other
sites of serpentinization are members of the Clostridia,
whose closest known relatives are fermenters and which
may actually be involved in H2 production. Significant new
insights into the composition and activity of the microbial communities at serpentinite-hosted alkaline springs
on land are likely over the next few years as more sites
are investigated.
Although studies are so far limited, active microbial populations might also inhabit subsurface environments within
serpentinites. It appears likely, however, that living within
a serpentinite may present some significant challenges to
microbial life (Schrenk et al. 2013). For one, the capacity
for organisms to utilize H 2 and CH4 as energy sources
depends on the availability of suitable electron acceptors,
and the supply of these acceptors is likely to be limited in
the reducing environments within serpentinites. In the
absence of suitable electron acceptors, some fermentative organisms can still metabolize organic compounds,
but these metabolic pathways provide substantially less
energy. The extremely alkaline conditions within serpentinites lead to additional challenges. High pH results in the
precipitation of carbonate minerals and the nearly complete
removal of aqueous inorganic carbon species, leaving few
carbon sources that can be fi xed into biomass. Under such
circumstances, carbon monoxide and formate may become
prominent carbon sources for microbial growth. High pH
may also interfere with metabolic processes, such as the
transport of nutrients across the membrane, the maintenance of membrane proton gradients required for energy
conservation, and the stability of nucleic acids and other
macromolecules (Schrenk et al. 2013). While the presence
of microbial populations in serpentine-hosted springs
and other strongly alkaline environments demonstrates
that microorganisms can adapt to these conditions, these
adaptations undoubtedly come at a high-metabolic-energy
cost, which would be a severe constraint in areas of limited
energy supply.
Despite these challenges, there are several indications that
microbial activity does occur in subsurface habitats within
serpentinites. Some serpentinites recovered by drilling into
the subsurface beneath the ocean floor show enrichments
in the lighter isotope of sulfur that are indicative of microbial sulfate reduction (Alt and Shanks 1998), while others
reveal the presence of complex organic matter with an
apparently biological origin (Ménez et al. 2012). Microbial
methanogenesis in the subsurface may also contribute to
the isotopic composition of CH4 observed in submarine
vent fluids (Proskurowski et al. 2008). Some of the microorganisms found in serpentinite-hosted alkaline spring
waters and hydrothermal fluids represent organisms flushed
from the subsurface, but more direct sampling of these
habitats will be required to confi rm their presence and
activity within the rocks (Schrenk et al. 2013).
132
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SEPENTINITES AND THE ORIGIN
AND EARLY EVOLUTION OF LIFE
Ultramafic rocks that undergo serpentinization on modern
Earth represent pieces of the mantle that have been
displaced to the near surface, where they are exposed to
circulating ground- or seawater. Today, lavas erupted from
melting of the mantle have a basaltic composition, and
basalts do not undergo serpentinization because of their
higher silica content. Prior to ~3 billion years ago, however,
higher mantle temperatures allowed ultramafic lavas to
erupt at Earth’s surface, forming rocks called komatiites.
As a result of komatiite eruptions, ultramafic rocks were
much more widespread near Earth’s surface than they are
today, and serpentinization must also have been much
more widespread. The H 2 and CH4 produced by these
serpentinites would have provided an abundant source of
metabolic energy for chemosynthetic organisms on ancient
Earth, just as they do today (Schulte et al. 2006).
The characteristics that make serpentinites favorable
habitats for chemosynthetic microbial communities on the
modern Earth have focused attention on these systems
as possible sites for the origin and early evolution of life
(Sleep et al. 2011). In particular, these systems would have
the basic ingredients required for the so-called chemoautotrophic origin-of-life scenarios, including an abundance of
chemical energy sources and conditions conducive to the
reduction of CO2 to simple organic compounds. While most
early theories for the origin of life on early Earth postulated that life emerged from a “prebiotic soup” of organic
compounds, difficulties in accumulating aqueous solutions
with the right mix of organic molecules have led some
researchers to consider alternative scenarios (Martin et al.
2008; Lane et al. 2010). For example, it has been proposed
that the initial steps in the development of life were simple
reactions taking place in hydrothermal environments that
yielded chemical energy and led to the synthesis of prebiotic organic compounds (Martin et al. 2008; Martin and
Russell 2007). In these scenarios, reaction paths associated with the abiotic synthesis of acetate or other simple
organic compounds from CO2 , perhaps catalyzed by Fe
and Ni sulfide minerals, gradually transformed to become
the fi rst biosynthetic pathways. Support for these theories
may be provided by the close similarity of abiotic carbonreduction reactions in serpentinite systems to metabolic
pathways for energy conservation and biomass synthesis
found in many extant methanogens (FIG. 4); genomic
Abiotic pathway:
CO2
+H2
CO
Carbonyl
C
RS
CO2
H
C
Methylene-H4MPT
+ Ni-Fe-S
enzymes
+2H
+H2
CH3CO-Ni
H H
H
H H
C
Methyl-H4MPT
+H2
Biomass
+H
Methyl
+H2
CO
H
C
Formyl-H4MPT
Methenyl-H4MPT
+H2
+H
Methylene
CO2
+H2
SR
H
H
E LEMENTS
+H
CH4
Fe
S
133
Parallels between
the abiotic reduction of CO2 to CH4 and the
metabolic pathways used by
methanogenic archaea to extract
energy and fix carbon into
biomass. The abiotic pathway
shows the sequential reduction of
carbon on the surface of a
catalyst as it occurs in FischerTropsch-type reactions, successively forming surface-bound
carbonyl, formyl, carbide, methylene, and methyl moieties. The
inset in the biotic pathway shows
an iron–sulfur cluster at the core
of the carbon monoxide dehydrogenase enzyme used by most
methanogenic microorganisms in
biomass synthesis. RS and SR
refer to sulfur bonds linking the
Fe–S cluster to the organic
components of the enzyme.
H4MPT is tetrahydromethanopterin, a cofactor involved in
biological methanogenesis.
FIGURE 4
H2O
H
C
Carbide
Ultramafic rocks are not unique to Earth but likely constitute a large fraction of all rocky bodies in our Solar System.
Owing to the bulk composition of the materials that formed
the Solar System, olivine is by far the most abundant silicate
mineral that condensed during Solar System formation
and is the predominant silicate in meteorites. The Earth’s
mantle comprises nearly 70% of the mass of the planet
and, since similar materials condensed to form other rocky
SR
RS
O
In addition to electron-transfer reactions, pH gradients may
have been an additional source of metabolic energy in these
environments (Lane et al. 2010). Extant microorganisms
gain metabolic energy by maintaining a proton gradient
across their membranes, and in serpentine-hosted submarine hydrothermal environments on early Earth, such
gradients would evolve naturally at the interface between
hydrothermal-vent fluids and seawater. If the two were
physically separated by a semiporous barrier, such as a
layer of sulfide minerals at a submarine hydrothermal vent,
a strong proton gradient and electrical potential would
develop to drive chemical reactions. One could imagine
the gradual replacement of the barrier by an organic
membrane and subsequent incorporation into a developing
biological metabolism.
H
+H
Formyl
Even if life did not actually originate in this environment, the fluids discharged from serpentinites would have
provided one of the most abundant sources of energy for
biology on early Earth, at least until the onset of photosynthesis. Geochemical gradients that developed at the
interface between alkaline, H 2 -rich hydrothermal fluids
and mildly acidic, CO2 -rich seawater would have provided
sources of chemical energy for evolving metabolisms
(Schulte et al. 2006; Sleep et al. 2011). Although O2 would
not have been present in more than trace amounts at that
time, CO2 and possibly other electron donors, such as SO42and NO3 -, would have been available to provide energy via
reactions that include methanogenesis and sulfate reduction (TABLE 1).
Biotic pathway:
H2
O
evidence suggests that these pathways may be among the
most primitive carbon-fi xation pathways in all microbial
life. The cores of many enzymes involved in carbon fi xation
in extant chemosynthetic microorganisms contain Fe–S
clusters whose structure resembles the unit cells of sulfide
minerals found in deep-sea hydrothermal-vent chimneys
(FIG. 2), suggesting the possibility that the enzyme cores
may represent remnants of the earliest stages of biochemical evolution.
+ energy
CH4
A PR IL 2013
planets and moons, ultramafic rocks most likely dominate
the mantles of other differentiated planetary bodies in our
Solar System as well. Mars, for instance, is thought to have
an ultramafic mantle beneath a thin (a few kilometers)
basaltic crust, and a large fraction of Martian meteorites
that have been recovered on Earth are ultramafic rocks.
have not been identified among the meteorites that come
from Mars, probably because these rocks are too friable to
survive ejection from the Martian surface and transfer to
the Earth. Similar circumstances suggest the probability
that serpentinites occur on other planetary bodies, such as
Europa and Saturn’s moons Titan and Enceladus.
Wherever the ultramafic rocks on other planetary bodies
are exposed to circulating aqueous fluids at temperatures
below ~350 ºC, they will inevitably undergo serpentinization, just as they do on Earth. On the surface of Mars,
serpentine minerals associated with areas of olivine-rich
outcrops have been identified in spectra obtained by
orbiting spacecraft (Ehlmann et al. 2010), and serpentinization has been suggested as a possible source of CH4
in the Martian atmosphere. Considering the abundant
evidence for water on Mars, it seems likely that serpentinites are widespread in the subsurface, and active serpentinization may even be taking place today. Serpentinites
If life on Earth really did get its start at a serpentinitehosted hydrothermal vent or spring, it raises the distinct
possibility that life may also have gotten started at other
serpentinite environments beyond Earth. Hydrogenbased microbial communities may continue to inhabit
these environments, utilizing many of the same chemical
pathways and energy sources that support terrestrial life
(Schulte et al. 2006). Through continued study of the
chemistry and microbiology of serpentinites, we may fi nd
a solution to the origin of life on Earth, and better understand the prospects for fi nding life elsewhere.
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