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| Chemical and biochemical reactions. A schematic of the H 2-dependent conversions of CO 2 to CH 4 without cofactors (a) and with cofactors (b,c) in acetogens (to acetate) and methanogens growing on H 2 and CO 2. The numbers next to the arrows indicate the approximate change in free energy (G 0 ) at 25°C and pH 7 (G 0 ) in kJ per mole. The thermodynamic values are taken from REFS 55,56. For details of the biologically catalysed reactions, see the review by Maden 55. For details of the reactions without cofactors under hydrothermal conditions, in which the thermodynamic values provided do not directly apply, see REF. 101. The dotted oval represents bifunctional CO dehydrogenase/ acetyl-coenzyme A (acetyl CoA) synthase (CODH/ACS), a conserved enzyme that is common to the acetyl-CoA pathway of CO 2 reduction in both acetogens and methanogens. The enzymes that are involved in methyl synthesis in acetogens and methanogens are not evolutionary related, even though similar chemical steps are involved 55,63. This has been interpreted to mean that the overall exergonic chemical conversions are more ancient than the enzymes that catalyse them in modern cells. Although all reactions shown are reversible, arrows are shown in only one direction for simplicity. The asterisks at the methyl-H 4 MPT to CH 4 conversion and the acetyl-CoA to acetate conversion 54 indicate that several enzymes and cofactors that are not shown here are involved 55. In both acetogens 54 and methanogens 53 , net energy conservation (ATP gain) involves the generation of ion gradients using the overall reaction shown. This chemiosmotic potential is then harnessed by an ATPase. The coupling site in methanogenesis (not shown) entails the conversion of methyl-H 4 MPT to CH 4 (REF. 53); the coupling site in acetogenesis (not shown) has recently been suggested to involve a ferredoxin-NAD + oxidoreductase 102. The formate to formyl-H 4 F conversion in acetogens involves ATP hydrolysis (not shown), which lowers G 0 for the reaction to-10 kJ per mole 55 ; the chemiosmotic potential is required for the synthesis of formyl-MF in methanogens 53. For both acetogens and methanogens, black arrows indicate reactions that are involved in core ATP synthesis, whereas grey arrows indicate that a portion of the total carbon flux is used to satisfy the carbon needs of the cell. H 4 F, tetrahydrofolate; H 4 MPT, tetrahydromethanopterin; HSCoA, coenzyme A; MF, methanofuran; Ni[E], an Fe-Ni-S cluster in CODH/ACS. Part a adapted, with permission, from REF. 101 (2006) National Academy of Sciences. Parts b,c adapted, with permission, from REF. 55 (2000) Portland Press.
Content may be subject to copyright.
The chemistry of life is the chemistr y of reduced
organic compounds, and therefore all theories for
the origin of life must offer testable hypotheses to
account for the source of these compounds. The best-
known theories for the origin of organic compounds
are based on the notion of an ‘organic soup’ that was
generated either by lightning-driven reactions in the
early atmosphere of the Earth or by delivery of organic
compounds to the Earth from space (B OX 1). When
submarine hydrothermal vents were discovered 30
years ago, hypotheses on the source of life’s reduced
carbon started to change. Hydrothermal vents revealed
a vast and previously unknown domain of chemistry
on the Earth. These vents harbour rich ecosystems, the
energy source of which stems mainly from mid-ocean-
ridge volcanism1,2. The 360°C sulphide chimneys of
the vent systems are primordial environments that
are reminiscent of early Earth, with reactive gases,
dissolved elements, and thermal and chemical gradi-
ents that operate over spatial scales of centimetres to
metres. This discovery had an immediate impact on
hypotheses about the origin of life, because it was rec-
ognized that the vent systems were chemically reactive
environments that constituted suitable conditions for
sustained prebiotic syntheses3.
In 2000, a completely new type of vent system was
discovered that is characterized by carbonate chimneys
that rise 60 metres above the ultramafic sea-floor4,5.
This vent system was named the Lost City hydrother-
mal field (LCHF), and might be particularly relevant
to our understanding of the origins of life. The ultra-
mafic underpinnings of the Lost City system have a
similar chemical composition to lavas that erupted into
the primordial oceans on early Earth5,6. Consequently, the
LCHF provides insights into past mantle geochemistry
and presents a better understanding of the chemical con-
straints that existed during the evolutionary transition
from geochemical to biochemical processes.
Hydrothermal vents occur at sea-floor spreading
zones and have a global distribution (FIG. 1): vent systems
have been discovered at almost all sea-floor locations
that have been studied in detail7. At spreading zones,
magma chambers that contain molten rock (800–
1,200°C) discharge lavas onto the ocean floor over time
periods that range from <10 years between eruptions to
>50,000 years between eruptions8. These eruptions pro-
duce black smokers and associated diffuse flow systems
that host dense and diverse biological communities9,10.
By contrast, the mountains of the Lost City-like systems
are tens of kilometres off-axis, rarely contain volcanic
rocks and are formed by sustained fault activity that has
lasted for millions of years4,5,11. Lost City systems are pro-
foundly different from black smokers, so it is important
to contrast the two (for an in-depth comparison of Lost
City systems and black smokers, see REF. 12).
Black smokers
Examples of black smokers, such as the Faulty Towers
complex (FIG. 2a), are located directly above magma
chambers that are found 1–3 kilometres beneath the sea-
floor12. Black smoker chimneys emit hot (up to 405°C),
chemically modified sea-water13. Beneath the fissured
sea-floor, downwelling sea-water comes into close
contact with the magma chamber during its circulation
from the ocean floor, before moving through the crust
to re-emerge at the vents. Effluent at black smokers is
typically acidic (pH 2–3) and rich in dissolved transi-
tion metals14, such as Fe(II) and Mn(II). Because the
black smoker systems are fuelled by volcanoes, black
smoker fluids commonly contain high concentrations of
*Institut für Botanik III,
Heinrich-Heine Universität
Düsseldorf, 40225
Düsseldorf, Germany.
School of Oceanography,
University of Washington,
Seattle, Washington 98195,
§Jet Propulsion Laboratory,
California Institute of
Technology, Pasadena,
California 91109, USA.
Correspondence to W.M.
e-mail: w.martin@
Published online
29 September 2008
Hydrothermal vents and the
origin of life
William Martin*, John Baross, Deborah Kelley and Michael J. Russell§
Abstract | Submarine hydrothermal vents are geochemically reactive habitats that harbour
rich microbial communities. There are striking parallels between the chemistry of the H2–CO2
redox couple that is present in hydrothermal systems and the core energy metabolic
reactions of some modern prokaryotic autotrophs. The biochemistry of these autotrophs
might, in turn, harbour clues about the kinds of reactions that initiated the chemistry of life.
Hydrothermal vents thus unite microbiology and geology to breathe new life into research
into one of biology’s most important questions — what is the origin of life?
N OVM EBER 20 08
magmatic CO2 (4–215 mmol per kg), H2S (3–110 mmol
per kg) and dissolved H2 (0.1–50 mmol per kg), with
varying amounts of CH4 (0.05–4.5 mmol per kg) that is
formed both through biogenic and abiogenic processes12.
A range of temperatures exist, from the hot interior of
black smokers to the interface with cold (2°C), oxygenated
sea-water (FIG. 2b).
The dissolved gases and metals in black smokers fuel
the microbial communities that serve as the base of the
food chain in these ecosystems. Some of the archaea in
black smokers can replicate at temperatures up to 121°C15,
which is currently thought to be the upper temperature
limit of life. There are also examples of ancient, fossilized
black smokers, including one found in 90-million-year-
old copper deposits in Cyprus that contained fossilized
fauna16 and another found in 3,235-million-year-old
sulphide deposits in Western Australia that contained
filamentous microfossils17.
Lost City systems
The off-axis vents are radically different to black smok-
ers. However, our current understanding of these
systems is based on research into only one system: the
LCHF5,18. Off-axis vents are located several kilometres
away from the spreading zone. Their exhalate has also
circulated through the crust, where it can be heated up
to ~200°C19,20, but their waters do not come into close
contact with the magma chamber. Supplementar y
information S1 (figure) shows a schematic view of
the LCHF, w hich is located near the summit of a
4,000-metre mountain named the Atlantis Massif that
sits on 1.5–2-million-year-old crust, at a water depth
of ~750 metres4,21.
Fluid circulation within the massif is driven by con-
vection that dissipates heat from the underlying mantle
rocks, and perhaps, in part, by exothermic chemical
reactions between the circulating fluids and host rocks.
These rocks have different compositions compared with
those of submarine volcanoes, because they are domi-
nated by the magnesium- and iron-rich mineral olivine
and because they have lower silica concentrations. This
geochemical setting results in a highly alkaline (pH 9–11)
effluent and a combination of extreme conditions that
have not previously been observed in the marine envi-
ronment, including venting of 40–91°C hydrothermal
fluids with high concentrations of dissolved H2, CH4 and
other low-molecular-mass hydrocarbons, but almost
no dissolved CO2 (REFS 5,20,22). As discussed below,
Box 1 | Prebiotic soup theory
The concept that life arose from a prebiotic soup or primeval broth that covered the Earth is generally attributed to
Oparin84 and Haldane85. The theory received support from Miller’s86 demonstration that organic molecules could be
obtained by the action of simulated lightning on a mixture of the gases CH4, NH3 and H2, which were thought at that time
to represent Earth’s earliest atmosphere. The organic compounds that were measured included hydrogen cyanide (HCN),
aldehydes, amino acids, oil and tar. Additional amino acids were produced by Strecker synthesis through the hydrolysis of
the reaction products of HCN, ammonium chloride and aldehydes, and in later experiments polymerization of HCN
produced the nucleic acid bases adenine and guanine87. However, further condensation and polymerization of these
organic precursor molecules requires some mechanism to promote their concentration. Suggestions for this mechanism
have included evaporation of tidal pools, adsorption to clays, concentration in ice through eutectic melts and giant oil
slicks. Temperature cycling might also have been a factor in peptide production, although cold to freezing conditions are
now considered to be more favourable for prebiotic soup87.
In their original models, Oparin84 and Haldane85 assumed that protein was the source of genetic information, which
would have been transferred directly from protein to protein as colloidal organic droplets (coacervates) that
subsequently multiplied through the assimilation of further organic molecules. Oparin84 favoured abiotic synthesis, in
which an information-containing protein was the first step to life. By contrast, Haldane85 proposed that some form of
metabolism was the first step.
This issue of an ‘information first’ (or RNA world) versus a ‘metabolism first’ (or autotrophic origins) mechanism is still
debated in the origin-of-life community today. Current formulations of the information-first view posit that an evolutionary
transition occurred from peptide nucleic acids to tetrose nucleic acids, and eventually to RNA87,88, during which tetrose was
derived from formaldehyde condensations and bases were derived from HCN condensations. A large repertoire of RNAs
then took over as self-replicating entities in a prelude to the advent of DNA and proteins. According to this view, the various
stages that are involved in the origin and evolution of life from the prebiotic epoch culminated in exhaustion of the initial
prebiotic supply of preformed organic molecules, prompting the evolutionary-origin genetically encoded biosynthetic
pathways as compensation. Variants of the prebiotic broth theory propose that the essential building blocks of life were
synthesized in space and reached early Earth by comets89. Although there has been no debate about the occurrence of
organic molecules in comets, this mechanism still produces organic soup, but without the help of lightning.
An alternative proposal to prebiotic broth involves the H2-dependent chemistry of transition-metal sulphide catalysts
in a hydrothermal-vent setting. Such chemical conversions are similar to those involved in the CO2-reducing
biochemistry of modern microorganisms that use the Wood–Ljungdahl acetyl-coenzyme A (acetyl-CoA) pathway and
present a plausible starting point for biochemical evolution. However, this pathway leads not to prebiotic broth, but to
acetyl-CoA, an energy-rich thioester that could be the most central carbon backbone in microbial metabolism. The
synthesis of acetate and CH4 from H2 and CO2 releases energy, and therefore energy need not be derived from lightning
or conditions in space. Hence, the reactions typically take place readily on the Earth, both in modern acetogenesis and
methanogenesis, as well as in abiogenic CH4 or acetate production at contemporary hydrothermal vents. The favourable
thermodynamics of CH4 and acetate formation could, in principle, support synthesis of more complicated biomolecules
that could become concentrated at their site of synthesis63.
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Nature Reviews | Microbiology
Turtle pits
Juan de
Fuca Middle Valley
Axial and Cleft
Escanaba Trough
Guaymas Basin
21 °N
13 °N
9–10 °N
Lost City
Menez Gwen
Reykjanes Ridge
Luck Strike
Snake Pit
Santorini and Milos
German Flats
East Pacific
Rise Central Indian
Esmeralda Bank
Alice Springs
Nikko Seamount
Sumisu Caldera
Manus Basin Vailulu’u
White Lady
Vai Lili
Brothers Caldera
Soria Moria
17° 30 S
21° 30 S
Southwest Indian
Broken Spur
Hook Ridge
Two or more different
microorganisms that associate
during growth to form
characteristically ordered
alkaline pH is an important property of vents that should
be considered when contemplating the biochemical
origins of life.
Mixing of warm, high-pH fluids with sea-water results
in carbonate precipitation and the growth of chimneys
that tower up to 60 metres above the surrounding sea-
floor. 14C radioisotopic dating indicates that hydrother-
mal activity has been ongoing for at least 30,000 years19,
whereas recent uranium–thorium dating indicates that
venting has been active for ~100,000 years23. A substan-
tial proportion of the exposed sea-floor that is on, and
near to, slow- and ultra-slow spreading ridges consists
of ultramafic rocks that are similar to those that host the
LCHF24–26. These rocks are sites of an important set of
geochemical reactions named serpentinization (BOX 2),
and have been producing geological H2 for as long as
there has been water on the Earth.
What grows at Lost City, and how?
Metagenomics and environmental sequencing of ribos-
omal RNA have shown that microbial communities
in actively venting carbonate chimneys in the LCHF
(FIG. 2c–e) are dominated by a novel phylotype of anaero-
bic methanogens from the Methanosarcinales order5,27,28.
These methanogens can use several organic compounds,
some of which have been implicated in anaerobic meth-
ane oxidation (AMO) in both hydrothermal sediments29,30
and methane seeps31,32. In chimneys that have little or no
active venting, the Lost City Methanosarcinales (LCMS)
group is replaced by a single phylotype of the anaerobic
methanotrophic clade ANME-1. A diverse bacterial
assemblage populates the chimney exteriors, where sul-
phur-oxidizing and methane-oxidizing bacteria use the
interface of oxygenated sea-water with H2- and CH4-rich
hydrothermal fluid. Sulphate-reducing Firmicutes have
also been identified; these organisms might serve as a
link between the high-temperature, anaerobic chimney
interiors and the sea-water-bathed chimney exteriors.
Some of the relevant core metabolic reactions that
underlie microbial growth at the LCHF are summarized
in TABLE 1. The vent effluent is devoid of oxygen and
harbours only anaerobes, although aerobes occur where
there is contact with ocean water.
Where the LCHF carbonate chimneys are bathed
in >80nC hydrothermal fluid, the LCMS group forms
dense biofilms that are tens of micrometres thick and
comprise ~100% of the archaeal community28. Recently,
methyl-coenzyme M reductase (mcrA) gene sequences
that correspond to both LCMS and ANME-1 have also
been recovered from LCHF carbonate chimneys28.
ANME-1 has been identified in numerous environ-
ments, including CH4 seeps in anoxic marine sediments,
CH4 hydrates, carbonate reefs in the Black Sea and
mud volcanoes31–35. Genomic evidence indicates that
anaerobic, methane-oxidizing archaea harbour nearly
all of the genes necessary for methanogenesis, including
mcrA36,37, but it has been unclear whether LCMS and
ANME-1 are sources or sinks of CH4 within the Lost
City system.
In all marine environments in which AMO is known
to occur, anaerobic, methanotrophic archaebacteria co-
occur with sulphate-reducing eubacteria, commonly in
tightly coupled consortia32, although cells are not always
in direct physical contact with each other29. However,
a recent report has also linked AMO with denitrifica-
tion in a freshwater canal38. Incubation experiments
show that the marine consortia represent a syntrophic
metabolic relationship between CH4-oxidizing archaea
Figure 1 | Global distribution of known hydrothermal vents. Temperature and chemical anomalies hint that many
more sites exist throughout the world’s oceans. Data courtesy of D. Fornari and T. Shank, Woods Hole Oceanographic
Institute, Massachusetts, USA.
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H2 oxidation
Fe reduction
S° reduction
Fe, Mn oxidation
Nature Reviews | Microbiology
Stable isotope study
The use or analysis of stable
isotopes, such as 2H, 13C or 15N,
that do not undergo radioactive
decay. Isotope discrimination
properties of an enzymatically
catalysed process can produce
characteristic isotope ratios,
for example13C or 12C, that
differ from those generated by
various non-enzymatic
processes. This provides
insights into the partitioning of
elements during microbial
metabolism, and in
geochemistry, can provide
insights into the biological and
geological source of substances
such as CH4.
and sulphate-reducing bacteria39–42. AMO is not ener-
getically feasible unless sulphate-reducing bacteria or
some other metabolic group of bacteria or archaea are
present to use H2 that is generated from the anaerobic
oxidation of CH4.
Almost all marine sites where AMO has been shown
to occur are cold, sediment-hosted environments that
are supported by CH4 hydrates, CH4 seeps or mud
volcanoes. The only two exceptions are the Guaymas
Basin, where warm sediments overlie a hydrothermal
system and AMO can occur at temperatures as high as
85nC30,43,44, and the LCHF, where biofilms that are com-
posed of organisms related to the ANME-3 group are
in direct contact with serpentinization-derived CH4 at
temperatures in excess of 90nC5,28. The results from ear-
lier phylogenetic and natural stable isotope studies5,27,28,45
were unable to determine whether actively venting
carbonate chimneys at Lost City are sites of methano-
genesis or AMO. Newer data, however, indicate that
CH4 and associated short hydrocarbons in the efflu-
ent of LCHF are not formed by biological activity,
but instead are of geochemical origin22. This, in turn,
suggests that LCMS and ANME-1 are probably oxidiz-
ing CH4 at LCHF, and that they are doing so in the
presence of abundant environmental H2. This interpre-
tation would be consistent with the recent intriguing
results of Moran et al.46, who showed that high partial
pressures of H2 did not significantly inhibit AMO in
active sediments, but that methyl sulphide was inhibi-
tory, which indicated an important role for methyl
sulphide and only a peripheral role, if any, for H2 in
AMO in this sediment system.
Figure 2 | Hydrothermal vents. There are two main types of hydrothermal vent: the black smoker type (a,b) and the Lost
City type (c–e). a | A black smoker in the Faulty Towers complex in the Mothra hydrothermal field on the Endeavour Segment
of the Juan de Fuca Ridge. The tallest chimney rises 22 metres above the sea-floor. The ‘furry’ appearance of the chimneys
reflects the fact that the chimney walls are encrusted in dense communities of tube worms, scale worms, palm worms,
sulphide worms and limpets. The two-pronged chimney in the middle with an active plume is a 300°C chimney called Finn,
from which a 121°C organism was cultured that uses Fe(III) as an electron acceptor in the presence of N2 and CO2 (REF. 15).
b | The outer surface of black smoker chimneys is bathed in a mixture of 2°C, oxygenated sea-water and warm vent fluid that
escapes from within the structure. The inner walls that form the boundary of the central up-flow conduits commonly
exceed 300°C, and temperatures are fixed by a steady supply of rapidly rising, strongly reducing vent fluid. Intermediate
conditions exist as gradients between these extremes. Changes in microbial abundance, diversity and community structure
have been associated with inferred environmental gradients in the chimney walls99,100. c | Microbial sampling at the Lost City
hydrothermal field. The robotic vehicle Hercules is shown hovering near the summit of the 60-metres-tall Poseidon
complex. White areas are active or recently active sites of venting. d | The top left part of the Nature Tower. Wreck-fish,
which are ~1 metre in length and are commonly found at a water depth of 750 metres, routinely investigated the vehicles.
The Poseidon complex has four pinnacles, two of which are shown here. Actively venting edifices are composed of
aragonite (CaCO3) and brucite (Mg(OH)2). The grey–brown material also contains carbonate, but is richer in calcite that has
recrystallized from aragonite. e | A close up of a 75°C, diffusely venting carbonate chimney showing a titanium water
sampler. Dense colonies of filamentous bacteria thrive in the high pH, CH4- and H2-rich fluids. The insides of the chimneys
are dominated by a single phylotype of archaea from the Methanosarcinales order that grow at 80°C. A phylotype of
anaerobic methanotrophic archaea are restricted to lower-temperature chimneys. Bacterial 16S ribosomal RNA gene
sequences correspond to a diverse community that includes species of Methylobacter (or Methylomonas), species of
Thiomicrospira, members of the Firmicutes phylum and Desulfotomaculum alkaliphilus28. Parts a,b courtesy of D. Kelley and
J. Deloney, University of Washington, USA. Images c–e courtesy of D. Kelley, Institute for Exploration, University of Rhode
Island, USA, and the National Ocean and Atmospheric Administration Office of Ocean Exploration.
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Clues from Lost City effluent CH4
The millimolar concentrations of abiogenic CH4 present
in the Lost City effluent do not seem to originate from
marine CO2 in down-draft waters, but instead seem to
originate from CO2 that has leached from an inorganic
carbon source in the mantle22. Provided that H2 from
serpentinization is the reductant for CH4 synthesis at
LCHF, the overall reaction that produces CH4 in the
subsea-floor hydrothermal system is the same as that
used by methanogens to fuel carbon and energy metabo-
lism (TABLE 1). This thought-provoking finding raises an
important question: is the geochemical synthesis of CH4
at Lost City a model for the simple types of core chemical
reactions from which biological CH4 production arose?
Keeping in mind that the answer might be no, the
idea is worth pursuing. It should be noted that propo-
nents of the idea that life started from prebiotic soup
(BOX 1) would certainly disagree with this view47, but
we will not argue their case here. Hypotheses about
the origin-of-life chemistry have long been couched in
terms of chemical equilibria48. However, life is far from
an equilibrium process. In all living systems, there is a
main chemical reaction at the core of energy metabo-
lism — the chemical reaction that cells use to synthe-
size their ATP — and a few examples of core chemical
reactions that generate ATP in the bacteria and archaea
that inhabit the Lost City are listed in TABLE 1.
Hydrothermal vents have breathed fresh life into a
century-old concept regarding the origin of life. This
concept is known today as autotrophic origins and posits
that life started from CO2, that the first organisms were
autotrophs and that these autotrophs obtained their
reduced carbon from CO2 and other simple C1 com-
pounds, using H2 as the main electron donor3. Central
to some versions of the autotrophic origins hypothesis is
the view that the acetyl-coenzyme A (acetyl-CoA) path-
way of CO2 fixation is the most ancient among modern
CO2-fixing pathways49,50 and that the biochemistry of
this pathway might parallel a simpler abiotic chemistry
at the origin of metabolism. The acetyl-CoA pathway
that is found in modern acetogens and methanogens is
particularly relevant to this hypothesis. This is because,
in contrast to the other four pathways of CO2-fixation
that are known51,52, the acetyl-CoA pathway not only
Box 2 | Serpentinization: the source of H2 and CH4 at Lost City
Hydrothermal vents, and Lost City in particular, have sparked interest in a geochemical process known as
serpentinization90. At off-axis vents, sea-water invades the warm (100°C) to hot (400°C) oceanic crust through cracks and
crevasses where the chemical reactions of serpentinization take place. The relevant sea-water constituents for the
serpentinization reaction are H2O and CO2 (dissolved as HCO3
). The relevant crustal constituents are Fe2+-containing
rocks91. At Lost City, this rock consists mainly of the mineral olivine (~Mg1.6Fe0.4SiO4). Seismic data indicate that the fluids
beneath Lost City percolate to depths of 500 metres (or deeper) beneath the sea-floor at moderately high temperatures
(150–200°C) The crust beneath Lost City is 1–2 million years old based on magnetic anomaly information, and it is likely
that the rocks which are ~500 metres to 1 kilometre beneath the sea-floor reach temperatures of ~300°C. Under these
conditions, Fe2+ in the rocks reduces H2O to produce Fe3+, H2 and hydrocarbons according roughly to Equation 1.
(Mg,Fe)2SiO4 + H2O + C l Mg3SiO5(OH)4 + Mg(OH)2 + Fe3O4 + H2 + CH4 + C2–C5 (1)
Unaltered and hydrothermally altered mantle rocks contain various carbon compounds, including graphite, CH
4 and CO2.
Work by Proskurowski et al.22 indicates that beneath Lost City, hydrocarbons can be generated according to Equation 2.
CO2aq + [2 + (m/2n)]H2 l(1/n)CnHm + 2H2O (2)
The resulting minerals are magnetite (Fe3O4), which contains Fe3+ as a product of Fe2+ oxidation, brucite (Mg(OH)2) and a
hydroxylated magnesium–iron silicate called serpentine (Mg2.85Fe0.15Si2O5(OH)4), after which the process is named.
Serpentinization has probably been ongoing since there were oceans on the Earth92. One cubic metre of olivine can
deliver approximately 500 moles of H2 during serpentinization93. Most of the Earth’s oceanic crust consists of olivine (or
pyroxene, which can also participate in serpentinization reactions), and the total volume of the Earth’s ocean is estimated
to circulate through hydrothermal vents every ~100,000 years93. Thus, the vast amounts of Fe2+, the Earth’s electron
reservoir for H2 production via serpentinization, in the mantle is nowhere near exhaustion92. Serpentinization delivers, and
has always delivered, a substantial amount of H2 as a source of electrons for primary production in submarine ecosystems.
At the Lost City hydrothermal field (LCHF), serpentinization produces H2 that can reduce CO2 to CH4 geochemically22. The
same geochemical process might have given rise to the energy-releasing chemical reactions at the core of carbon and
energy metabolism in methanogens and acetogens, reactions that were eventually augmented by cofactors and
Serpentinization occurs both beneath the hot and acidic (pH 2–3) black smokers and within the cooler and alkaline
(pH 9–11) off-axis vent systems, such as Lost City12. Therefore, although both types of vent would have offered a pH
gradient that was similar to the Hadean ocean (see the main text), the lower temperatures found at off-ridge vents would
provide more favourable conditions for sustained abiotic synthesis and accumulation of reduced carbon compounds
The chimneys at the LCHF are mainly composed of carbonates, rather than of iron monosulphide (FeS) minerals, which
because of their catalytic properties play a central part in our thinking about biochemical origins63–65. However, the
Hadean ocean was replete with Fe(II), and therefore FeS chimneys would have been abundant at that time. Thus, although
the chemistry of the serpentinization process in the Hadean was perhaps not much different than that observed today, the
specific geochemical conditions at the vent–ocean interface in the Hadean would have differed markedly from those
observed in today’s oxic oceans64.
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Table 1 | Anaerobic and aerobic microbial metabolic reactions and potential energy yields in hydrothermal vent environments
Metabolism Reaction $G0` (kJ
per mole)*
Examples in vent environments
Methanogenesis 4 H2 + CO2 l CH4 + 2 H2O
+ H2O lCH4 + H CO3
4 HCOO + H+ l3 HCO3
+ CH4
Methanococcus spp. common in magma-hosted vents;
Methanosarcinales at Lost City
S° reduction S° + H2 lH2S–45 Lithotrophic and heterotrophic; hyperthermophilic
Anaerobic CH4
oxidation CH4 + SO4
2– l HS + HCO3
+ H2O–21 Methanosarcina spp. and epsilonproteobacteria at mud
volcanoes and methane seeps
Sulfate reduction SO4
2– + H+ + 4 H2 lHS + 4 H20–170 Deltaproteobacteria
Fe reduction 8 Fe3+ + CH3CO2
+ 4 H2O l2 HCO3
+ 8 Fe2+ +
9 H+
Epsilonproteobacteria, thermophilic bacteria and
hyperthermophilic Crenarchaeota
Fermentation C6H12O6 l2 C2H6O + 2 CO2–300 Many genera of bacteria and archaea
oxidation§HS + 2 O2 lSO4
2– + H+–750 Many genera of bacteria; common vent animal symbionts
CH4 oxidation CH4 + 2 O2 lHCO3
+ H+ + H2O–750 Common in hydrothermal systems; vent animal
H2 oxidation H2 + 0.5 O2 lH2O–230 Common in hydrothermal systems; vent animal
Fe oxidation Fe2+ + 0.5 O2 + H+ lFe3+ + 0.5 H20–65 Common in low-temperature vent fluids; rock-hosted
microbial mats
Mn oxidation Mn2+ + 0.5 O2 + H2O lMnO2 + 2 H+–50 Common in low-temperature vent fluids; rock-hosted
microbial mats; hydrothermal plumes
Respiration C6H12O6 + 6 O2 l6 CO2 + 6 H2O–2,870 Many genera of bacteria
*From REFS 73,103 and W.J. Brazelton (personal communication). Some hyperthermophiles from the Archaea and Bacteria domains can couple the reduction of Fe with
the oxidation of H2 (REFS 104,105). §Some epsilonproteobacteria from subsea-floor hydrothermal vents, including newly erupted vents, can oxidize H
2S to (REF. 106).
Chemiosmotic coupling
The coupling of endergonic and
exergonic reactions through a
proton motive force.
Chemiosmotic coupling results
in the conservation of chemical
energy. In its most familiar
form, chemiosmotic coupling
entails the pumping of protons
from the inside of the cell to
the outside of the cell as
electrons are passed from a
donor to an acceptor through
an electron transport chain in
the prokaryotic plasma
membrane. This generates a
pH and electrical-potential
gradient across the plasma
membrane known as
the proton motive force. The
proton motif force represents
electrochemical energy that
can be harnessed in various
ways, but the best-known of
these involves ATPases, also
called coupling factors, which
synthesize ATP from ADP and
inorganic phosphate as
protons pass through them to
re-enter the cytoplasm.
provides a source of carbon, but is also the source of
ATP. During the reduction of CO2 with electrons from
H2, acetogens and methanogens use the acetyl-CoA
pathway to generate an ion gradient that can be har-
nessed by chemiosmotic coupling53–55. Using CO for either
methanogenesis or acetogenesis instead of H2 and CO2
provides more energy56, and thus might be of interest in
the context of the origins of life.
Such considerations bring C1 metabolism into focus
and have drawn attention to the thermodynamic equi-
libria of carbon species that result from the H2–CO2
couple at hydrothermal vents (FIG. 3). In the hot (>350°C)
conditions of black smokers, carbon that is in equilibrium
with water, even in the presence of significant levels of H2,
usually occurs as CO2. As temperatures decrease to 150°C
or lower, as at the LCHF, reduced-carbon species are
favoured57,58. McCollom and Seewald59,60 investigated the
equilibria that are present between H2, CO2 and reduced
C1 species in conditions that mimicked serpentinization-
driven reactions in off-axis vents. They found that, perhaps
surprisingly, there are no substantial kinetic barriers in the
reduction of CO2 to formate (and CO), formaldehyde and
methanol (the reactions proceed quickly), but that kinetic
barriers in the reduction to CH4 were appreciable60. In
particular, the reaction HCO3
+ H2 lHCOO + H2O
was found to be “rapid on geologic timescales at temperatures
as low as 100°C.” (REF. 59)
If these experimental conditions approximate Lost City
conditions in the subsurface, which seems likely, CH4-rich
Lost City effluents should contain reduced carbon species
in addition to CH4. Indeed, the Lost City fluids contain
dissolved organic carbon at 95 MM, which is more than
twice the concentration of local background (non-vent)
water, and both formate and acetate are present in signifi-
cantly higher concentrations than in deep sea-water61,62.
The presence of acetate and formate (in addition to CH4)
fits well with the hypothesis that the types of chemical
reactions which are catalysed by minerals in the mantle at
Lost City are inorganic analogues, and even the possible
evolutionary precursors, of the energy-releasing reactions
that predated microbial metabolism63. If life started from
CO2, and life began in hydrothermal vents, then a better
understanding of the reduction of CO2 to CH4, formate
and acetate during serpentinization, and a better under-
standing of the catalysts and the chemical intermediates
in that process, might allow new insights into the initial
reactions that provided reduced carbon for life. Simple
chemical compounds that could focus some of our cur-
rent thinking on primordial biochemistry in the context of
hydrothermal origins include transition metals and transi-
tion metal sulphides64,65, methyl sulphide63,66, thioesters67,
CO68, acetyl phosphate69 and carbonyl sulphide70, as well
as carbamyl phosphate, carboxy phosphate and formyl
phosphate63. Theoretically, it would seem that CO and
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V OLUME 6 w ww. nature. com/revi ews/micr o
Box 3 | The RNA-world concept
The discovery that RNA has catalytic activities94, similar to proteins, but also carries heritable information, similar to DNA,
had an immense impact on our thinking about early evolution. The ‘RNA world’ (REF. 95) was envisaged as an inventive
phase of biogenesis in which RNA alone performed the vital functions of life (catalysis, heredity, recombination and
evolution), together with RNA-like cofactors, such as NAD+ or FAD96. This concept is so conceptually satisfying that
questions which surround the origins of DNA and protein from RNA are sometimes couched in terms of how rather than
if83. But the RNA world does not solve conceptual problems that relate to life’s origin for free; rather, it exacts an
exorbitant price. As one of the most esteemed proponents of the RNA world hypothesis, the late Leslie E. Orgel88, once
pointed out: “[w]hile acceptance of an RNA World greatly simplifies the problem of the origin of life, it also has a negative
aspect. If the origin of the RNA World preceded the origin of protein synthesis, little can be learned about the chemistry
of the origin of life from the study of protein enzyme mechanisms. The justification of prebiotic syntheses by appealing to
their similarity to enzymatic mechanisms has been routine in the literature of prebiotic chemistry. Acceptance of the
RNA World hypothesis invalidates this type of argument. If the RNA World originated de novo on the primitive Earth, it
erects an almost opaque barrier between biochemistry and prebiotic chemistry.”
This quote symbolically marks the dividing line in the ‘metabolism first’ versus ‘information first’ debate (BOX 1). Did
enzymes invent all biochemical reactions or did chemistry (similar to some biochemical reactions) naturally exist before
the assistance of enzymes? Enzymes do not perform feats of magic, but merely allow chemical reactions that have a
tendency to occur anyway to occur more rapidly. The enzymes that generate CH4 from H2 and CO2, for example, are
complex and highly ordered in modern methanogens, but the overall reaction that they catalyse takes place in
hydrothermal vents either with (microbially) or without (geochemically) the help of proteinaceous catalysts. Indeed, the
first step of biological methanogenesis, the formation of a carbamate, is spontaneous and requires no protein at all
97. Of
course, it remains within the realm of possibilities that modern microbial metabolism holds no relics of the chemistry that
preceded the origin of genetic material88. An alternative, however, is that the evolutionary growth of organically
catalysed reactions was derived from a central trail blazed by exergonic, spontaneous and/or inorganically catalysed
reactions, and that this trail was, in turn, constrained by that which is thermodynamically favourable98. Prerequisite to this
view is a sustained source of chemical energy, which hydrothermal vents provide. In this sense, the similarity between
chemical conversions presented by the acetyl-coenzyme A pathway63 and carbon reduction at hydrothermal vents22
(FIG. 3) are deserving of closer inspection, as both release energy, some of which is harnessed by the acetyl-coenzyme A
pathway to allow additional chemical work.
chemically accessible methyl groups, such as CH3SH,
would be able to support sustainable acetyl thioester
and acetyl phosphate synthesis in a hydrothermal vent
setting. Acetate would be the initial end product of such
primordial biochemistry, which would involve substrate-
level phosphorylation. It has been suggested that a simple
carbon and energy metabolism of this type at an alkaline
hydrothermal vent might have been capable of supporting
the origin of microbial life even up to translation, genes
and proteins63. The origin of chemiosmotic coupling, the
main means of ATP synthesis among microorganisms, is
more complicated. However, as discussed below, alkaline
vents offer a possible solution even for this mechanism,
because they provide a geochemically generated electro-
chemical gradient of protons at the vent–ocean interface.
Alkaline pH and gradients are important
An exciting property of Lost City effluent is its alkalinity
(pH 9–11), which produces a pH gradient at the vent–
ocean interface. It is feasible that the naturally chemios-
motic nature of alkaline hydrothermal vents in the Hadean
eon, when chimney interiors had a pH of 9–10 and the
outer walls of chimneys were bathed in ocean fluids with
a pH of 5–6, were essential for the origin of free-living
cells63,64,71. The nature and chemistry of chemiosmotic har-
nessing72 (through an ATPase) is more conserved than the
myriad of mechanisms or proteins that generate proton
gradients in bacteria and archaea73,74. Accordingly, it has
been suggested that the ability to harness a continuous and
naturally existing proton gradient at an alkaline hydro-
thermal vent is older than the ability to generate a proton
gradient with a chemistry that is specified by genes63.
This idea might seem counter-intuitive, but what
are the alternatives? At the most basic level, there are
protein–cofactor complexes that generate chemios-
motic potential (for example, the myriad proteins and
membrane-soluble carriers that comprise electron-
transport chains among prokaryotes7 5,76) and protein
complexes that harness chemiosmotic potential to
conserve chemical energ y as ATP (ATPases)77,78.
Regarding the question of which came first, there are
two simple possibilities: either energ y-consuming
pumping or energy-conserving chemiosmotic harness-
ing came first. It is possible that early chemical systems
could have expended energy to generate ion gradients
and only later developed mechanisms to harness them.
However, this hypothetical scenario would require energy
to burn, something that early chemical systems might not
have had in abundant supply.
Alternatively, it is also possible that the ion gradi-
ents were always present, being produced by alkaline
hydrothermal effluents that interfaced with almost
pH-neutral ocean water. In turn, this naturally existing
energy source could have been tapped into by proteins
that later evolved a more complicated and diversified
chemistry in which ion gradients were generated across
the plasma membrane63. This would have provided early
chemical systems with energy to burn, which would
have boosted biochemical evolution in a dramatic man-
ner, as a large amount of chemical-free energy would
have been made available in the form of phosphoan-
hydride bonds. These bonds provide phosphorylating
potential that allow reactions which are thermody-
namically unfavourable (but perhaps are favourable for
N OVM EBER 20 08
Nature Reviews | Microbiology
Without cofactors Acetogenesis Methanogenesis
+H2, –H2O
Cell carbon
ab c
Figure 3 | Chemical and biochemical reactions. A schematic of the
H2-dependent conversions of CO2 to CH4 without cofactors (a) and with cofactors
(b,c) in acetogens (to acetate) and methanogens growing on H2 and CO2. The
numbers next to the arrows indicate the approximate change in free energy ($G0)
at 25°C and pH 7 ($G0`) in kJ per mole. The thermodynamic values are taken from
REFS 55,56. For details of the biologically catalysed reactions, see the review by
Maden55. For details of the reactions without cofactors under hydrothermal
conditions, in which the thermodynamic values provided do not directly apply,
see REF. 101. The dotted oval represents bifunctional CO dehydrogenase/
acetyl-coenzyme A (acetyl CoA) synthase (CODH/ACS), a conserved enzyme that
is common to the acetyl-CoA pathway of CO2 reduction in both acetogens and
methanogens. The enzymes that are involved in methyl synthesis in acetogens
and methanogens are not evolutionary related, even though similar chemical
steps are involved55,63. This has been interpreted to mean that the overall
exergonic chemical conversions are more ancient than the enzymes that catalyse
them in modern cells. Although all reactions shown are reversible, arrows are
shown in only one direction for simplicity. The asterisks at the methyl-H4MPT to
CH4 conversion and the acetyl-CoA to acetate conversion54 indicate that several
enzymes and cofactors that are not shown here are involved55. In both acetogens54
and methanogens53, net energy conservation (ATP gain) involves the generation of
ion gradients using the overall reaction shown. This chemiosmotic potential is then
harnessed by an ATPase. The coupling site in methanogenesis (not shown) entails
the conversion of methyl-H4MPT to CH4 (REF. 53); the coupling site in acetogenesis
(not shown) has recently been suggested to involve a ferredoxin–NAD+
oxidoreductase102. The formate to formyl-H4F conversion in acetogens involves
ATP hydrolysis (not shown), which lowers $G0` for the reaction to –10 kJ per
mole55; the chemiosmotic potential is required for the synthesis of formyl-MF in
methanogens53. For both acetogens and methanogens, black arrows indicate
reactions that are involved in core ATP synthesis, whereas grey arrows indicate
that a portion of the total carbon flux is used to satisfy the carbon needs of the
cell. H4F, tetrahydrofolate; H4MPT, tetrahydromethanopterin; HSCoA, coenzyme A;
MF, methanofuran; Ni[E], an Fe–Ni–S cluster in CODH/ACS. Part a adapted, with
permission, from REF. 101 (2006) National Academy of Sciences. Parts b,c adapted,
with permission, from REF. 55 (2000) Portland Press.
self-replication or geochemically independent reactions)
to proceed more readily. For example, the conversion of
formate to the formylated pterin cofactor (formyl-H4F)
shown in FIG. 3b is thermodynamically unfavourable
($G0` equals 22 kJ per mole) without ATP hydrolysis,
but is favourable ($G0` equals –10 kJ per mole) when
accompanied by ATP hydrolysis55, whereby acetogens
gain their net ATP from chemiosmotic coupling54.
Curiously, the synthesis of formyl-H4F in methanogen-
esis from formyl-H4MPT (FIG. 3c) also requires energy
input55, but this energy does not come from ATP.
Instead the enzyme that directly catalyses the reaction
consumes the part of the chemiosmotic gradient that is
generated by the later reactions of methane synthesis79.
Both modern acetogenesis and methanogenesis require
chemiosmotic gradients to operate, which points to the
antiquity of chemiosmotic coupling mechanisms and
suggests that before mechanisms evolved to harness
naturally existing chemiosmotic potential at alkaline
vents, geochemically provided reduced-C1 compounds
were essential to the initiation of both acetogenesis and
methanogenesis63. Such C1 compounds could have been
methyl groups that were generated through serpentini-
zation, which would agree with recent findings from
Lost City22.
The temperature gradients and porous structure of
both modern5 and ancient71 hydrothermal vents could
also enable the concentration80 and perhaps even rep-
lication81 of the products of organic synthesis to form
primitive genetic material82. The view that life arose at a
hydrothermal vent is compatible with concepts germane
to the RNA world83 (BOX 3), in that microcompartments at
vents would provide a physical and chemical environment
that is conducive to chemical synthesis, concentration
and polymerization.
The discovery of hydrothermal vent systems pro-
foun dly change d how we vi ew the ge ol ogi cal,
geochemical and ecological history of the Earth.
Under-sea vents are abundant on the floor of the
world’s oceans and are important sources of many ele-
ments and organic compounds that are transferred into
the hydrosphere. They can support life without input
from photosynthesis and they harbour fascinating
life with symbiotic relationships that involve lithoau-
totrophic microorganisms that use chemical energy to
support metazoans. Moreover, a real or virtual sojourn
to active deep-sea hydrothermal vent environments is
also a visit to primordial Earth — active hydrothermal
systems existed as soon as liquid water accumulated on
the Earth more than 4.2 billion years ago. It is possible
that present-day hydrothermal vent microorganisms
harbour relict physiological characteristics that resem-
ble the earliest microbial ecosystems on the Earth. It
is also possible that geochemical processes of carbon
reduction in hydrothermal systems represent the same
kind of energy-releasing chemistry that gave rise to the
first biochemical pathways. Life need not have evolved
this way, but the mere prospect that it could have is
reason enough to probe these environments further.
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1. Corliss, J. B. et al. Submarine thermal springs on the
Galapagos rift. Science 203, 1073–1083 (1979).
2. Spiess, F. N. et al. East Pacific rise: hot springs and
geophysical experiments. Science 207, 1421–1433
3. Baross, J. A. & Hoffman, S. E. Submarine
hydrothermal vents and associated gradient
environments as sites for the origin and evolution of
life. Orig. Life Evol. Biosph. 15, 327–345 (1985).
4. Kelley, D. S. et al. An off-axis hydrothermal vent field
near the Mid-Atlantic Ridge at 30°N. Nature 412,
145–149 (2001).
Reports the discovery of the LCHF and important
differences of LCHF geochemistry compared with
black smokers.
5. Kelley, D. S. et al. A serpentinite-hosted ecosystem:
the Lost City hydrothermal field. Science 307,
1428–1434 (2005).
6. de Wit, M. J. Early Archean processes: evidence from
the South African Kaapvaal craton and its greenstone
belts. Geologie en Mijinbouw 76, 369–371 (1998).
7. Baker, E. T. & German, C. R. in Mid-Ocean Ridges:
Hydrothermal Interactions between the Lithosphere
and Oceans (eds German, C., Lin, J. & Parson, L. M.)
245–266 (American Geophysical Union, Washington
DC, 2004).
8. Hammond, S. R. Offset caldera and crater collapse on
Juan de Fuca ridge-flank volcanoes. Bull. Volcanol. 58,
617–627 (1997).
9. Delaney, J. R. et al. The quantum event of oceanic
crustal accretion: impacts of diking at mid-ocean
ridges. Science 281, 222–230 (1998).
10. Embley, R. W. & Lupton, J. E. in The Subseafloor
Biosphere at Mid-Ocean Ridges (eds Wilcock, W. S. D.,
DeLong, E. F., Kelley, D. S., Baross, J. A. & Cary, S. C.)
75–97 (American Geophysical Union, Washington DC,
11. Karson, J. A., Früh-Green, G. L., Kelley, D. S., Williams,
E. A., Yoerger, D. R. & Jakuba, M. Detachment shear
zone of the Atlantis Massif core complex, Mid-Atlantic
ridge, 30°N. Geochem. Geophys. Geosyst. 7,
Q06016 (2006).
12. Kelley, D. S., Baross, J. A. & Delaney, J. R. Volcanoes,
fluids, and life at mid-ocean ridge spreading centers.
Annu. Rev. Earth Planet Sci. 30, 385–491 (2002).
13. Von Damm, K. L. et al. Extraordinary phase separation
and segregation in vent fluids from the southern East
Pacific Rise. Earth Planet Sci. Lett. 206, 265–378
14. Von Damm, K. L. in Physical, Chemical, Biological, and
Geological Interactions within Seafloor Hydrothermal
Systems (eds Humphris, S., Zierenberg, R., Mullineau, L.
& Thomson R.) 222–247 (American Geophysical
Union, Washington DC, 1995).
15. Kashefi, K. & Lovley, D. R. Extending the upper
temperature limit for life. Science 301, 934 (2003).
16. Little, C. T. S., Cann, J. R., Herrington, R. J. &
Morisseau, M. Late Cretaceous hydrothermal vent
communities from the Troodos Ophiolite, Cyprus.
Geology 27, 1027–1030 (1999).
17. Rasmussen, B. Filamentous microfossils in a
3,235-million-year-old volcanogenic massive sulphide
deposit. Nature 405, 676–679 (2000).
18. Ludwig, K. A., Kelley, D. S., Butterfield, D. A., Nelson,
B. K. & Früh-Green, G. Formation and evolution of
carbonate chimneys at the Lost City Hydrothermal
Field. Geochim. Cosmochim. Acta 70, 3625–3645
19. Früh-Green, G. L. et al. 30,000 years of hydrothermal
activity at the Lost City Vent Field. Science 301,
495–498 (2003).
20. Proskurowski, G., Lilley, M. D., Kelley, D. S. & Olson,
E. J. Low temperature volatile production at the Lost
City Hydrothermal Field, evidence from a hydrogen
stable isotope geothermometer. Chem. Geol. 229,
331–343 (2006).
21. Blackman, D. K. et al. Geology of the Atlantis massif,
(Mid-Atlantic Ridge 30°N): implications for the
evolution of an ultramafic oceanic core complex. Mar.
Geophys. Res. 23, 443–469 (2002).
22. Proskurowski, G. et al. Abiogenic hydrocarbon
production at lost city hydrothermal field. Science
319, 604–607 (2008).
Reports isotopic evidence which indicated that CH4
and volatile hydrocarbon production at Lost City is
a geochemical, not a biological, process. This study
therefore implicates serpentinization in abiogenic
carbon reduction, which could be highly relevant in
an origin-of-life context.
23. Ludwig, K. A., Kelley, D. S., Shen, C., Cheng, H. &
Edwards, R L. U/Th geochronology of carbonate
chimneys at the Lost City hydrothermal field. Eos
Trans. AGU 86, V51B–1487 (2005).
24. Bach, W., Banerjee, N. R., Dick, H. J. B. & Baker, E. T.
Discovery of ancient and active hydrothermal systems
along the ultra-slow spreading Southwest Indian Ridge
10°–16°E. Geochem. Geophys. Geosystems 3, 1044
25. Dick, H. J. B., Lin, J. & Schouten, H. An ultraslow-
spreading class of ocean ridge. Nature 426, 405–412
26. Edmonds, H. N. et al. Discovery of abundant
hydrothermal venting on the ultraslow-spreading Gakkel
ridge in the Arctic. Nature 421, 252–256 (2003).
27. Schrenk, M. O., Kelley, D. S., Bolton, S. & Baross, J. A.
Low archaeal diversity linked to sub-seafloor
geochemical processes at the Lost City Hydrothermal
Field, Mid-Atlantic Ridge. Environ. Microbiol. 6,
1086–1095 (2004).
28. Brazelton, W. J., Schrenk, M. O., Kelley, D. S. &
Baross, J. A. Methane and sulfur metabolizing
microbial communities dominate in the Lost City
hydrothermal vent ecosystem. Appl. Environ.
Microbiol. 72, 6257–6270 (2006).
29. Orphan, V. J., House, C. H., Hinrichs, K. U., McKeegan,
K. D. & DeLong, E. F. Direct phylogenetic and isotopic
evidence for multiple groups of Archaea involved in
the anaerobic oxidation of methane. Geochim.
Cosmochim. Acta 66, A571 (2002).
30. Teske, A. et al. Microbial diversity of hydrothermal
sediments in the Guaymas Basin: evidence for
anaerobic methanotrophic communities. Appl.
Environ. Microbiol. 68, 1994–2007 (2002).
31. Aloisi, G. I. et al. CH4-consuming microorganisms and
the formation of carbonate crusts at cold seeps. Earth
Planet. Sci. Lett. 203, 195–203 (2002).
32. Boetius, A. et al. A marine microbial consortium
apparently mediating anaerobic oxidation of methane.
Nature 407, 623–626 (2000).
33. Michaelis, W. et al. Microbial reefs in the Black Sea
fueled by anaerobic oxidation of methane. Science
297, 1013–1015 (2002).
34. Orphan, V. J. et al. Comparative analysis of methane-
oxidizing archaea and sulfate-reducing bacteria in
anoxic marine sediments. Appl. Environ. Microbiol.
67, 1922–1934 (2001).
35. Thomsen, T. R., Finster, K. & Ramsing, N. B.
Biogeochemical and molecular signatures of anaerobic
methane oxidation in a marine sediment. Appl.
Environ. Microbiol. 67, 1646–1656 (2001).
36. Hallam, S. J. et al. Reverse methanogenesis: testing
the hypothesis with environmental genomics. Science
305, 1457–1462 (2004).
37. Meyerdierks, A. et al. Insights into the genomes of
archaea mediating the anaerobic oxidation of
methane. Environ. Microbiol. 7, 1937–1951 (2005).
38. Raghoebarsing, A. et al. A microbial consortium
couples anaerobic methane oxidation to
denitrification. Nature 440, 918–921 (2006).
39. Girguis, P. R., Cozen, A. E. & DeLong E. F. Growth and
population dynamics of anaerobic methane-oxidizing
archaea and sulfate-reducing bacteria in a continuous-
flow bioreactor. Appl. Environ. Microbiol. 71,
3725–3733 (2005).
40. Hoehler, T. M., Alperin, M. J., Albert, D. B. & Martens,
C. S. Field and laboratory studies of methane
oxidation in an anoxic marine sediment: evidence for a
methanogen–sulfate reducer consortium. Global
Biogeochem. Cycles 8, 451–463 (1994).
41. Nauhaus, K., Boetius, A., Kruger, M. & Widdel, F.
In vitro demonstration of anaerobic oxidation of
methane coupled to sulphate reduction in sediment
from a marine gas hydrate area. Environ. Microbiol. 4,
296–305 (2002).
42. Nauhaus, K., Treude, T., Boetius, A. & Krüger, M.
Environmental regulation of the anaerobic oxidation of
methane: a comparison of ANME-I and ANME-II
communities. Environ. Microbiol. 7, 98–106 (2005).
43. Schouten, S., Wakeham, S. G., Hopmans, E. C. &
Damste, J. S. S. Biogeochemical evidence that
thermophilic archaea mediate the anaerobic oxidation
of methane. Appl. Environ. Microbiol. 69,
1680–1686 (2003).
44. Kallmeyer, J. & Boetius, A. Effects of temperature and
pressure on sulfate reduction and anaerobic oxidation of
methane in hydrothermal sediments of Guaymas Basin.
Appl. Environ. Microbiol. 70, 1231–1233 (2004).
45. Boetius, A. Lost City life. Science 307, 1420–1422
46. Moran, J. J. et al. Methyl sulfides as intermediates in
the anaerobic oxidation of methane. Environ.
Microbiol. 10, 162–173 (2008).
47. Bada, J. L. & Lazcano, A. Some like it hot, but not the
first biomolecules. Science 296, 1982–1983 (2002).
48. Orgel, L. E. The implausibility of metabolic cycles on
the prebiotic Earth. PLoS Biol. 6, e18 (2008).
49. Fuchs, G. CO2 fixation in acetogenic bacteria:
variations on a theme. FEMS Microbiol. Rev. 39,
181–213 (1986).
50. Fuchs, G. & Stupperich, E. in Evolution of Prokaryotes
(eds Schleifer, K. H. & Stackebrandt, E.) 235–251
(Academic, London, 1985).
51. Berg, I. A., Kockelkorn, D., Buckel, W. & Fuchs, G.
A 3-hydroxypropionate/4-hydroxybutyrate autotrophic
carbon dioxide assimilation pathway in Archaea.
Science 318, 1782–1786 (2007).
52. Thauer, R. K. A fifth pathway of carbon fixation.
Science 318, 1732–1733 (2007).
53. Thauer, R. K., Kaster, A. K., Seedorf, H., Buckel, W. &
Hedderich R. Methanogenic archaea: ecologically
relevant differences in energy conservation. Nature
Rev. Microbiol. 6, 579–591 (2008).
Provides the most recent summary of methanogen
bioenergetics and explains important and newly
recognized differences in the energy metabolism of
methanogens that possess cytochromes compared
with those that lack cytochromes.
54. Müller, V. Energy conservation in acetogenic bacteria.
Appl. Environ. Microbiol. 69, 6345–6353 (2003).
55. Maden, B. E. H. Tetrahydrofolate and
tetrahydromethanopterin compared: functionally
distinct carriers in C1 metabolism. Biochem. J. 350,
609–629 (2000).
56. Rother, M. & Metcalf, W. W. Anaerobic growth of
Methanosarcina acetivorans C2A on carbon
monoxide: an unusual way of life for a methanogenic
archaeon. Proc. Natl Acad. Sci. USA 101,
16929–16934 (2004).
57. Shock, E. L. Geochemical constraints on the origin of
organic compounds in hydrothermal systems.
Orig. Life Evol. Biosph. 20, 331–367 (1990).
58. Shock, E. L., McCollom, T. M. & Schulte, M. D.
in Thermophiles: The Keys to Molecular Evolution and
The Origin of Life? (eds Wiegel, J. & Adams, M. W. W.)
59–76 (Taylor and Francis, London, 1998).
59. McCollom, T. M. & Seewald, J. S. Experimental
constraints on the hydrothermal reactivity of organic
acids and acid anions: I. Formic acid and formate.
Geochim. Cosmochim. Acta 67, 3625–3644 (2003).
60. McCollom, T. M. & Seewald J. S. Abiotic synthesis of
organic compounds in deep-sea hydrothermal
environments. Chem. Rev. 107, 382–401 (2007).
61. Lang, S. Q., Butterfield, D., Hedges, J. & Lilley, M.
Production of isotopically heavy dissolved organic
carbon in the Lost City Hydrothermal Vent Field.
Eos Trans. AGU 86, V43C–06 (2005).
62. Lang, S. Q., Butterfield, D. & Lilley, M. Organic
geochemistry of Lost City Hydrothermal fluids.
InterRidge Theoretical Institute ‘Biogeochemical
interaction at deep-sea vents’ [online], http://
63. Martin, W. & Russell, M. J. On the origin of
biochemistry at an alkaline hydrothermal vent. Philos.
Trans. R. Soc. Lond. B 367, 1187–1925 (2007).
64. Russell, M. J. & Hall, A. J. The emergence of life from
iron monosulphide bubbles at a submarine
hydrothermal redox and pH front. J. Geol. Soc. London
154, 377–402 (1997).
65. Cody, G. D. Transition metal sulfides and the origin of
metabolism. Annu. Rev. Earth Planet. Sci. 32,
569–599 (2004).
66. Heinen, W. & Lauwers, A. M. Organic sulfur
compounds resulting from the interaction of iron
sulfide, hydrogen sulfide and carbon dioxide in an
anaerobic aqueous environment. Orig. Life Evol.
Biosph. 26, 131–150 (1996).
Detected Fe(II)- and hydrogen sulphide-dependent
CO2 reduction of methyl sulphide and other
compounds under mild conditions as might have
been encountered in Hadean hydrothermal vents.
67. Huber, C. & Wächtershäuser, G. Activated acetic acid
by carbon fixation on (Fe, Ni)S under primordial
conditions. Science 276, 245–247 (1997).
Detected Fe(II)- and Ni(II)-dependent synthesis of
acetate and the thioester acetyl methyl sulphide
from CO and methyl sulfide under conditions as
might have been encountered in Hadean
hydrothermal vents.
68. Wächtershäuser, G. From volcanic origins of
chemoautotrophic life to Bacteria, Archaea and
Eukarya. Philos. Trans. R. Soc. Lond. B 361,
1787–1806 (2006).
N OVM EBER 20 08
69. Ferry, J. G. & House, C. H. The step-wise evolution of
early life driven by energy conservation. Mol. Biol.
Evol. 23, 1286–1292 (2006).
70. Leman, L., Orgel, L. & Ghadiri, M. R. Carbonyl sulfide-
mediated prebiotic formation of peptides. Science
306, 283–286 (2004).
71. Russell, M. J., Daniel, R. M., Hall, A. J. &
Sherringham, J. A hydrothermally precipitated
catalytic iron sulphide membrane as a first step
toward life. J. Mol. Evol. 39, 231–243 (1994).
72. Amend, J. P. & Shock, E. L. Energetics of overall
metabolic reactions of thermophilic and
hyperthermophilic Archaea and Bacteria. FEMS
Microbiol. Rev. 25, 175–243 (2001).
73. Mitchell, P. Coupling of phosphorylation to electron
and hydrogen transfer by a chemi-osmotic type of
mechanism. Nature 191, 144–148 (1961).
74. Berry, S. The chemical basis of membrane
bioenergetics. J. Mol. Evol. 54, 595–613 (2002).
75. Schäfer, G., Engelhard, M. & Müller, V. Bioenergetics
of the Archaea. Microbiol. Mol. Biol. Rev. 63,
570–620 (1999).
76. Baymann, F. et al. The redox protein construction kit:
pre-last universal common ancestor evolution of
energy conserving enzymes. Philos. Trans. R. Soc.
Lond. B 358, 267–274 (2003).
77. Junge, W. ATP synthase and other motor proteins.
Proc. Natl Acad. Sci. USA 96, 4735–4737 (1999).
78. Murata, T., Yamato, I., Kakinuma, Y., Leslie, A. G. W. &
Walker, J. E. Structure of the rotor of the V-type Na+-
ATPase from Enterococcus hirae. Science 308,
654–659 (2005).
79. Kaesler, B. & Schönheit, P. The role of sodium ions in
methanogenesis. Formaldehyde oxidation to CO2 and
2 H2 in methanogenic bacteria is coupled with primary
electrogenic Na+ translocation at a stoichiometry of
2–3 Na+/CO2. Eur. J. Biochem. 184, 223–232 (1989).
80. Baaske, P., Weinert, F. M., Duhr, S., Lemke, K. H.,
Russell, M. J. & Braun, D. Extreme accumulation of
nucleotides in simulated hydrothermal pore systems.
Proc. Natl Acad. Sci. USA 104, 9346–9351 (2007).
81. Braun, D. & Libchaber, A. Thermal force approach to
molecular evolution. Phys. Biol. 1, P1–P8 (2004).
82. Koonin, E. V. An RNA-making reactor for the origin of
life. Proc. Natl Acad. Sci. USA 104, 9105–9106
83. Joyce, G. F. The antiquity of RNA-based evolution.
Nature 418, 214–221 (2002).
84. Oparin, A. I. The Origin of Life (Dover, New York,
85. Haldane, J. B. S. The origin of life. Rationalist Annual
148, 3–10 (1929).
86. Miller, S. L. A production of amino acids under
possible primitive Earth conditions. Science 117,
528–529 (1953).
87. Bada, J. L. How life began on Earth: a status report.
Earth Planet. Sci. Lett. 226, 1–15 (2004).
88. Orgel, L. E. Prebiotic chemistry and the origin of the
RNA World. Crit. Rev. Biochem. Mol. Biol. 39,
99–123 (2004).
89. de Duve, C. Vital Dust: Life as a Cosmic Imperative
(Basic Books, New York, 1995).
90. Schulte, M., Blake, D., Hoehler, T. & McCollom, T. M.
Serpentinization and its implications for life on the
early Earth and Mars. Astrobiology 6, 364–376
91. Bach, W. et al. Unraveling the sequence of
serpentinization reactions: petrography, mineral
chemistry, and petrophysics of serpentinites from
MAR 15ºN (ODP Leg 209, Site 1274). Geophys. Res.
Lett. 33, L13306 (2006).
92. Sleep, N. H., Meibom, A., Fridriksson, T., Coleman,
R. G. & Bird, D. K. H2-rich fluids from serpentinization:
geochemical and biotic implications. Proc. Natl Acad.
Sci. USA 101 , 12818–12823 (2004).
93. Fisher, A. T. Marine hydrogeology: recent
accomplishments and future opportunities.
Hydrogeol. J. 13, 69–97 (2005).
94. Cech, T. R. A model for the RNA-catalyzed replication
of RNA. Proc. Natl Acad. Sci. USA 83, 4360–4363
95. Gilbert, W. The RNA world. Nature 319, 618 (1986).
96. White, H. B. Coenzymes as fossils of an earlier
metabolic state. J. Mol. Evol. 7, 101–104 (1976).
97. Bartoschek, S., Vorholt, J. A., Thauer. R. K.,
Geierstanger, B. H. & Griesinger, C.
N-carboxymethanofuran (carbamate) formation
from methanofuran and CO2 in methanogenic
archaea. Thermodynamics and kinetics of the
spontaneous reaction. Eur. J. Biochem. 267,
3130–3138 (2000).
98. Morowitz, H. J., Kostelnik, J. D., Yang, J. & Cody, G. D.
The origin of intermediary metabolism. Proc. Natl
Acad. Sci. USA 97, 7704–7708 (2000).
99. Schrenk, M. O., Kelley, D. S., Delaney, J. R. & Baross,
J. A. Incidence and diversity of microorganisms within
the walls of an active deep-sea sulfide chimney. Appl.
Environ. Microbiol. 69, 3580–3592 (2003).
100. Pagé, A., Tivey, M. K., Stakes, D. S. & Reysenbach,
A.-L. Temporal and spatial archaeal colonization of
hydrothermal vent deposits. Environ. Microbiol. 10 ,
874–884 (2008).
101. Seewald, J. S., Zolotov, M. Y. & McCollom, T. M.
Experimental investigation of single carbon
compounds under hydrothermal conditions. Geochim.
Cosmochim. Acta 70, 446–460 (2006).
Provides important insights into the chemical
equilibria and speciation of C1 intermediates in
the reaction of H2 and CO2 to CH4 under
conditions that simulate submarine
hydrothermal vents. This study showed that
formate and CO are readily generated from CO2
and H2 and revealed kinetic barriers to CH4
102. Imkamp, F., Biegel, E., Jayamani, E., Buckel, W. &
Müller, V. Dissection of the caffeate respiratory chain
in the acetogen Acetobacterium woodii:
identification of an Rnf-type NADH dehydrogenase
as a potential coupling site. J. Bacteriol. 189,
8145–8153 (2007).
103. Edwards, K. J., Bach, W. & McColluom, T. M.
Geomicrobiology in oceanography: microbe–mineral
interactions at and below the seafloor. Trends
Microbiol. 13, 449–456 (2005).
104. Kashefi, K., Holmes, D. E., Lovley, D. R. & Tor, J. M.
in The Subseafloor Biosphere at Mid-Ocean Ridges
(eds Wilcock, W. S. D., DeLong, E. F., Kelley, D. S.,
Baross, J. A. & Cary, S. C.) 199–212 (American
Geophysical Union, Washington DC, 2004).
105. Campbell, B. J. & Engel, A. S. The versatile
E-proteobacteria: key players in sulphidic habitats.
Nature Rev. Microbiol. 4, 458–468 (2006).
106. Vargas, M., Kashefi, K., Blunt-Harris, E. L. & Lovley,
D. R. Microbiological evidence for Fe(III) reduction on
early Earth. Nature 395, 65–67 (1998).
We thank J. F. Allen, N. Lane and C. Schmidt for comments.
M.J.R. is supported by the Jet Propulsion Laboratory,
California Institute of Technology, through a contract from the
National Aeronautics and Space Administration. D.K. and J.B.
are supported by a grant from the National Science
Foundation (grant number OCE-0137206) and a grant from
the National Oceanic and Atmospheric Administration Office
of Exploration. J.B. received additional support from the
NASA Astrobiology Institute through the Cornegie
Geophysical Institute. W.M. is supported, in part, by a Julius-
von-Haast Fellowship from the government of New Zealand
and by the Deutsche Forschungsgemeinschaft.
See online article: S1 (figure)
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... In concert with this prebiotic chemistry research, early Earth geochemists have proposed a number of environments that may have been favorable to prebiotic reactions, such as hydrothermal systems on land or the seafloor (24)(25)(26)(27)(28), iron-sulfur mineral surfaces (29,30), clays (31,32), and ice (8,33), among others. While no environment has been shown to provide the perfect mixture of thermodynamic drive, molecular stabilization, and the production of a comprehensive suite of protobiomolecules, several of the proposed origin of life environments suggest that these details are not out of reach. ...
... Phylogenetic evidence strongly suggests that the ATP synthase complex predated the LUCA because the catalytic and noncatalytic subunits of ATP synthase are members of the same family of universal paralogs and were likely both present in the proteome of the LUCA (57,58,60). This very early origin of the ATP synthase complex has led to a model proposing that, before ETCs, ATP generation could have been powered by geochemical proton gradients (102) produced by serpentinite-hosted alkaline hydrothermal vents (Fig. 3) (28,103,104) in some ways analogous to the Lost City Hydrothermal Field, which produces an alkaline vent fluid as serpentine is formed through the hydration of olivine-bearing ocean crust (26,105). In an early Earth context, the interface between alkaline hydrothermal vent fluid and mildly acidic early Earth seawater (106,107) could have generated a proton gradient that powered an ancient ATP synthase (103,108). ...
... Various authors have proposed that some components of chemiosmosis, including aspects of ETC enzymes, proton gradient generation, and formation of ATP or polyphosphate energy currency, could have functioned in a prebiotic setting at or prior to the origin of life (26,103). Though a complete prebiotic pathway similar to a biological ETC, involving discrete reactions that can be individually tested, has not yet been demonstrated in the lab, some aspects of ETC systems have been shown to function in a prebiotic context. ...
Full-text available
The origin and early evolution of life is generally studied under two different paradigms: bottom up and top down. Prebiotic chemistry and early Earth geochemistry allow researchers to explore possible origin of life scenarios. But for these "bottom-up" approaches, even successful experiments only amount to a proof of principle. On the other hand, "top-down" research on early evolutionary history is able to provide a historical account about ancient organisms, but is unable to investigate stages that occurred during and just after the origin of life. Here, we consider ancient electron transport chains (ETCs) as a potential bridge between early evolutionary history and a protocellular stage that preceded it. Current phylogenetic evidence suggests that ancestors of several extant ETC components were present at least as late as the last universal common ancestor of life. In addition, recent experiments have shown that some aspects of modern ETCs can be replicated by minerals, protocells, or organic cofactors in the absence of biological proteins. Here, we discuss the diversity of ETCs and other forms of chemiosmotic energy conservation, describe current work on the early evolution of membrane bioenergetics, and advocate for several lines of research to enhance this understanding by pairing top-down and bottom-up approaches.
... origin of life | vesicles | inorganic mineral surfaces | surface chemistry | alkaline hydrothermal vents One of the leading models for the emergence of life on earth is the alkaline hydrothermal vent theory (1)(2)(3)(4)(5). Off-axis hydrothermal vents (comparable to the well-known Lost City vent field) are focusing centers for various thermodynamic gradients that can drive a wide range of chemical processes (6)(7)(8)(9). ...
... Cold, CO 2 -rich, oxidized sea water as present in the Hadean (10)(11)(12), percolates into the porous, mineral environs of the vents. Within the vent chimneys lie networks of microscopic pores, through which the fluid is permeating (3). The seawater eventually circles back to rejoin the ocean, passing through the growing vent chimneys and emerging very different in composition and temperature (13)(14)(15). ...
... Accordingly to the alkaline vent theory, an array of prebiotic reactions, exploiting disequilibria and the presence of small-molecule precursors took place, producing biomolecules such as small peptides (16)(17)(18)(19)(20). In the meantime, the rock-water reaction known as serpentinization could have released H 2 in the midst of such vent structures, enabling reducing reactions such as alkane polymerization (3) and ketone reduction to alcohols (21). We can surmise that the synthesis of many prebiotic molecules would have occurred in the presence of hydrothermal vents, that created favorable conditions for the emergence of primitive biochemistry (9,22,23). ...
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Alkaline hydrothermal vents have become a candidate setting for the origins of life on Earth and beyond. This is due to several key features including the presence of gradients of temperature, redox potential, pH, the availability of inorganic minerals, and the existence of a network of inorganic pore spaces that could have served as primitive compartments. Chemical gardens have long been used as experimental proxies for hydrothermal vents. This paper investigates-10pc]Please note that the spelling of the following author name in the manuscript differs from the spelling provided in the article metadata: Richard J. G. Löffler. The spelling provided in the manuscript has been retained; please confirm. a set of prebiotic interactions between such inorganic structures and fatty alcohols. The integration of a medium-chain fatty alcohol, decanol, within these inorganic minerals, produced a range of emergent 3 dimensions structures at both macroscopic and microscopic scales. Fatty alcohols can be considered plausible prebiotic amphiphiles that might have assisted the formation of protocellular structures such as vesicles. The experiments presented herein show that neither chemical gardens nor decanol alone promote vesicle formation, but chemical gardens grown in the presence of decanol, which is then integrated into inorganic mineral structures, support vesicle formation. These observations suggest that the interaction of fatty alcohols and inorganic mineral structures could have played an important role in the emergence of protocells, yielding support for the evolution of living cells.
... Hydrothermal systems (Class II): Submarine hydrothermal vents, especially alkaline hydrothermal vents (AHVs), have garnered a great deal of attention since the 1980s [Corliss et al., 1981, Baross andHoffman, 1985] as promising sites for the origin(s) of life, and as habitats for intricate microbial ecosystems [Martin et al., 2008, Russell et al., 2014, Sojo et al., 2016, Cartwright and Russell, 2019, Russell, 2021; however, these environments have attracted criticism of their capacity to engender abiogenesis Bada [2004], Sutherland [2017]. Submarine hydrothermal vents are not only documented on Earth and Enceladus [Waite et al., 2017, Cable et al., 2021, but could also occur on other icy worlds in the Solar system [Hand et al., 2020]. ...
The ubiquity of information transmission via molecular communication between cells is comprehensively documented on Earth; this phenomenon might even have played a vital role in the origin(s) and early evolution of life. Motivated by these considerations, a simple model for molecular communication entailing the diffusion of signaling molecules from transmitter to receiver is elucidated. The channel capacity $C$ (maximal rate of information transmission) and an optimistic heuristic estimate of the actual information transmission rate $\mathcal{I}$ are derived for this communication system; the two quantities, especially the latter, are demonstrated to be broadly consistent with laboratory experiments and more sophisticated theoretical models. The channel capacity exhibits a potentially weak dependence on environmental parameters, whereas the actual information transmission rate may scale with the intercellular distance $d$ as $\mathcal{I} \propto d^{-4}$ and could vary substantially across settings. These two variables are roughly calculated for diverse astrobiological environments, ranging from Earth's upper oceans ($C \sim 3.1 \times 10^3$ bits/s; $\mathcal{I} \sim 4.7 \times 10^{-2}$ bits/s) and deep sea hydrothermal vents ($C \sim 4.2 \times 10^3$ bits/s; $\mathcal{I} \sim 1.2 \times 10^{-1}$ bits/s) to the hydrocarbon lakes and seas of Titan ($C \sim 3.8 \times 10^3$ bits/s; $\mathcal{I} \sim 2.6 \times 10^{-1}$ bits/s).
... There are many theories on a possible emergence of life at alkaline hydrothermal vents (AHVs) on Earth. The "RNA world" theory (Gilbert, 1986), and the "metabolism first" theory at AHVs (Martin et al., 2008) feature prominently in the discussion about the emergence of life and are now considered to be not necessarily mutually exclusive (Preiner et al., 2020). A key unknown in the emergence of life is, how nucleic acids could overcome the large dilution factor of the prebiotic oceans, which has been referred to as the "concentration problem" (De Duve, 1991). ...
Full-text available
Mechanisms of nucleic acid accumulation were likely critical to life's emergence in the ferruginous oceans of the early Earth. How exactly prebiotic geological settings accumulated nucleic acids from dilute aqueous solutions, is poorly understood. As a possible solution to this concentration problem, we simulated the conditions of prebiotic low-temperature alkaline hydrothermal vents in co-precipitation experiments to investigate the potential of ferruginous chemical gardens to accumulate nucleic acids via sorption. The injection of an alkaline solution into an artificial ferruginous solution under anoxic conditions (O2 < 0.01% of present atmospheric levels) and at ambient temperatures, caused the precipitation of amakinite ("white rust"), which quickly converted to chloride-containing fougerite ("green rust"). RNA was only extractable from the ferruginous solution in the presence of a phosphate buffer, suggesting RNA in solution was bound to Fe2+ ions. During chimney formation, this iron-bound RNA rapidly accumulated in the white and green rust chimney structure from the surrounding ferruginous solution at the fastest rates in the initial white rust phase and correspondingly slower rates in the following green rust phase. This represents a new mechanism for nucleic acid accumulation in the ferruginous oceans of the early Earth, in addition to wet-dry cycles and may have helped to concentrate RNA in a dilute prebiotic ocean.
... That is not unreasonable, because rock-water interactions such as serpentinization in the submarine crust can produce H 2 -rich hydrothermal systems on a global scale, with individual systems persisting over hundreds of thousands of years (Arndt & Nisbet 2012;Russell & Arndt 2005;Russell et al. 2014;Sleep 2010Sleep , 2018Westall et al. 2018). These hydrothermal systems are internally structured, containing labyrinths of interconnected cell-like pores that frustrate the mixing of alkaline hydrothermal fluids with ocean waters saturated in CO 2 (Martin & Russell 2003Martin et al. 2008;Nitschke & Russell 2009;Russell & Hall 1997;Russell et al. 1989Russell et al. , 1994. Critically, in the Hadean era, 4 billion years ago, there may have been as much as 1 bar of atmospheric CO 2 , making the early oceans mildly acidic (pH 5-6) (Arndt & Nisbet 2012, Russell & Arndt 2005, Sleep 2018. ...
Full-text available
The origin of life entails a continuum from simple prebiotic chemistry to cells with genes and molecular machines. Using life as a guide to this continuum, we consider how selection could promote increased complexity before the emergence of genes. Structured, far-from-equilibrium environments such as hydrothermal systems drive the reaction between CO 2 and H 2 to form organics that self-organize into protocells. CO 2 fixation within protocells generates a reaction network with a topology that prefigures the universal core of metabolism. Positive feedback loops amplify flux through this network, giving a metabolic heredity that promotes growth. Patterns in the genetic code show that genes and proteins arose through direct biophysical interactions between amino acids and nucleotides in this protometabolic network. Random genetic sequences template nonrandom peptides, producing selectable function in growing protocells. This context-dependent emergence of information gives rise seamlessly to an autotrophic last universal common ancestor. Expected final online publication date for the Annual Review of Ecology, Evolution, and Systematics, Volume 54 is November 2023. Please see for revised estimates.
... Our understanding of the emergence of methanotrophic metabolism is within the framework of the hydrothermal theory for the origin of life (eg, [84]) with all its advantages (continuous flow of energy and matter, the temperature gradient, great possibilities of homogeneous and heterogeneous metal catalysis). Before the occurrence of cellular structures, the primary autotrophic metabolism on the surface of minerals created the chemical space of competing autocatalytic carbon fixation cycles. ...
Full-text available
In theories of the origin of life, the most reasonable is the concept of the primacy of autotrophic metabolism, in which carbon dioxide (CO2) is considered as the only source of carbon for the functioning of nascent metabolic pathways. The aim of this paper was to demonstrate that the origin and development of primary autotrophic metabolism on early Earth were influenced by the two different regimes of degassing of the Earth-reducing (predominance CH4) and oxidative (CO2). It follows from this that the ancestral carbon used in metabolism may have been derived from CH4 if the outflow of magma fluid to the surface of the Earth consisted mainly of methane. In such an environment, the primary autotrophic metabolic systems had to be methanotrophic. Due to the absence of molecular oxygen in the Archean conditions, this metabolism would have been anaerobic, i.e., oxidation of methane should have been carried out by inorganic high-potential electron acceptors. In light of the primacy and prevalence of CH4-dependent metabolism in hydrothermal systems of the ancient Earth, we propose a model of carbon fixation where the methane is fixed/transformed in a sequence of reactions in an autocatalytic methane-fumarate cycle. Nitrogen oxides are thermodynamically most favorable among possible oxidants of methane; however, even the activity of oxygen created by mineral buffers of iron in hydrothermal conditions is sufficient for methanotrophic acetogenesis. The Hadean-Archaean hydrothermal system model is considered in the form of a phase diagram, which demonstrates the area of redox and P, T conditions favorable for the formation and development of primary methanotrophic metabolism.
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Thiocyanate may have played as important a role as cyanide in the synthesis of several molecules. However, its concentration in the seas of the prebiotic Earth could have been very low. Thiocyanate was dissolved in two different seawaters: a) a composition that comes close to the seawater of the prebiotic Earth (seawater-B, Ca2+ and Cl−) and b) a seawater (seawater-A, Mg2+ and SO42−) that could be related to the seas of Mars and other moons in the solar system. In addition, forsterite-91 was a very common mineral on the prebiotic Earth and Mars. Two important results are reported in this work: 1) thiocyanate adsorbed onto forsterite-91 and 2) the amount of thiocyanate adsorbed, adsorption thermodynamic, and adsorption kinetic depend on the composition of the artificial seawater. For all experiments, the adsorption was thermodynamically favorable (ΔG < 0). The adsorption data fitted well in the Freundlich and Langmuir–Freundlich models. When dissolving thiocyanate in seawater 4.0-A-Gy and seawater 4.0-B-Gy, the adsorption of thiocyanate onto forsterite-91 was ruled by enthalpy and entropy, respectively. As shown by n values, the thiocyanate/foraterite-91 system is heterogeneous. For all kinetic data, the pseudo-first-order model presented the best fit. The constant rate for thiocyanate dissolved in seawater 4.0-A-Gy was twice that compared to thiocyanate dissolved in seawater 4.0-B-Gy or ultrapure-water. The interaction between thiocyanate and Fe2+ of forsterite-91 was with the nitrogen atom of thiocyanate. In the presence of thiocyanate, sulfate interacts with forsterite-91 as an inner-sphere surface complex, and without thiocyanate as an outer-sphere surface complex.
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The commonly supposed template-based format for RNA self-replication requires both duplex assembly and disassembly. This requisite binary provision presents a challenge to the development of a serviceable self-replication model since chemical reactions are thermochemically unidirectional. We submit that a solution to this problem lies in volcanic landmasses that engage in continuous cycles of wetting and drying and thus uniquely provide the twofold state required for self-replication. Moreover, they offer conditions that initiate chain branching, and thus furnish a path to autocatalytic self-replication. The foundations of this dual thermochemical landscape arise from the broad differences in the properties of the bulk water phase on the one hand, and the air/water interfacial regions that emerge in the evaporative stages on the other. With this reaction system as a basis and employing recognized thermochemical and kinetic parameters, we present simulations displaying the spontaneous and autocatalyzed conversion of racemic and unactivated RNA monomers to necessarily homochiral duplex structures over characteristic periods of years.
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Enceladus and Europa, icy moons of Saturn and Jupiter, respectively, are believed to be habitable with liquid water oceans and therefore are of interest for future life detection missions and mission concepts. With the limited data from missions to these moons, many studies have sought to better constrain these conditions. With these constraints, researchers have, based on modeling and experimental studies, hypothesized a number of possible metabolisms that could exist on Europa and Enceladus if these worlds host life. The most often hypothesized metabolisms are methanogenesis for Enceladus and methane oxidation/sulfate reduction on Europa. Here, we outline, review, and compare the best estimated conditions of each moon’s ocean. We then discuss the hypothetical metabolisms that have been suggested to be present on these moons, based on laboratory studies and Earth analogs. We also detail different detection methods that could be used to detect these hypothetical metabolic reactions and make recommendations for future research and considerations for future missions.
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Massive microbial mats covering up to 4-meter-high carbonate buildups prosper at methane seeps in anoxic waters of the northwestern Black Sea shelf. Strong 13C depletions indicate an incorporation of methane carbon into carbonates, bulk biomass,and specific lipids. The mats mainly consist of densely aggregated archaea ( phylogenetic ANME-1 cluster) and sulfate-reducing bacteria (Desulfosarcina/Desulfococcus group). If incubated in vitro,these mats perform anaerobic oxidation of methane coupled to sulfate reduction. Obviously, anaerobic microbial consortia can generate both carbonate precipitation and substantial biomass accumulation,which has implications for our understanding of carbon cycling during earlier periods of Earth’s history.
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The Kinousa, Memi, Kambia, Kapedhes, and Sha massive sulfide deposits located in the Troodos ophiolite, Cyprus, contain fossils from Late Cretaceous hydrothermal vent communities that lived on a spreading ridge above a subduction zone in the Neotethys ocean. The Troodos vent fossils provide unequivocal evidence for the exhalative origin of the host massive sulfide deposits, including those that are now located deep within the lava pile. The fossil vent assemblages are of low diversity; they contain numerous vestimentiferan worm tubes, uncommon cerithioid and epitoniid gastropods, and rare (?)serpulid worm tubes. Among the reported modern and ancient vent communities the presence of epitoniid gastropods is unique to Cyprus. At least three of the Troodos vent communities were living on the sea floor around the same time and were as closely spaced as vent communities on modern fast-spreading ridges. Together with slightly older vent worm tubes from the Semail ophiolite of Oman, currently 2500 km from Cyprus, the Troodos fossils show that hydrothermal vent communities were present in the Neotethys ocean from the Cenomanian to the Turonian, a time span of ˜5 m.y.
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The Lost City is a peridotite-hosted vent field distinctly different from other known hydrothermal systems. Fluids from Lost City are warm (40 to 90°C), reducing, highly alkaline (pH 9 to 11), and enriched in hydrogen, methane and other hydrocarbons [1]. Tall carbonate chimneys host dense microbial communities which have been implicated in methane and sulfur cycling [1]. The concentration and composition of organic matter in this environment has important ramifications for resident microbial communities as both a potential carbon source and as a potential electron donor. Additionally, organic components can serve as tracers of subsurface processes such as microbial autotrophic production or heterotrophic uptake which may otherwise be difficult to detect. Water samples were collected from the Lost City vent field in the summer of 2003 and analyzed for dissolved organic carbon (DOC) concentrations. Across the field, concentrations fell primarily along a single mixing line between the hydrothermal endmember fluids and local background seawater. Endmember fluids contain up to 95 muM DOC, more than twice the concentration in local background seawater. The presence of a single, field-wide mixing line suggests that the majority of the excess carbon is added at depth, with minimal interaction from the carbonate chimneys. To constrain its source, we analyzed the stable carbon (13C) isotopic composition of the DOC, which ranged from typical seawater values of -22.2 0/00 (VPDB) to -10.0 0/00 in the most hydrothermally pure samples. The excess DOC has a similar isotopic composition to both the methane in the fluids [2] and the lipids of methane-cycling archaea isolated in the chimney [1]. Ongoing molecular measurements will help constrain the potential sources of organic carbon to this system. [1] Kelley, D.S. et al. (2005) A Peridotite-Hosted Ecosystem: The Lost City Hydrothermal Field. Science. 307 (5714). [2] Proskurowski, G., Lilley, M.D., Frueh-Green, G.L., Olsen, E.J., and Kelley, D.S. (2004) The Use of Stable Hydrogen Isotopes as a Geothermometer in Hydrothermal Systems. Eos, Trans. American Geophysical Union 85(47): Fall Meeting Suppl. Abstract #B13A-0200
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We report the discovery of active and fossil hydrothermal systems during R/V Knorr Cruise 162, Legs VII and IX along a 400 km long segment of the ultra-slow Southwest Indian Ridge (SWIR) between 10 and 16°E, where the effective spreading rate for mantle upwelling is the slowest of any ocean ridge explored to date (8.4 mm yr−1 full rate). Eight of forty-one optical/temperature profiles contain hydrothermal plume characteristics that indicate firm evidence for two active vent sites and tentative evidence for as many as three others. Fossil hydrothermal material was recovered in 6 of the 38 dredge hauls and includes an occurrence of partially oxidized sulfide breccias, four deposits ofsepiolite and silica, as well as Mn-oxide and nontronite cemented breccias. The massive sulfide deposit likely developed during mixing of upwelling hot fluids with cold seawater within a shallow permeable fault breccia along a deep-seated normal fault bounding the southern rift valley wall. Silica and sepiolite deposits were found mostly on the rift valley walls and likely formed during low- to moderate-temperature ultramafic-hosted hydrothermal activity. The abundance of hydrothermal material and the frequency of localized hydrothermal activity is remarkable because the mantle upwelling and magma supply rates, and hence the magmatic heat input, along this section of the SWIR are lower than on any other explored segment of the global mid-ocean ridge system. This observation suggests that high mantle upwelling and magma supply rates are not required to drive mid-ocean ridge hydrothermal systems and that a close relationship between magmatic heat input and hydrothermal activity may not be established at the ultra-slow end of the ridge spreading spectrum. The frequency and distribution of hydrothermal activity in the study area may reflect a largely tectonic control on fluid circulation, with hydrothermal vent sites being preferentially associated with long-lived faults that provide fluid pathways. Our results suggest the contribution of magma-starved ridge segments to the global ocean-lithosphere geochemical budget is potentially much larger than previously thought.
Conference Paper
The biological oxidation of methane by anaerobic microorganisms is a significant sink for methane in the marine environment. Although there is convincing biogeochemical evidence for anaerobic oxidation of methane (AOM) by methanotrophic archaea and sulfate-reducing bacteria, the identity of these uncultured microorganisms is only now being described. In this study, we examined the diversity archaeal and bacterial assemblages involved in AOM using directly coupled isotopic and phylogenetic analyses at the level of single cells. The combined application of fluorescent in situ hybridization and secondary ion mass spectrometry (FISHSIMS) identified two phylogenetically distinct groups of archaea (ANME-1 and ANME-2) from marine methane seeps that were extremely depleted in carbon-13 (-83‰) and appear to be capable of directly oxidizing methane. These archaeal groups were observed to exist as monospecies aggregates or single cells as well as in physical association with bacteria including, but not limited to, members of the sulfate-reducing Desulfosarcina. The results from this work illustrate the complexity of the microbial communities and possible mechanisms involved in AOM. FISH-SIMS is an effective approach for understanding the dynamic microbial interactions within diverse methane-associated communities and may provide a useful culture-independent tool for deciphering the metabolic function of other environmentally significant microorganisms in situ.
Seafloor diking-eruptive events represent the irreducible, quantum events of upper oceanic crustal accretion. They record events by which a large portion of the oceanic crust has formed through geological history. Since 1993, the U.S. Navy's real-time Sound Surveillance System has allowed location of ongoing acoustic signatures of dike emplacement and basalt eruptions at ridge crests in the northeast Pacific. These diking-eruptive events trigger a sequence of related, rapidly evolving physical, chemical, and biological processes. Magmatic volatiles released during these events may provide nutrients for communities of subseafloor microorganisms, some of which thrive in high-temperature anaerobic environments. Many of the organisms identified from these systems are Archaea. If microorganisms can thrive in the water-saturated pores and cracks within deep, volcanically active portions of our planet, other hydrothermally active planets may harbor similar life forms.