The Origin of Life in Alkaline Hydrothermal Vents
Abstract
Over the last 70 years, prebiotic chemists have been very successful in synthesizing the molecules of life, from amino acids to nucleotides. Yet there is strikingly little resemblance between much of this chemistry and the metabolic pathways of cells, in terms of substrates, catalysts, and synthetic pathways. In contrast, alkaline hydrothermal vents offer conditions similar to those harnessed by modern autotrophs, but there has been limited experimental evidence that such conditions could drive prebiotic chemistry. In the Hadean, in the absence of oxygen, alkaline vents are proposed to have acted as electrochemical flow reactors, in which alkaline fluids saturated in H2 mixed with relatively acidic ocean waters rich in CO2, through a labyrinth of interconnected micropores with thin inorganic walls containing catalytic Fe(Ni)S minerals. The difference in pH across these thin barriers produced natural proton gradients with equivalent magnitude and polarity to the proton-motive force required for carbon fixation in extant bacteria and archaea. How such gradients could have powered carbon reduction or energy flux before the advent of organic protocells with genes and proteins is unknown. Work over the last decade suggests several possible hypotheses that are currently being tested in laboratory experiments, field observations, and phylogenetic reconstructions of ancestral metabolism. We analyze the perplexing differences in carbon and energy metabolism in methanogenic archaea and acetogenic bacteria to propose a possible ancestral mechanism of CO2 reduction in alkaline hydrothermal vents. Based on this mechanism, we show that the evolution of active ion pumping could have driven the deep divergence of bacteria and archaea. Key Words: Origin of life—Alkaline hydrothermal vent—Chemiosmotic coupling—Proton gradients—Methanogens—Acetogens—CO2 reduction. Astrobiology 16, 181–197.
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References
Amend J.P. and McCollom T.M. (2009) Energetics of biomolecule synthesis on early Earth. In Chemical Evolution II: From the Origins of Life to Modern Society, edited by Zaikowski L., Friedrich J.M., and Seidel S.R., American Chemical Society, Washington, DC, pp 63–94.
Amend J.P., LaRowe D.E., McCollom T.M., and Shock E.L. (2013) The energetics of organic synthesis inside and outside the cell. Philos Trans R Soc Lond B Biol Sci 368.
Arndt N.T. and Nisbet E.G. (2012) Processes on the young Earth and the habitats of early life. Annu Rev Earth Planet Sci 40:521–549.
Baaske P., Weinert F.M., Duhr S., Lemke K.H., Russell M.J., and Braun D. (2007) Extreme accumulation of nucleotides in simulated hydrothermal pore systems. Proc Natl Acad Sci USA 104:9346–9351.
Bach W., Paulick H., Garrido C.J., Ildefonse B., Meurer W.P., and Humphris S.E. (2006) Unraveling the sequence of serpentinization reactions: petrography, mineral chemistry, and petrophysics of serpentinites from MAR 15°N (ODP Leg 209, Site 1274). Geophys Res Lett 33:L13306.
Baross J. and Hoffman S. (1985) Submarine hydrothermal vents and associated gradient environments as sites for the origin and evolution of life. Orig Life Evol Biosph 15:327–345.
Bender G., Pierce E., Hill J., Darty J., and Ragsdale S. (2011) Metal centers in the anaerobic microbial metabolism of CO and CO2. Metallomics 3:797–815.
Berg J.M., Tymoczko J.L., Gatto G.J., and Stryer L. (2015) Biochemistry, W.H. Freeman & Company, New York.
Bradley A., Hayes J., and Summons R. (2009) Extraordinary 13C enrichment of diether lipids at the Lost City hydrothermal field indicates a carbon-limited ecosystem. Geochim Cosmochim Acta 73:102–118.
Brandes J.A., Boctor N.Z., Cody G.D., Cooper B.A., Hazen R.M., and Yoder H.S. Jr. (1998) Abiotic nitrogen reduction on the early Earth. Nature 395:365–367.
Brazelton W.J., Mehta M.P., Kelley D.S., and Baross J.A. (2011) Physiological differentiation within a single-species biofilm fueled by serpentinization. mBio 2.
Buckel W. and Thauer R.K. (2013) Energy conservation via electron bifurcating ferredoxin reduction and proton/Na+ translocating ferredoxin oxidation. Biochim Biophys Acta 1827:94–113.
Budin I., Bruckner R.J., and Szostak J.W. (2009) Formation of protocell-like vesicles in a thermal diffusion column. J Am Chem Soc 131:9628–9629.
Ciccarelli F.D., Doerks T., von Mering C., Creevey C.J., Snel B., and Bork P. (2006) Toward automatic reconstruction of a highly resolved tree of life. Science 311:1283–1287.
Cleaves H.J., Chalmers J.H., Lazcano A., Miller S.L., and Bada J.L. (2008) A reassessment of prebiotic organic synthesis in neutral planetary atmospheres. Orig Life Evol Biosph 38:105–115.
Cody G.D. (2004) Transition metal sulfides and the origins of metabolism. Annu Rev Earth Planet Sci 32:569–599.
de Duve C. (2005) Singularities: Landmarks on the Pathways of Life, Cambridge University Press, New York.
Ducluzeau A.-L., van Lis R., Duval S., Schoepp-Cothenet B., Russell M.J., and Nitschke W. (2009) Was nitric oxide the first deep electron sink? Trends Biochem Sci 34:9–15.
Duhr S. and Braun D. (2006) Why molecules move along a temperature gradient. Proc Natl Acad Sci USA 103:19678–19682.
Eck R.V. and Dayhoff M.O. (1966) Evolution of the structure of ferredoxin based on living relics of primitive amino acid sequences. Science 152:363–366.
Ettwig K.F., Butler M.K., Le Paslier D., Pelletier E., Mangenot S., Kuypers M.M.M., Schreiber F., Dutilh B.E., Zedelius J., de Beer D., Gloerich J., Wessels H.J., van Alen T., Luesken F., Wu M.L., van de Pas-Schoonen K.T., Op den Camp H.J., Janssen-Megens E.M., Francoijs K.J., Stunnenberg H., Weissenbach J., Jetten M.S., and Strous M. (2010) Nitrite-driven anaerobic methane oxidation by oxygenic bacteria. Nature 464:543–548.
Ferry J. (2010) How to make a living by exhaling methane. Annu Rev Microbiol 64:453–473.
Ferry J. and House C. (2006) The stepwise evolution of early life driven by energy conservation. Mol Biol Evol 23:1286–1292.
Foley S., Buhre S., and Jacob D. (2003) Evolution of the Archaean crust by delamination and shallow subduction. Nature 421:249–252.
Früh-Green G.L., Kelley D.S., Bernasconi S.M., Karson J.A., Ludwig K.A., Butterfield D.A., Boschi C., and Proskurowski G. (2003) 30,000 years of hydrothermal activity at the Lost City vent field. Science 301:495–498.
Fuchs G. (2011) Alternative pathways of carbon dioxide fixation: insights into the early evolution of life? Annu Rev Microbiol 65:631–658.
Fyfe W.S. (1995) The water inventory of the Earth: fluids and tectonics. In Geofluids: Origin, Migration and Evolution of Fluids in Sedimentary Basins, edited by Parnell J., Geological Society of London, London, pp 1–7.
Geptner A., Kristmannsdóttir H., Kristjansson J., and Marteinsson V. (2002) Biogenic saponite from an active submarine hot spring, Iceland. Clays Clay Miner 50:174–185.
German C.R. and Von Damm K.L. (2006) Hydrothermal processes. In The Oceans and Marine Geochemistry, Treatise on Geochemistry Vol. 6, edited by Elderfield H., Elsevier, Amsterdam, pp 181–222.
Goldschmidt V. (1952) Geochemical aspects of the origin of complex organic molecules on the Earth, as precursors to organic life. New Biology 12:97–105.
Harel A., Bromberg Y., Falkowski P.G., and Bhattacharya D. (2014) Evolutionary history of redox metal-binding domains across the tree of life. Proc Natl Acad Sci USA 111:7042–7047.
Harms U., Weiss D.S., Gartner P., Linder D., and Thauer R.K. (1995) The energy conserving N5-methyltetrahydromethanopterin:coenzyme M methyltransferase complex from Methanobacterium thermoautotrophicum is composed of eight different subunits. Eur J Biochem 228:640–648.
Hedderich R. (2004) Energy-converting [NiFe] hydrogenases from archaea and extremophiles: ancestors of complex I. J Bioenerg Biomembr 36:65–75.
Heinen W. and Lauwers A.M. (1996) 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.
Hennet R.J.-C., Holm N.G., and Engel M.H. (1992) Abiotic synthesis of amino acids under hydrothermal conditions and the origin of life: a perpetual phenomenon? Naturwissenschaften 79:361–365.
Herschy B., Whicher A., Camprubi E., Watson C., Dartnell L., Ward J., Evans J.R.G., and Lane N. (2014) An origin-of-life reactor to simulate alkaline hydrothermal vents. J Mol Evol 79:213–227.
Holm N.G. and Charlou J.L. (2001) Initial indications of abiotic formation of hydrocarbons in the Rainbow ultramafic hydrothermal system, Mid-Atlantic Ridge. Earth Planet Sci Lett 191:1–8.
Huber C. and Wächtershäuser G. (1997) Activated acetic acid by carbon fixation on (Fe, Ni) S under primordial conditions. Science 276:245–247.
Hulett H.R., Wolman Y., Miller S.L., Ibanez J., Oro J., Fox S.W., and Windsor C.R. (1971) Formaldehyde and ammonia as precursors to prebiotic amino acids. Science 174:1038–1041.
Jaffrés J.B.D., Shields G.A., and Wallmann K. (2007) The oxygen isotope evolution of seawater: a critical review of a long-standing controversy and an improved geological water cycle model for the past 3.4 billion years. Earth-Science Reviews 83:83–122.
Joye S.B. (2012) Microbiology: a piece of the methane puzzle. Nature 491:538–539.
Kaster A.-K., Moll J., Parey K., and Thauer R.K. (2011) Coupling of ferredoxin and heterodisulfide reduction via electron bifurcation in hydrogenotrophic methanogenic archaea. Proc Natl Acad Sci USA 108:2981–2986.
Kasting J.F. (2010) Early earth: faint young Sun redux. Nature 464:687–689.
Keller M.A., Turchyn A.V., and Ralser M. (2014) Non-enzymatic glycolysis and pentose phosphate pathway-like reactions in a plausible Archean ocean. Mol Syst Biol 10.
Kelley D.S., Karson J.A., Blackman D.K., Früh-Green G.L., Butterfield D.A., Lilley M.D., Olson E.J., Schrenk M.O., Roe K.K., Lebon G.T., Rivizzigno P.; AT3-60 Shipboard Party. (2001) An off-axis hydrothermal vent field near the Mid-Atlantic Ridge at 30 degrees N. Nature 412:145–149.
Kelley D.S., Baross J.A., and Delaney J.R. (2002) Volcanoes, fluids, and life at mid-ocean ridge spreading centers. Annu Rev Earth Planet Sci 30:385–491.
Kelley D.S., Karson J.A, Früh-Green G.L., Yoerger D.R., Shank T.M., Butterfield D.A, Hayes J.M., Schrenk M.O., Olson E.J., Proskurowski G., Jakuba M., Bradley A., Larson B., Ludwig K., Glickson D., Buckman K., Bradley A.S., Brazelton W.J., Roe K., Elend M.J., Delacour A., Bernasconi S.M., Lilley M.D., Baross J.A., Summons R.E., and Sylva S.P. (2005) A serpentinite-hosted ecosystem: the Lost City hydrothermal field. Science 307:1428–1434.
Kelly S., Wickstead B., and Gull K. (2011) Archaeal phylogenomics provides evidence in support of a methanogenic origin of the Archaea and a thaumarchaeal origin for the eukaryotes. Proc Biol Sci 278:1009–1018.
Kim J., Senn S., Harel A., Jelen B.I., and Falkowski P.G. (2013) Discovering the electronic circuit diagram of life: structural relationships among transition metal binding sites in oxidoreductases. Philos Trans R Soc Lond B Biol Sci 368:1–9.
Koga Y., Kyuragi T., Nishihara M., and Sone N. (1998) Did archaeal and bacterial cells arise independently from noncellular precursors? A hypothesis stating that the advent of membrane phospholipid with enantiomeric glycerophosphate backbones caused the separation of the two lines of descent. J Mol Evol 46:54–63.
Konn C., Charlou J.L., Donval J.P., Holm N.G., Dehairs F., and Bouillon S. (2009) Hydrocarbons and oxidized organic compounds in hydrothermal fluids from Rainbow and Lost City ultramafic-hosted vents. Chem Geol 258:299–314.
Lane N. (2014) Bioenergetic constraints on the evolution of complex life. Cold Spring Harb Perspect Biol 6.
Lane N. (2015) The Vital Question: Energy, Evolution, and the Origins of Complex Life, WW Norton & Co., New York.
Lane N. and Martin W.F. (2012) The origin of membrane bioenergetics. Cell 151:1406–1416.
Lane N., Allen J.F., and Martin W. (2010) How did LUCA make a living? Chemiosmosis in the origin of life. BioEssays 32:271–280.
Lang S.Q., Früh-Green G.L., Bernasconi S.M., Lilley M.D., Proskurowski G., Méhay S., and Butterfield D.A. (2012) Microbial utilization of abiogenic carbon and hydrogen in a serpentinite-hosted system. Geochim Cosmochim Acta 92:82–99.
Li F., Hinderberger J., Seedorf H., Zhang J., Buckel W., and Thauer R.K. (2008) Coupled ferredoxin and crotonyl coenzyme A (CoA) reduction with NADH catalyzed by the butyryl-CoA dehydrogenase/Etf complex from Clostridium kluyveri. J Bacteriol 190:843–850.
Lomans B.P., Maas R., Luderer R., Op den Camp H.J.M., Pol A., van der Drift C., and Vogels G.D. (1999) Isolation and characterization of Methanomethylovorans hollandica gen. nov., sp. nov., isolated from freshwater sediment, a methylotrophic methanogen able to grow on dimethyl sulfide and methanethiol. Appl Environ Microbiol 65:3641–3650.
Lomans B.P., van der Drift C., Pol A., and Op den Camp H.J.M. (2002) Microbial cycling of volatile organic sulfur compounds. Cell Mol Life Sci 59:575–588.
Lowell R.P., Rona P.A., and Von Herzen R.P. (1995) Seafloor hydrothermal systems. J Geophys Res 100:327–352.
Ludwig K.A., Kelley D.S., Shen C., Cheng H., and Edwards R.L. (2005) U/Th geochronology of carbonate chimneys at the Lost City hydrothermal field [abstract #V51B–1487]. In American Geophysical Union Fall Meeting 2005, American Geophysical Union, Washington, DC.
Ludwig K.A., Kelley D.S., Butterfield D.A., Nelson B.K., and Früh-Green G. (2006) Formation and evolution of carbonate chimneys at the Lost City hydrothermal field. Geochim Cosmochim Acta 70:3625–3645.
Macdonald A.H. and Fyfe W.S. (1985) Rate of serpentinization in seafloor environments. Techtonophysics 116:123–135.
Maden B. (1995) No soup for starters? Autotrophy and the origins of metabolism. Trends Biochem Sci 20:337–341.
Maden B.E. (2000) Tetrahydrofolate and tetrahydromethanopterin compared: functionally distinct carriers in C1 metabolism. Biochem J 350:609–629.
Major T.A., Burd H., and Whitman W.B. (2004) Abundance of 4Fe-4S motifs in the genomes of methanogens and other prokaryotes. FEMS Microbiol Lett 239:117–123.
Marteinsson V.T., Kristjánsson J.K., Kristmannsdóttir H., Dahlkvist M., Sæmundsson K., Hannington M., Pétursdóttir S.K., Geptner A., and Stoffers P. (2001) Discovery and description of giant submarine smectite cones on the seafloor in Eyjafjordur, northern Iceland, and a novel thermal microbial habitat. Appl Environ Microbiol 67:827–833.
Martin W. and Russell M.J. (2003) On the origins of cells: a hypothesis for the evolutionary transitions from abiotic geochemistry to chemoautotrophic prokaryotes, and from prokaryotes to nucleated cells. Philos Trans R Soc Lond B Biol Sci 358:59–83.
Martin W. and Russell M.J. (2007) On the origin of biochemistry at an alkaline hydrothermal vent. Philos Trans R Soc Lond B Biol Sci 362:1887–1925.
Martin W., Baross J., Kelley D., and Russell M.J. (2008) Hydrothermal vents and the origin of life. Nat Rev Microbiol 6:805–814.
Martin W.F. (2011) Early evolution without a tree of life. Biol Direct 6.
Martin W.F. (2012) Hydrogen, metals, bifurcating electrons, and proton gradients: the early evolution of biological energy conservation. FEBS Lett 586:485–493.
Martin W.F., Sousa F.L., and Lane N. (2014) Energy at life's origin. Science 344:1092–1093.
Mast C.B. and Braun D. (2010) Thermal trap for DNA replication. Phys Rev Lett 104:188102.
Mast C.B., Schink S., Gerland U., and Braun D. (2013) Escalation of polymerization in a thermal gradient. Proc Natl Acad Sci USA 110:8030–8035.
Matthews R.G. and Drummond J.T. (1990) Providing one-carbon units for biological methylations: mechanistic studies on serine hydroxymethyltransferase, methylenetetrahydrofolate reductase, and methyltetrahydrofolate-homocysteine methyltransferase. Chem Rev 90:1275–1290.
McCollom T.M. (2013a) Miller-Urey and beyond: what have we learned about prebiotic organic synthesis reactions in the past 60 years? Annu Rev Earth Planet Sci 41:207–229.
McCollom T.M. (2013b) Laboratory simulations of abiotic hydrocarbon formation in Earth's deep subsurface. Reviews in Mineralogy and Geochemistry 75:467–494.
McCollom T.M. and Bach W. (2009) Thermodynamic constraints on hydrogen generation during serpentinization of ultramafic rocks. Geochim Cosmochim Acta 73:856–875.
McDermott J.M., Seewald J.S., German C.R., and Sylva S.P. (2015) Pathways for abiotic organic synthesis at submarine hydrothermal fields. Proc Natl Acad Sci USA 112:7668–7672.
Miller S.L. (1953) A production of amino acids under possible primitive Earth conditions. Science 117:528–529.
Mitchell P. (1957) The origin of life and the formation and organising functions of natural membranes. In Proceedings of the First International Symposium on the Origin of Life on the Earth, edited by Oparin A.I., Pasynskii A.G., Braunshtein A.E., and Pavlovskaya T.E., Academy of Sciences (USSR), Moscow, pp 229–234.
Mitchell P. (1961) Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism. Nature 191:144–148.
Mitchell P. (1966) Chemiosmotic coupling in oxidative and photosynthetic phosphorylation. Biol Rev 41:444–501.
Miyakawa S., Yamanashi H., Kobayashi K., Cleaves H.J., and Miller S.L. (2002) Prebiotic synthesis from CO atmospheres: implications for the origins of life. Proc Natl Acad Sci USA 99:14628–14631.
Mloszewska A.M., Pecoits E., Cates N.L., Mojzsis S.J., O'Neil J., Robbins L.J., and Konhauser K.O. (2012) The composition of Earth's oldest iron formations: the Nuvvuagittuq Supracrustal Belt (Québec, Canada). Earth Planet Sci Lett 317–318:331–342.
Moran J.J., Beal E.J., Vrentas J.M., Orphan V.J., Freeman K.H., and House C.H. (2008) Methyl sulfides as intermediates in the anaerobic oxidation of methane. Environ Microbiol 10:162–173.
Müller V., Imkamp F., Biegel E., Schmidt S., and Dilling S. (2008) Discovery of a ferredoxin:NAD+-oxidoreductase (Rnf) in Acetobacterium woodii: a novel potential coupling site in acetogens. Ann NY Acad Sci 1125:137–146.
Ni S., Woese C.R., Aldrich H.C., and Boone D.R. (1994) Transfer of Methanolobus siciliae to the genus Methanosarcina, naming it Methanosarcina siciliae, and emendation of the genus Methanosarcina. Int J Syst Bacteriol 44:357–359.
Nicholls D.G. and Ferguson S.J. (2013) Bioenergetics, Academic Press, London.
Nitschke W. and Russell M. (2013) Beating the acetyl coenzyme A pathway to the origin of life. Philos Trans R Soc Lond B Biol Sci 368.
Nitschke W. and Russell M.J. (2009) Hydrothermal focusing of chemical and chemiosmotic energy, supported by delivery of catalytic Fe, Ni, Mo/W, Co, S and Se, forced life to emerge. J Mol Evol 69:481–496.
Nitschke W. and Russell M.J. (2012) Redox bifurcations: mechanisms and importance to life now, and at its origin. BioEssays 34:106–109.
Oparin A.I. (1938) The Origin of Life, Macmillan, New York.
Oremland R.S. and Boone D.R. (1994) Methanolobus taylorii sp. nov., a new methylotrophic, estuarine methanogen. Int J Syst Bacteriol 44:573–575.
Orgel L.E. (2008) The implausibility of metabolic cycles on the prebiotic Earth. PLoS Biol 6.
Oro’ J., Kimball A., Fritz R., and Master F. (1959) Amino acid synthesis from formaldehyde and hydroxylamine. Arch Biochem Biophys 85:115–130.
Patel B.H., Percivalle C., Ritson D.J., Duffy C.D., and Sutherland J.D. (2015) Common origins of RNA, protein and lipid precursors in a cyanosulfidic protometabolism. Nat Chem 7:301–307.
Petitjean C., Deschamps P., Lopez-Garcia P., and Moreira D. (2014) Rooting the domain Archaea by phylogenomic analysis supports the foundation of the new kingdom Proteoarchaeota. Genome Biol Evol 7:191–204.
Pinti D. (2005) The origin and evolution of the oceans. In Lectures in Astrobiology, Vol. 1, edited by Gargaud M., Barbier B., Martin H., and Reisse J., Springer, Berlin, pp 83–112.
Poehlein A., Schmidt S., Kaster A.-K., Goenrich M., Vollmers J., Thürmer A., Bertsch J., Schuchmann K., Voigt B., Hecker M., Daniel R., Thauer R.K., Gottschalk G., and Müller V. (2012) An ancient pathway combining carbon dioxide fixation with the generation and utilization of a sodium ion gradient for ATP synthesis. PLoS One 7.
Powner M.W., Gerland B., and Sutherland J.D. (2009) Synthesis of activated pyrimidine ribonucleotides in prebiotically plausible conditions. Nature 459:239–242.
Proskurowski G., Lilley M.D., Kelley D.S., and Olson E.J. (2006) Low temperature volatile production at the Lost City hydrothermal field, evidence from a hydrogen stable isotope geothermometer. Chem Geol 229:331–343.
Proskurowski G., Lilley M.D., Seewald J.S., Früh-Green G.L., Olson E.J., Lupton J.E., Sylva S.P., and Kelley D.S. (2008) Abiogenic hydrocarbon production at Lost City hydrothermal field. Science 319:604–607.
Ragsdale S.W. and Pierce E. (2008) Acetogenesis and the Wood-Ljungdahl pathway of CO2 fixation. Biochim Biophys Acta 1784:1873–1898.
Raymann K., Brochier-Armanet C., and Gribaldo S. (2015) The two-domain tree of life is linked to a new root for the Archaea. Proc Natl Acad Sci USA 112:6670–6675.
Reeves E.P., McDermott J.M., and Seewald J.S. (2014) The origin of methanethiol in mid-ocean ridge hydrothermal fluids. Proc Natl Acad Sci USA 111:5474–5479.
Roldan A., Hollingsworth N., Roffey A., Islam H.-U., Goodall J.B.M., Catlow C.R.A., Darr J.A., Bras W., Sankar G., Holt K.B., Hogarth G., and de Leeuw N.H. (2015) Bio-inspired CO2 conversion by iron sulfide catalysts under sustainable conditions. Chem Commun 51:7501–7504.
Russell M. (2003) The importance of being alkaline. Science 302:580–581.
Russell M.J. and Arndt N.T. (2005) Geodynamic and metabolic cycles in the Hadean. Biogeosciences 2:97–111.
Russell M.J. and Hall A.J. (1997) The emergence of life from iron monosulphide bubbles at a submarine hydrothermal redox and pH front. J Geol Soc London 154:377–402.
Russell M.J. and Martin W. (2004) The rocky roots of the acetyl-CoA pathway. Trends Biochem Sci 29:358–363.
Russell M.J., Hall A.J., and Turner D. (1989) In vitro growth of iron sulphide chimneys: possible culture chambers for origin-of-life experiments. Terra Nova 1:238–241.
Russell M.J., Daniel R.M., and Hall A.J. (1993) On the emergence of life via catalytic iron-sulphide membranes. Terra Nova 5:343–347.
Russell M.J., Daniel R.M., Hall A.J., and Sherringham J.A. (1994) A hydrothermally precipitated catalytic iron sulphide membrane as a first step toward life. J Mol Evol 39:231–243.
Russell M.J., Hall A.J., and Martin W. (2010) Serpentinization as a source of energy at the origin of life. Geobiology 8:355–371.
Russell M.J., Barge L.M., Bhartia R., Bocanegra D., Bracher P.J., Branscomb E., Kidd R., McGlynn S., Meier D.H., Nitschke W., Shibuya T., Vance S., White L., and Kanik I. (2014) The drive to life on wet and icy worlds. Astrobiology 14:308–343.
Sagan C. and Mullen G. (1972) Earth and Mars: evolution of atmospheres and surface temperatures. Science 177:52–56.
Saladino R., Crestini C., Pino S., Costanzo G., and Di Mauro E. (2012) Formamide and the origin of life. Phys Life Rev 9:84–104.
Scheller S., Goenrich M., Boecher R., Thauer R.K., and Jaun B. (2010) The key nickel enzyme of methanogenesis catalyses the anaerobic oxidation of methane. Nature 465:606–608.
Schoepp-Cothenet B., van Lis R., Atteia A., Baymann F., Capowiez L., Ducluzeau A.-L., Duval S., ten Brink F., Russell M.J., and Nitschke W. (2013) On the universal core of bioenergetics. Biochim Biophys Acta 1827:79–93.
Schuchmann K. and Müller V. (2014) Autotrophy at the thermodynamic limit of life: a model for energy conservation in acetogenic bacteria. Nat Rev Microbiol 12:809–821.
Seyfried W.E., Pester N.J., Tutolo B.M., and Ding K. (2015) The Lost City hydrothermal system: constraints imposed by vent fluid chemistry and reaction path models on subseafloor heat and mass transfer processes. Geochim Cosmochim Acta 163:59–79.
Shields G.A. and Kasting J.F. (2007) Evidence for hot early oceans? Nature 447:E1–E2.
Shock E. and Canovas P. (2010) The potential for abiotic organic synthesis and biosynthesis at seafloor hydrothermal systems. Geofluids 10:161–192.
Shock E.L., McCollom T.M., and Schulte M.D. (1998) The emergence of metabolism from within hydrothermal systems. In Thermophiles: The Keys to Molecular Evolution and the Origin of Life? edited by Wiegel J. and Adams M.W.W., Taylor & Francis, London, pp 59–76.
Sleep N.H. (2010) The Hadean-Archaean environment. Cold Spring Harb Perspect Biol 2.
Sleep N.H., Meibom A., Fridriksson T., Coleman R.G., and Bird D.K. (2004) H2-rich fluids from serpentinization: geochemical and biotic implications. Proc Natl Acad Sci USA 101:12818–12823.
Sleep N.H., Bird D.K., and Pope E.C. (2011) Serpentinite and the dawn of life. Philos Trans R Soc Lond B Biol Sci 366:2857–2869.
Sojo V. (2015) On the biogenic origins of homochirality. Orig Life Evol Biosph 45:219–224.
Sojo V., Pomiankowski A., and Lane N. (2014) A bioenergetic basis for membrane divergence in archaea and bacteria. PLoS Biol 12.
Sousa F.L. and Martin W.F. (2014) Biochemical fossils of the ancient transition from geoenergetics to bioenergetics in prokaryotic one carbon compound metabolism. Biochim Biophys Acta 1837:964–981.
Sousa F.L., Thiergart T., Landan G., Nelson-Sathi S., Pereira I.A.C., Allen J.F., Lane N., and Martin W.F. (2013) Early bioenergetic evolution. Philos Trans R Soc Lond B Biol Sci 368:1–30.
Staben C. and Rabinowitz J. (1984) Formation of formylmethionyl-tRNA and initiation of protein synthesis. In Folates and Pterins, Vol. I: Chemistry and Biochemistry of Folates, edited by Blakley R.L. and Benkovic S.J., Wiley, New York, pp 457–495.
Stetter K.O. (2006) Hyperthermophiles in the history of life. Philos Trans R Soc Lond B Biol Sci 361:1837–1842.
Summers D.P. (2005) Ammonia formation by the reduction of nitrite/nitrate by FeS: ammonia formation under acidic conditions. Orig Life Evol Biosph 35:299–312.
Summers D.P. and Chang S. (1993) Prebiotic ammonia from reduction of nitrite by iron(II) on the early Earth. Nature 365:630–633.
Surín S., Cubonová L., Majerník A.I., McDermott P., Chong J.P.J., and Smigán P. (2007) Isolation and characterization of an amiloride-resistant mutant of Methanothermobacter thermautotrophicus possessing a defective Na+/H+ antiport. FEMS Microbiol Lett 269:301–308.
Thauer R.K. (2011) Anaerobic oxidation of methane with sulfate: on the reversibility of the reactions that are catalyzed by enzymes also involved in methanogenesis from CO2. Curr Opin Microbiol 14:292–299.
Thauer R.K., Jungermann K., and Decker K. (1977) Energy conservation in chemotrophic anaerobic bacteria. Bacteriol Rev 41:100–180.
Thauer R.K., Kaster A.-K., Seedorf H., Buckel W., and Hedderich R. (2008) Methanogenic archaea: ecologically relevant differences in energy conservation. Nat Rev Microbiol 6:579–591.
Tivey M.K. (2007) Generation of seafloor hydrothermal vent fluids and associated mineral deposits. Oceanography 20:50–65.
Trail D., Watson E.B., and Tailby N.D. (2011) The oxidation state of Hadean magmas and implications for early Earth's atmosphere. Nature 480:79–82.
Vidová M., Bobáľová J., and Šmigáň P. (2011) Harmaline-resistant mutant of Methanothermobacter thermautotrophicus with a lesion in Na+/H+ antiport. Gen Physiol Biophys 30:54–60.
Von Damm K.L. (1990) Seafloor hydrothermal activity: black smoker chemistry and chimneys. Annu Rev Earth Planet Sci 18:173–204.
Wächtershäuser G. (1988) Pyrite formation, the first energy source for life: a hypothesis. Syst Appl Microbiol 10:207–210.
Wächtershäuser G. (2000) Life as we don't know it. Science 289:1307–1308.
White L.M., Bhartia R., Stucky G.D., Kanik I., and Russell M.J. (2015) Mackinawite and greigite in ancient alkaline hydrothermal chimneys: identifying potential key catalysts for emergent life. Earth Planet Sci Lett 430:105–114.
Williams T.A. and Embley T.M. (2014) Archaeal “dark matter” and the origin of eukaryotes. Genome Biol Evol 6:474–481.
Williams T.A., Foster P.G., Nye T.M.W., Cox C.J., and Embley T.M. (2012) A congruent phylogenomic signal places eukaryotes within the Archaea. Proc Biol Sci 279:4870–4879.
Yamaguchi A., Yamamoto M., Takai K., Ishii T., Hashimoto K., and Nakamura R. (2014) Electrochemical CO2 reduction by Ni-containing iron sulfides: how is CO2 electrochemically reduced at bisulfide-bearing deep-sea hydrothermal precipitates? Electrochim Acta 141:311–318.
Zahnle K., Arndt N., Cockell C., Halliday A., Nisbet E., Selsis F., and Sleep N.H. (2007) Emergence of a habitable planet. Space Sci Rev 129:35–78.
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Copyright 2016, Mary Ann Liebert, Inc.
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Published online: 16 February 2016
Published ahead of print: 3 February 2016
Published in print: February 2016
Accepted: 12 January 2016
Received: 9 September 2015
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