Journal of Molecular Evolution

, Volume 69, Issue 5, pp 481–496 | Cite as

Hydrothermal Focusing of Chemical and Chemiosmotic Energy, Supported by Delivery of Catalytic Fe, Ni, Mo/W, Co, S and Se, Forced Life to Emerge

  • Wolfgang Nitschke
  • Michael J. RussellEmail author


Energised by the protonmotive force and with the intervention of inorganic catalysts, at base Life reacts hydrogen from a variety of sources with atmospheric carbon dioxide. It seems inescapable that life emerged to fulfil the same role (i.e., to hydrogenate CO2) on the early Earth, thus outcompeting the slow geochemical reduction to methane. Life would have done so where hydrothermal hydrogen interfaced a carbonic ocean through inorganic precipitate membranes. Thus we argue that the first carbon-fixing reaction was the molybdenum-dependent, proton-translocating formate hydrogenlyase system described by Andrews et al. (Microbiology 143:3633–3647, 1997), but driven in reverse. Alkaline on the inside and acidic and carbonic on the outside - a submarine chambered hydrothermal mound built above an alkaline hydrothermal spring of long duration - offered just the conditions for such a reverse reaction imposed by the ambient protonmotive force. Assisted by the same inorganic catalysts and potential energy stores that were to evolve into the active centres of enzymes supplied variously from ocean or hydrothermal system, the formate reaction enabled the rest of the acetyl coenzyme-A pathway to be followed exergonically, first to acetate, then separately to methane. Thus the two prokaryotic domains both emerged within the hydrothermal mound—the acetogens were the forerunners of the Bacteria and the methanogens were the forerunners of the Archaea.


Origin of life Hydrothermal vent Chemiosmosis Chemoautotrophy LUCA 



We thank Anne-Lise Ducluzeau, Allan Hall, Isik Kanik, Bill Martin, Randall Mielke, Shawn McGlynn, Carola Schulzke and Anne Volbeda for help and support. WN was financially supported by the French Agence Nationale pour la Recherche (ANR-06-BLAN-0384). MJR’s research was carried out at the Jet Propulsion Laboratory, California Institute of Technology, under a contract with the National Aeronautics and Space Administration: Exobiology and Evolutionary Biology and supported by NASA’s Astrobiology Institute (Icy Worlds).


  1. Anbar AD (2008) Elements and evolution. Science 322:1481–1483PubMedGoogle Scholar
  2. Andrews SC, Berkst BC, McClay J, Amblert A, Quail MA, Golby P, Guest JR (1997) A 12-cistron Escherichia coli operon (huf) encoding a putative proton-translocating formate hydrogenlyase system. Microbiology 143:3633–3647PubMedGoogle Scholar
  3. Bada JL, Lazcano A (2003) Prebiotic soup—revisiting the Miller experiment. Science 300:745–746PubMedGoogle Scholar
  4. Bagramyan K, Trchounian A (2003) Structural and functional features of formate hydrogen lyase, an enzyme of mixed acid fermentation from Escherichia coli. Biochemistry (Moscow) 68:1445–1458Google Scholar
  5. Baltscheffsky M (1967) Inorganic pyrophosphatase and ATP as energy donors in chromatophores from Rhodospirillum rubrum. Nature 216:241–243PubMedGoogle Scholar
  6. Baltscheffsky H (1996) Energy conversion leading to the origin and early evolution of life: did inorganic pyrophosphate precede adenosine triphosphate? In: Baltscheffsky H (ed) Origin and evolution of biological energy conversion. VCH Publishers, Cambridge, pp 1–9Google Scholar
  7. Baltscheffsky H, von Stedingk LV, Heldt H-W, Baltscheffsky M (1966) Inorganic pyrophosphate: formation in bacterial photophosphorylation. Science 153:1120–1122PubMedGoogle Scholar
  8. Baltscheffsky M, Schultz A, Baltscheffsky H (1999) H+-PPases: a tightly membrane-bound family. FEBS Lett 457:527–533PubMedGoogle Scholar
  9. Baltscheffsky H, Perrson B, Schultz A, Pérez-Castiñeira JR, Baltscheffsky M (2004) Origin and evolution of very early sequence motifs in enzymes. In: Seckbach J et al (eds) Life in the universe. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 107–110Google Scholar
  10. Baymann F, Lebrun E, Brugna M, Schoepp-Cothenet B, Giudici-Orticoni MT, Nitschke W (2003) The redox construction kit: pre-LUCA evolution of energy-conserving enzymes. Philos Trans R Soc Lond B358:267–274Google Scholar
  11. Beinert H, Holm RH, Münck E (1997) Iron–sulfur clusters: nature’s modular, multipurpose structures. Science 277:653–659PubMedGoogle Scholar
  12. Bethke C (1996) Geochemical reaction modeling. Oxford University Press, OxfordGoogle Scholar
  13. Beverskog B, Puigdomenech I (1997) Revised Pourbaix diagrams for nickel at 25–300°C. Corros Sci 39:969–980Google Scholar
  14. Bonomi F, Werth MT, Kurtz DM (1985) Assembly of FenSn(SR)2- (n = 2, 4) in aqueous media from iron salts, thiols and sulfur, sulfide, thiosulfide plus rhodonase. Inorg Chem 24:4331–4335Google Scholar
  15. Boone DR, Castenholz RW, Garrity G (eds) (2001) Bergey’s manual of systematic bacteriology, the archaea, photosynthetic bacteria, and deeply branched bacteria, vol 1, 2nd edn. Springer Verlag, BerlinGoogle Scholar
  16. Boyington C, Gladyshev VD, Khangulov V, Stadtman TC, Sun PD (1997) Crystal structure of formate dehydrogenase H: catalysis involving Mo, molybdopterin, selenocysteine, and an 4Fe4S cluster. Science 275:1305–1308PubMedGoogle Scholar
  17. Braterman PS, Cairns-Smith AG (1983) Photo-oxidation of hydrated Fe2+-significance for banded iron formations. Nature 303:163–164Google Scholar
  18. Brugna-Guiral M, Tron P, Nitschke W, Stetter KO, Burlat B, Guigliarelli B, Bruschi M, Giudici-Orticoni M-T (2003) [NiFe] hydrogenases from the hyperthermophilic bacterium Aquifex aeolicus: properties, function and phylogenetics. Extremophiles 7:145–157PubMedGoogle Scholar
  19. Coleman M, Ader M, Chaudhuri SK, Coates JD (2003) Microbial isotopic fractionation of perchlorate chlorine. Appl Environ Microbiol 69:4997–5000PubMedGoogle Scholar
  20. Crofts AR, Meinhardt SW, Jones KR, Snozzi M (1983) The role of the quinone pool in the cyclic electron-transfer chain Rhodopseudomonas sphaeroides. Biochim Biophys Acta 723:202–218Google Scholar
  21. da Silva JJRF, Williams RJP (1991) The biological chemistry of the elements. Clarendon Press, OxfordGoogle Scholar
  22. Darwin CR (1872) Origin of species by natural selection, 6th edn. John Murray, LondonGoogle Scholar
  23. Davis BK (2005) Coevolution theory of the genetic code: is the precursor–product hypothesis invalid? Bioessays 27:1308–1309PubMedGoogle Scholar
  24. de Zwart II, Meade SJ, Pratt AJ (2004) Biomimetic phosphoryl transfer catalysed by iron(II)-mineral precipitates. Geochim Cosmochim Acta 68:4093–4098Google Scholar
  25. Di Giulio M (2003) The early phases of genetic code origin: conjectures on the evolution of coded catalysis. Orig Life Evol Biosph 33:479–489PubMedGoogle Scholar
  26. Di Giulio M (2008) An extension of the coevolution theory of the origin of the genetic code. Biol Direct 3:37PubMedGoogle Scholar
  27. Doolittle WF (1999) Phylogenetic classification and the universal tree. Science 284:2124–2129PubMedGoogle Scholar
  28. Drozdowicz YM, Rea PA (2001) Vacuolar H+-pyrophosphatases: from the evolutionary backwaters into the mainstream. Trends Plant Sci 6:206–211PubMedGoogle Scholar
  29. Ducluzeau A-L (2009) Origine enzymatique de la respiration aerobie. PhD thesis, Université de Provence, pp 356Google Scholar
  30. Ducluzeau A-L, Ouchane S, Nitschke W (2008) The cbb 3 oxidases are an ancient innovation of the domain Bacteria. Mol Biol Evol 25:1158–1166PubMedGoogle Scholar
  31. Ducluzeau A-L, van Lis R, Duval S, Schoepp-Cothenet B, Russell MJ, Nitschke W (2009) Was nitric oxide the first deep electron sink? Trends Biochem Sci 34:9–15PubMedGoogle Scholar
  32. Duval S, Ducluzeau A-L, Nitschke W, Schoepp-Cothenet B (2008) Enzyme phylogenies as markers for the oxidation state of the environment: the case of the respiratory arsenate reductase and related enzymes. BMC Evol Biol 8:206–219PubMedGoogle Scholar
  33. Elston T, Wang H, Oster G (1998) Energy transduction in ATP synthase. Nature 391:510–513PubMedGoogle Scholar
  34. Erickson BE, Helz GR (2000) Molybdenum (VI) speciation in sulfidic waters: stability and lability of thiomolybdates. Geochim Cosmochim Acta 64:1149–1158Google Scholar
  35. Forterre P (2002) The origin of DNA genomes and DNA replication proteins. Curr Opin Microbiol 5:525–532PubMedGoogle Scholar
  36. Fuchs G (1989) Alternative pathways of autotrophic CO2 fixation. In: Schlegel HG, Bowen B (eds) Autotrophic bacteria. Science Technology, Madison, WI, pp 365–382Google Scholar
  37. Goldschmidt VM (1952) Geochemical aspects of the origin of complex organic molecules on Earth, as precursors to organic life. New Biol 12:97–105Google Scholar
  38. Haeckel E (1870) Natürliche Schöpfungsgeschichte: Gemeinverständliche wissenschaftliche Vorträge über die Entwicklungslehre im allgemeinen und diejenige von Darwin, Goethe und Lamarck im besonderen, über die Anwendung derselben auf den Ursprung des Menschen und andere damit zusammenhängende Grundfragen der Naturwissenschaft. Georg Reimer, Berlin, p 688Google Scholar
  39. Haeckel E (1876) The history of creation: or the development of the Earth and its inhabitants by the action of natural causes, a popular exposition of evolution in general, and that of Darwin, Goethe and Lamark in particular vol 1, (trans: Lankester ER). Henry S. King & Co., London, p 374Google Scholar
  40. Hagan WJ, Parker A, Steuerwald A, Hathaway M (2007) Phosphate solubility and the cyanate-mediated synthesis of pyrophosphate. Orig Life Evol Biosph 37:113–122PubMedGoogle Scholar
  41. Harvey RB (1924) Enzymes of thermal algae. Science 50:481–482Google Scholar
  42. Hedderich R, Klimmeck O, Kröger A, Dirmeier R, Keller M, Stetter KO (1999) Anaerobic respiration with elemental sulfur and with disulfides. FEMS Microbiol Rev 22:353–381Google Scholar
  43. Hedlund J, Cantoni R, Baltscheffsky M, Baltscheffsky H, Persson B (2006) Analysis of ancient sequence motifs in the H+-PPase family. FEBS J 273:5183–5193PubMedGoogle Scholar
  44. Helz GR, Miller CV, Charnock JM, Mosselmans JFW, Pattrick RAD, Garner CD, Vaughan DJ (1996) Mechanism of molybdenum removal from the sea and its concentration in black shales. EXAFS evidence. Geochimica Cosmochimica Acta 60:3631–3642Google Scholar
  45. Hennet RJ-C, Holm NG, Engel MH (1992) Abiotic synthesis of amino acids under hydrothermal conditions and the origin of life: a perpetual phenomenon? Naturwissenschaften 79:361–365PubMedGoogle Scholar
  46. Hirono M, Nakanishi Y, Maeshima M (2007) Essential amino acid residues in the central transmembrane domains and loops for energy coupling of Streptomyces coelicolor A3(2) H+-pyrophosphatase. Biochim Biophys Acta 1767:930–939PubMedGoogle Scholar
  47. Huber C, Wächtershäuser G (2003) Primordial reductive amination revisited. Tetrahedron Lett 44:1695–1697Google Scholar
  48. Huber C, Eisenreich W, Hecht S, Wächtershäuser G (2003) A possible primordial peptide cycle. Science 301:938–940PubMedGoogle Scholar
  49. Hurt E, Hauska G (1982) Involvement of plastoquinone bound within the isolated cytochrome b6f complex from chloroplasts in oxidant-induced reduction of cytochrome b6. Biochim Biophys Acta 682:466–473Google Scholar
  50. Jones CM, Stres B, Rosenquist M, Hallin S (2008) Phylogenetic analysis of nitrite, nitric oxide, and nitrous oxide respiratory enzymes reveal a complex evolutionary history for denitrification. Mol Biol Evol 25:1955–1966PubMedGoogle Scholar
  51. Konhauser KO, Pecoits E, Lalonde SV, Papineau D, Nisbet EG, Barley ME, Arndt NT, Zahnle K, Kamber BS (2009) Oceanic nickel depletion and a methanogen famine before the Great Oxidation Event. Nature 458:750–753PubMedGoogle Scholar
  52. Koonin E, Martin W (2005) On the origin of genomes and cells within inorganic compartments. Trends Genet 21:647–654PubMedGoogle Scholar
  53. Krumholz LR, Harris SH, Tay ST, Suflita JM (1999) Characterization of two subsurface H2-utilizing bacteria, Desulfomicrobium hypogeium sp. nov. and Acetobacterium psammolithicum sp. nov., and their ecological roles. Appl Environ Microbiol 65:2300–2306PubMedGoogle Scholar
  54. Lang SQ, Butterfield D, Lilley M (2007) Organic geochemistry of lost city hydrothermal fluids. InterRidge Theoretical Institute ‘Biogeochemical interaction at deep-sea vents’. Abstract (
  55. Lebrun E, Brugna M, Baymann F, Muller D, Lièvremont D, Lett MC, Nitschke W (2003) Arsenite oxidase, an ancient bioenergetic enzyme. Mol Biol Evol 20:686–693PubMedGoogle Scholar
  56. Leduc S (1911) The mechanism of life. Rebman Ltd, LondonGoogle Scholar
  57. Lolkema JS, Chaban Y, Boekema EJ (2003) Subunit composition, structure, and distribution of bacterial V-type ATPases. J Bioenerg Biomembr 35:323–335PubMedGoogle Scholar
  58. Maden BEH (2000) Tetrahydrofolate and tetrahydromethanopterin compared: functionally distinct carriers in C1 metabolism. Biochem J 350:609–629PubMedGoogle Scholar
  59. Madigan MT, Martinko JM, Dunlap DP, Clark DP (2008) Brock biology of microorganisms, 12th edn. Benjamin Cummings, San FranciscoGoogle Scholar
  60. Marshall WL (1994) Hydrothermal synthesis of amino acids. Geochim Cosmochim Acta 58:2099–2106Google Scholar
  61. Martin W, Russell MJ (2007) On the origin of biochemistry at an alkaline hydrothermal vent. Philos Trans R Soc B362:1887–1925Google Scholar
  62. Martin RS, Mather TA, Pyle DM (2007) Volcanic emissions and the early Earth atmosphere. Geochim Cosmochim Acta 71:3673–3685Google Scholar
  63. Mat W, Xue H, Wong JT (2008) The genomics of LUCA. Front Biosci 13:5605–5613PubMedGoogle Scholar
  64. McGlynn SH, Mulder DW, Shepard EM, Broderick JB, Peters JW (2009) Hydrogenase cluster biosynthesis: organometallic chemistry nature’s way. Dalton Trans 22:4274–4285PubMedGoogle Scholar
  65. Mereschkowsky C (1910) Theorie der zwei Plasmaarten als Grundlage der Symbiogenesis, einer neuen Lehre von der Entstehung der Organismen. Biol Centralbl 30: 278–303, 321–347, 353–367Google Scholar
  66. Milner-White EJ, Russell MJ (2008) Predicting the conformations of peptides and proteins in early evolution. Biol Direct 3:3. doi: 10.1186/1745-6150-3-3 PubMedGoogle Scholar
  67. Mitchell P (1967) Proton-translocation phosphorylation in mitochondria, chloroplasts and bacteria: natural fuel cells and solar cells. FASEB J 26:1370–1379Google Scholar
  68. Morita RY (2000) Is H2 the universal energy source for long-term survival? Microb Ecol 38:307–320Google Scholar
  69. Mulholland SE, Gibney BR, Rabanal F, Dutton PL (1999) Determination of nonligand amino acids critical to [4Fe-4S]2+/+ assembly in ferredoxin maquettes. Biochemistry 38:10442–10448PubMedGoogle Scholar
  70. Müller V, Grüber G (2003) ATP synthases: structure, function and evolution of unique energy converters. Cell Mol Life Sci 60:473–494Google Scholar
  71. Müller V, Imkamp F, Biegel E, Schmidt S, Dilling S (2003) Discovery of a ferredoxin:NAD + -oxidoreductase (Rnf) in Acetobacterium woodii: a novel coupling site in acetogens. Ann NY Acad Sci 1125:137–146Google Scholar
  72. Nekrasov IY-A, Konyushok AA (1982) The physicochemical conditions of tungstenite formation. Mineralogicheskii Zhurnal 4:33–40 (in Russian)Google Scholar
  73. Nitschke W, Kramer DM, Riedel A, Liebl U (1995) From naphtho- to benzoquinones—(r)evolutionary reorganizations of electron transfer chains. In: Mathis P (ed) Photosynthesis: from light to biosphere, vol 1. Kluwer Academic Publishers, Dordrecht, pp 945–950Google Scholar
  74. Olsen GJ, Woese CR (1993) Ribosomal RNA: a key to phylogeny. FASEB J 7:113–123PubMedGoogle Scholar
  75. Oremland RS, Blum JS, Culbertson CW, Visscher PT, Miller LG, Dowdle P, Strohmaier FE (1994) Isolation, growth, and metabolism of an obligately anaerobic, selenate-respiring bacterium, strain SES-3. Appl Environ Microbiol 60:3011–3019PubMedGoogle Scholar
  76. Osborn HF (1917) The origin and evolution of life: on the theory of action, reaction and interaction of energy. Charles Scribner’s Sons, New York, NYGoogle Scholar
  77. Pavlov AA, Kasting JF (2002) Mass-independent fractionation of sulfur isotopes in Archaean sediments: strong evidence for an anoxic Archean atmosphere. Astrobiology 2:27–41PubMedGoogle Scholar
  78. Ragsdale SW (1997) The Eastern and Western branches of the Wood/Ljungdahl pathway: how the East and West were won. Biofactors 6:3–11PubMedGoogle Scholar
  79. Rickard D, Butler IB, Olroyd A (2001) A novel iron sulphide switch and its implications for Earth and planetary science. Earth Planet Sci Lett 189:85–91Google Scholar
  80. Robertson DE, Prince RC, Bowyer JR, Matsuura K, Dutton PL, Ohnishi T (1984) Thermodynamic properties of the semiquinone and its binding site in the ubiquinol-cytochrome (c2) oxidoreductase of respiratory and photosynthetic systems. J Biol Chem 259:1758–1763PubMedGoogle Scholar
  81. Russell MJ, Arndt NT (2005) Geodynamic and metabolic cycles in the Hadean. Biogeosciences 2:97–111CrossRefGoogle Scholar
  82. Russell MJ, Hall AJ (1997) The emergence of life from iron monosulphide bubbles at a submarine hydrothermal redox and pH front. J Geol Soc London 154:377–402PubMedGoogle Scholar
  83. Russell MJ, Hall AJ (2006) The onset and early evolution of life. In: Kesler SE, Ohmoto H (eds) Evolution of early earth’s atmosphere, hydrosphere, and biosphere—constraints from ore deposits. Geological Society of America, Memoir 198, pp 1–32Google Scholar
  84. Russell MJ, Hall AJ (2009) A hydrothermal source of energy and materials at the origin of life. In: Chemical evolution II: from origins of life to modern society. American Chemical Society, (in press)Google Scholar
  85. Russell MJ, Martin W (2004) The rocky roots of the acetyl-CoA pathway. Trends Biochem Sci 29:358–363PubMedGoogle Scholar
  86. Russell MJ, Hall AJ, Turner D (1989) In vitro growth of iron sulphide chimneys: possible culture chambers for origin-of-life experiments. Terra Nova 1:238–241Google Scholar
  87. Russell MJ, Daniel RM, Hall AJ (1993) On the emergence of life via catalytic iron sulphide membranes. Terra Nova 5:343–347Google Scholar
  88. Russell MJ, Daniel RM, Hall AJ, Sherringham J (1994) A hydrothermally precipitated catalytic iron sulphide membrane as a first step toward life. J Mol Evol 39:231–243Google Scholar
  89. Schoepp-Cothenet B, Lieutaud C, Baymann F, Verméglio A, Friedrich T, Kramer DM, Nitschke W (2009) Menaquinone as pool quinone in a purple bacterium. Proc Natl Acad Sci USA 106:8549–8554PubMedGoogle Scholar
  90. Schönheit P, Moll J, Thauer RK (1979) Nickel, cobalt, and molybdenum requirement for growth of Methanobacterium thermoautotrophicum. Arch Microbiol 123:105–107PubMedGoogle Scholar
  91. Schultz A, Baltscheffsky M (2003) Properties of mutated Rhodospirillum rubrum H+-pyrophosphatase expressed in Escherichia coli. Biochim Biophys Acta 1607:141–151PubMedGoogle Scholar
  92. Schulzke C (2005) Temperature dependent electrochemical investigations of molybdenum and tungsten oxobisdithiolene complexes. Dalton Trans 713–720Google Scholar
  93. Schütz M, Brugna M, Lebrun E, Baymann F, Huber R, Stetter KO, Hauska G, Toci R, Lemesle-Meunier D, Tron P, Schmidt C, Nitschke W (2000) Early evolution of cytochrome bc-complexes. J Mol Biol 300:663–676PubMedGoogle Scholar
  94. Seewald JS, Zolotov MY, McCollom T (2006) Experimental investigation of single carbon compounds under hydrothermal conditions. Geochimica Cosmochimica Acta 70:446–460Google Scholar
  95. Seward TM, Barnes HL (1997) Metal transport in hydrothermal ore fluids. In: Barnes HL (ed) Geochemistry of hydrothermal ore deposits, 3rd edn. John Wiley & Sons, New York, pp 435–486Google Scholar
  96. Slesarev AI, Mezhevaya KV, Makarova KS et al (2002) The complete genome of hyperthermophile Methanopyrus kandleri AV19 and monophyly of archaeal methanogens. Proc Natl Acad Sci USA 99:4644–4649PubMedGoogle Scholar
  97. Spivack AJ, Staudigel H (1994) Low-temperature alteration of the upper oceanic crust and the alkalinity budget of seawater. Chem Geol 115:239–247Google Scholar
  98. Staudigel H, Hart SR, Richardson SH (1981) Alteration of the oceanic crust: processes and timing. Earth Planet Sci Lett 52:311–327Google Scholar
  99. Stetter KO, Gaag G (1983) Reduction of molecular sulphur by methanogenic bacteria. Nature 305:309–311Google Scholar
  100. Traube M (1867) Experimente zur Theorie der Zellenbildung und Endosmose. Archiv Anat u Physiol 1867:87–165Google Scholar
  101. Vargas M, Kashefi K, Blunt-Harris EL, Lovley DR (1998) Microbial evidence for Fe(III) reduction on early Earth. Nature 395:65–67PubMedGoogle Scholar
  102. Vignais PM, Billoud B (2007) Occurrence, classification and biological function of hydrogenases: an overview. Chem Rev 107:4206–4272PubMedGoogle Scholar
  103. Vignais PM, Billoud B, Meyer J (2001) Classification and phylogeny of hydrogenases. FEMS Microbiol Rev 25:455–501PubMedGoogle Scholar
  104. Volbeda A, Fontecilla-Camps JC (2006) Catalytic nickel–iron–sulfur clusters: from minerals to enzymes. In: Simmonneaux G (ed) Topics in organometallic chemistry, vol 17. Springer, Berlin, pp 57–82Google Scholar
  105. Von Jagow G, Ljungdahl PO, Graf P, Ohmishi T, Trumpower BL (1984) An inhibitor of mitochondrial respiration that binds to cytochromes and displaces quinone from the iron-sulfur proteins of the cytochrome bc1 complex. J Biol Chem 259:6318–6326Google Scholar
  106. Wächtershäuser G (1988) Before enzymes and templates: theory of surface metabolism. Microbiol Rev 52:452–484PubMedGoogle Scholar
  107. Walker JCG (1985) Carbon dioxide on the early Earth. Orig Life Evol Biosph 16:117–127PubMedGoogle Scholar
  108. Wallace W, Ward T, Breen A, Attaway H (1996) Identification of an anaerobic bacterium which reduces perchlorate and chlorate as Wolinella succinogenes. J Ind Microbiol 16:68–72Google Scholar
  109. Weiner J, Beaussart F, Bornberg-Bauer E (2006) Domain deletions and substitutions in the modular protein evolution. FEBS J 273:2037–2047PubMedGoogle Scholar
  110. Williams RJP, Frausto da Silva JJR (2003) Evolution was chemically constrained. J Theor Biol 220:323–343PubMedGoogle Scholar
  111. Woese CR (1987) Bacterial evolution. Microbiol Rev 51:221–271PubMedGoogle Scholar
  112. Wong JT (2009) Introduction. In: Wong JT, Laszcano A (eds) Prebiotic evolution & astrobiology, Chap 1. Landes Bioscience, Austin, Texas (in press)Google Scholar
  113. Wong JT (2009) Root of life. In: Wong JT, Laszcano A (eds) Prebiotic evolution & astrobiology, Chap 15. Landes Bioscience, Austin, Texas (in press)Google Scholar
  114. Wong JT, Chen J, Mat WK, Ng SK, Xue H (2007) Polyphasic evidence delineating the root of life and roots of biological domains. Gene 403:39–52PubMedGoogle Scholar
  115. Wood HG (1977) Some reactions in which inorganic pyrophosphate replaces ATP and serves as a source of energy. Fed Proc 36:2197–2205PubMedGoogle Scholar
  116. Yamagata Y, Wanatabe H, Saitoh M, Namba T (1991) Volcanic production of polyphosphates and its relevance to prebiotic evolution. Nature 352:516–519PubMedGoogle Scholar
  117. Yokey HP (1995) Comments on ‘‘Let there be Life; Thermodynamic Reflections on Biogenesis and Evolution’’ by Avshalom C. Elitzur. J Theor Biol 176:349–355Google Scholar
  118. Zachara JM, Kukkadapu RK, Frederickson JM, Gorby YA, Smith SC (2002) Biomineralization of poorly crystalline Fe(III) oxides by dissimilatory metal reducing bacteria (DMRB). Geomicrobiol J 19:179–207Google Scholar

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© U.S. Government 2009

Authors and Affiliations

  1. 1.Laboratoire de Bioénergétique et Ingénierie des Protéines (CNRS/UPR9036), IFR88Marseille Cedex 20France
  2. 2.Planetary Science & Life Detection, Section 3220, MS: 183-601, JPLCalifornia Institute of TechnologyPasadenaUSA

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