Carbon–Metal Bonds: Rare and Primordial in Metabolism
2019; Elsevier BV; Volume: 44; Issue: 9 Linguagem: Inglês
10.1016/j.tibs.2019.04.010
ISSN1362-4326
Autores Tópico(s)Photosynthetic Processes and Mechanisms
ResumoThe active sites of ancient enzymes that channel CO2, N2, and H2 into ancient metabolism share conserved chemical components: carbon–metal bonds.Although rare in biology, carbon–metal bonds are common in industrial catalysts and are in everyday materials, such as steel.In enzymes and cofactors, carbon forms covalent bonds with iron, nickel, and cobalt, transition metals characterized by unfilled d electron orbitals.Of nine carbon–metal bonds in primary metabolism, six can be traced to the last universal common ancestor (LUCA).Residing at the interface of the environment and metabolism, carbon–metal bonds are relics of primordial chemistry that existed on the early Earth, before the advent of enzymes. Submarine hydrothermal vents are rich in hydrogen (H2), an ancient source of electrons and chemical energy for life. Geochemical H2 stems from serpentinization, a process in which rock-bound iron reduces water to H2. Reactions involving H2 and carbon dioxide (CO2) in hydrothermal systems generate abiotic methane and formate; these reactions resemble the core energy metabolism of methanogens and acetogens. These organisms are strict anaerobic autotrophs that inhabit hydrothermal vents and harness energy via H2-dependent CO2 reduction. Serpentinization also generates native metals, which can reduce CO2 to formate and acetate in the laboratory. The enzymes that channel H2, CO2, and dinitrogen (N2) into methanogen and acetogen metabolism are the backbone of the most ancient metabolic pathways. Their active sites share carbon–metal bonds which, although rare in biology, are conserved relics of primordial biochemistry present at the origin of life. Submarine hydrothermal vents are rich in hydrogen (H2), an ancient source of electrons and chemical energy for life. Geochemical H2 stems from serpentinization, a process in which rock-bound iron reduces water to H2. Reactions involving H2 and carbon dioxide (CO2) in hydrothermal systems generate abiotic methane and formate; these reactions resemble the core energy metabolism of methanogens and acetogens. These organisms are strict anaerobic autotrophs that inhabit hydrothermal vents and harness energy via H2-dependent CO2 reduction. Serpentinization also generates native metals, which can reduce CO2 to formate and acetate in the laboratory. The enzymes that channel H2, CO2, and dinitrogen (N2) into methanogen and acetogen metabolism are the backbone of the most ancient metabolic pathways. Their active sites share carbon–metal bonds which, although rare in biology, are conserved relics of primordial biochemistry present at the origin of life. Intuition has it that there are some traces of ancient chemical evolution preserved in modern metabolism. This idea is germane to the continuity thesis (see Glossary) that unites theories viewing the origin of life as inherently probable because physical and chemical constraints apply uniformly across the transition from inanimate to living matter [1.Fry I. Are the different hypotheses on the emergence of life as different as they seem?.Biol. Philos. 1995; 10: 389-417Crossref Scopus (29) Google Scholar]. As such, continuity is inherent to theories about ancient metabolism that address transitions from inorganic geochemical settings to biochemical processes, because they embrace justified supposition that reactants and catalysts in the former gave rise to reactions in the latter. Life is a chemical reaction. It started out under anaerobic conditions [2.Amend J.P. Shock E.L. Energetics of overall metabolic reactions of thermophilic and hyperthermophilic Archaea and bacteria.FEMS Microbiol. Rev. 2001; 25: 175-243Crossref PubMed Google Scholar] because molecular oxygen is a product of microbial metabolism. If we look for chemical continuity between the geochemical setting where life arose and modern microbial metabolism, there are two places to look: energetics and catalysts. The pursuit of chemical continuity in energetics leads directly to the main exergonic (energy-releasing) reactions (the core bioenergetic reactions) that cells harness to conserve energy. There are hundreds of core bioenergetic reactions that anaerobes tap to conserve energy [2.Amend J.P. Shock E.L. Energetics of overall metabolic reactions of thermophilic and hyperthermophilic Archaea and bacteria.FEMS Microbiol. Rev. 2001; 25: 175-243Crossref PubMed Google Scholar, 3.Thauer R.K. et al.Energy-conservation in chemotrophic anaerobic bacteria.Bacteriol. Rev. 1977; 41: 100-180PubMed Google Scholar], but the only environments known that harbor naturally occurring reactions with bona fide similarity to bioenergetic reactions are hydrothermal vents. These vents harbor rock–water–carbon interactions that take place deep in the crust of the Earth in the strict absence of oxygen [4.McCollom T.M. Seewald J.S. Serpentinites, hydrogen, and life.Elements. 2013; 9: 129-134Crossref Scopus (0) Google Scholar, 5.Schrenk M.O. et al.Serpentinization, carbon and deep life.Rev. Mineral. Geochem. 2013; 75: 575-606Crossref Scopus (0) Google Scholar, 6.McDermott J.M. et al.Pathways for abiotic organic synthesis at submarine hydrothermal fields.Proc. Natl. Acad. Sci. U. S. A. 2015; 112: 7668-7672Crossref PubMed Google Scholar, 7.McCollom T.M. Abiotic methane formation during experimental serpentinization of olivine.Proc. Natl. Acad. Sci. U. S. A. 2016; 113: 13965-13970Crossref PubMed Scopus (38) Google Scholar, 8.Martin W. Russell M.J. On the origin of biochemistry at an alkaline hydrothermal vent.Philos. Trans. R. Soc. Lond. B. 2007; 362: 1887-1925Crossref PubMed Scopus (0) Google Scholar, 9.Martin W. et al.Hydrothermal vents and the origin of life.Nat. Rev. Microbiol. 2008; 6: 805-814Crossref PubMed Scopus (535) Google Scholar]. Those geochemical reactions generate large amounts of H2 that in turn reduces CO2 to generate formate and methane, which emerge in the vent effluent [4.McCollom T.M. Seewald J.S. Serpentinites, hydrogen, and life.Elements. 2013; 9: 129-134Crossref Scopus (0) Google Scholar, 5.Schrenk M.O. et al.Serpentinization, carbon and deep life.Rev. Mineral. Geochem. 2013; 75: 575-606Crossref Scopus (0) Google Scholar, 6.McDermott J.M. et al.Pathways for abiotic organic synthesis at submarine hydrothermal fields.Proc. Natl. Acad. Sci. U. S. A. 2015; 112: 7668-7672Crossref PubMed Google Scholar, 7.McCollom T.M. Abiotic methane formation during experimental serpentinization of olivine.Proc. Natl. Acad. Sci. U. S. A. 2016; 113: 13965-13970Crossref PubMed Scopus (38) Google Scholar]. The CO2-reducing geochemical reactions share in turn conspicuous similarity to the core bioenergetic reactions of some modern H2-dependent anaerobes [8.Martin W. Russell M.J. On the origin of biochemistry at an alkaline hydrothermal vent.Philos. Trans. R. Soc. Lond. B. 2007; 362: 1887-1925Crossref PubMed Scopus (0) Google Scholar, 9.Martin W. et al.Hydrothermal vents and the origin of life.Nat. Rev. Microbiol. 2008; 6: 805-814Crossref PubMed Scopus (535) Google Scholar], the acetogens [10.Schuchmann K. Müller V. Autotrophy at the thermodynamic limit of life: a model for energy conservation in acetogenic bacteria.Nat. Rev. Microbiol. 2014; 12: 809-821Crossref PubMed Scopus (228) Google Scholar] and methanogens [11.Thauer R.K. et al.Methanogenic archaea: ecologically relevant differences in energy conservation.Nat. Rev. Microbiol. 2008; 6: 579-591Crossref PubMed Scopus (820) Google Scholar], strictly anaerobic autotrophs that satisfy both their carbon and their energy needs from H2 and CO2. Ideas about the continuity of catalysts that promote the chemical reactions of life center around organic cofactors, thioesters, and iron sulfide (FeS) clusters, all of which are presumed to have preceded enzymes in evolution. Organic cofactors are essential to biochemistry [12.Morowitz H.J. Beginnings of Cellular Life: Metabolism Recapitulates Biogenesis. Yale University Press, 1992Google Scholar]. In many metabolic reactions, the cofactor provides the catalysis, the enzyme just holds it in place and provides a hydrophobic pocket where cofactor and substrate can react [13.Wolfenden R. Benchmark reaction rates, the stability of biological molecules in water, and the evolution of catalytic power in enzymes.Annu. Rev. Biochem. 2011; 80: 645-667Crossref PubMed Scopus (0) Google Scholar]. The popular idea of an RNA world [14.Joyce G.F. The antiquity of RNA-based evolution.Nature. 2002; 418: 214-221Crossref PubMed Scopus (589) Google Scholar] arose around the concept that cofactors preceded enzymes in evolution and were originally connected to RNA molecules as the precursors of proteins [15.White 3rd, H.B. Coenzymes as fossils of an earlier metabolic state.J. Mol. Evol. 1976; 7: 101-104Crossref PubMed Google Scholar]. Thioesters have long been recognized as being central to metabolism [8.Martin W. Russell M.J. On the origin of biochemistry at an alkaline hydrothermal vent.Philos. Trans. R. Soc. Lond. B. 2007; 362: 1887-1925Crossref PubMed Scopus (0) Google Scholar, 16.Goldford J.E. et al.Remnants of an ancient metabolism without phosphate.Cell. 2017; 168: 1126-1134Abstract Full Text Full Text PDF PubMed Scopus (0) Google Scholar]. The thioester bond is long and easily cleaved [17.Wald G. Life in the second and third periods; or why phosphorus and sulfur for high-energy bonds?.in: Kasha M. Pullman B. Horizons in Biochemistry. Academic Press, 1962: 127-142Google Scholar], making them highly reactive [18.Semenov S.N. et al.Autocatalytic, bistable, oscillatory networks of biologically relevant organic reactions.Nature. 2016; 537: 656-660Crossref PubMed Scopus (73) Google Scholar]. Thioester bonds have a high free energy of hydrolysis (–43 kJ/mol), higher than that of ATP (–31 kJ/mol) [8.Martin W. Russell M.J. On the origin of biochemistry at an alkaline hydrothermal vent.Philos. Trans. R. Soc. Lond. B. 2007; 362: 1887-1925Crossref PubMed Scopus (0) Google Scholar], which is often generated from thioesters in metabolism. Thioesters are thought to have preceded phosphates as energy currencies in evolution [16.Goldford J.E. et al.Remnants of an ancient metabolism without phosphate.Cell. 2017; 168: 1126-1134Abstract Full Text Full Text PDF PubMed Scopus (0) Google Scholar, 19.de Duve C. Singularities. Landmarks on the Pathways of Life. Cambridge University Press, 2005Crossref Scopus (72) Google Scholar] and they can be synthesized in the laboratory from carbon monoxide (CO) and methyl sulfide in the presence of FeS [20.Huber C. Wächtershäuser G. Activated acetic acid by carbon fixation on (Fe,Ni)S under primordial conditions.Science. 1997; 276: 245-247Crossref PubMed Scopus (435) Google Scholar], compounds that were likely present on the primordial Earth [8.Martin W. Russell M.J. On the origin of biochemistry at an alkaline hydrothermal vent.Philos. Trans. R. Soc. Lond. B. 2007; 362: 1887-1925Crossref PubMed Scopus (0) Google Scholar]. FeS clusters are traditionally viewed as primitive catalysts in metabolism because they are completely inorganic and because metal sulfides would have been common on the early Earth [21.Eck R.V. Dayhoff M.O. Evolution of the structure of ferredoxin based on living relics of primitive amino acid sequences.Science. 1966; 152: 363-366Crossref PubMed Google Scholar, 22.Wächtershäuser G. Groundworks for an evolutionary biochemistry – the iron sulfur world.Prog. Biophys. Mol. Biol. 1992; 58: 85-201Crossref PubMed Google Scholar]. Reduced FeS clusters are also a currency of chemical energy [23.Herrmann G. et al.Energy conservation via electron-transferring flavoprotein in anaerobic bacteria.J. Bacteriol. 2008; 190: 784-791Crossref PubMed Scopus (0) Google Scholar, 24.Müller V. et al.Electron bifurcation: a long-hidden energy-coupling mechanism.Annu. Rev. Microbiol. 2018; 72: 331-353Crossref PubMed Scopus (5) Google Scholar], similar to thioesters and ATP. They are also highly enriched in genomic reconstructions of the metabolism of the last universal common ancestor (LUCA) [25.Weiss M.C. et al.The physiology and habitat of the last universal common ancestor.Nat. Microbiol. 2016; 1: 16116Crossref PubMed Google Scholar], which used the acetyl-CoA pathway and lived off gases, harnessing energy by reducing CO2 with H2 [26.Weiss M.C. et al.The last universal common ancestor between ancient Earth chemistry and the onset of genetics.PLoS Genet. 2018; 14e1007518Crossref PubMed Scopus (5) Google Scholar]. Physiology is rich in continuity because some 4 billion years after the origin of life [27.Tashiro T. et al.Early trace of life from 3.95 Ga sedimentary rocks in Labrador, Canada.Nature. 2017; 549: 516-518Crossref PubMed Scopus (26) Google Scholar] ,the same chemical energy that powered LUCA still fuels the growth of modern methanogens and acetogens that inhabit the crust today [28.Silver B.J. et al.In situ cultivation of subsurface microorganisms in a deep mafic sill: implications for SLiMEs.Geomicrobiol J. 2010; 27: 329-27348Crossref Scopus (6) Google Scholar, 29.Takami H. et al.A deeply branching thermophilic bacterium with an ancient acetyl-CoA pathway dominates a subsurface ecosystem.PLoS One. 2012; 7e30559Crossref PubMed Scopus (63) Google Scholar, 30.Ijiri A. et al.Deep-biosphere methane production stimulated by geofluids in the Nankai accretionary complex.Sci. Adv. 2018; 4eaao4631Crossref PubMed Scopus (11) Google Scholar, 31.Rempfert K.R. et al.Geological and geochemical controls on subsurface microbial life in the Samail Ophiolite, Oman.Front. Microbiol. 2017; 8: 56Crossref PubMed Scopus (17) Google Scholar, 32.Suzuki S. et al.Genomic and in-situ transcriptomic characterization of the candidate phylum NPL-UPL2 from highly alkaline highly reducing serpentinized groundwater.Front. Microbiol. 2018; 9: 3141Crossref PubMed Google Scholar]. If the continuity principle holds at the active sites of enzymes, then enzymes with which anaerobes access CO2, N2, and H2 at the interface between the environment and biology can provide insights into the nature of primordial metabolism. Here, I discuss ancient enzymes at the core of metabolism in autotrophs that harness carbon and energy via the reduction of CO2 with H2. I make the case that their shared common structural feature that is otherwise very rare in biology (carbon–metal bonds) reflects chemical reactions and catalysts that were significant in the evolutionary context of the origin of life. Any discussion about carbon chemistry before enzymes or biochemistry at the origin of life is aided by considering benchmarks concerning the chemistry of the early Earth, which provides many helpful constraints. First, it constrains the times at which these reactions could have started. The moon-forming impact approximately 4.5 billion years ago is a crucial benchmark because it turned the Earth into a ball of boiling magma of at least 1500°C [33.Zahnle K. et al.Emergence of a habitable planet.Space Sci. Rev. 2007; 129: 35-78Crossref Scopus (0) Google Scholar], too hot for any organic compounds or anything resembling life. It is certain that the Earth was completely molten because it is spherical; the moon-forming impact left no crater. Second, it constricts what compounds were initially available. Magma converted carbon on Earth into atmospheric CO2 [33.Zahnle K. et al.Emergence of a habitable planet.Space Sci. Rev. 2007; 129: 35-78Crossref Scopus (0) Google Scholar, 34.Arndt N.T. Nisbet E.G. Processes on the young Earth and the habitats of early life.Annu. Rev. Earth Planet. Sci. 2012; 40: 521-549Crossref Scopus (0) Google Scholar, 35.Sleep N.H. Geological and geochemical constraints on the origin and evolution of life.Astrobiology. 2018; 18: 1-21Crossref PubMed Scopus (4) Google Scholar]. With the Earth in a molten state, gravity caused dense material-like native metals, such as iron and nickel, to sink to the core, with lighter material, such as silicates, differentiating to the surface [34.Arndt N.T. Nisbet E.G. Processes on the young Earth and the habitats of early life.Annu. Rev. Earth Planet. Sci. 2012; 40: 521-549Crossref Scopus (0) Google Scholar, 35.Sleep N.H. Geological and geochemical constraints on the origin and evolution of life.Astrobiology. 2018; 18: 1-21Crossref PubMed Scopus (4) Google Scholar]. By approximately 4.2 billion years ago, the surface had cooled, rock had formed, and water vapor had condensed to oceans [33.Zahnle K. et al.Emergence of a habitable planet.Space Sci. Rev. 2007; 129: 35-78Crossref Scopus (0) Google Scholar, 34.Arndt N.T. Nisbet E.G. Processes on the young Earth and the habitats of early life.Annu. Rev. Earth Planet. Sci. 2012; 40: 521-549Crossref Scopus (0) Google Scholar, 35.Sleep N.H. Geological and geochemical constraints on the origin and evolution of life.Astrobiology. 2018; 18: 1-21Crossref PubMed Scopus (4) Google Scholar]. Water was drawn into cracks in the crust, became heated at depth and circulated back into the ocean, giving rise to hydrothermal systems. Atmospheric CO2 became dissolved in the ocean, was sequestered in the crust as carbonates via hydrothermal convection, and then transferred to the mantle via subduction [33.Zahnle K. et al.Emergence of a habitable planet.Space Sci. Rev. 2007; 129: 35-78Crossref Scopus (0) Google Scholar, 34.Arndt N.T. Nisbet E.G. Processes on the young Earth and the habitats of early life.Annu. Rev. Earth Planet. Sci. 2012; 40: 521-549Crossref Scopus (0) Google Scholar, 35.Sleep N.H. Geological and geochemical constraints on the origin and evolution of life.Astrobiology. 2018; 18: 1-21Crossref PubMed Scopus (4) Google Scholar]. At depths of several kilometers within the crust, water circulating in hydrothermal convective currents began reacting with inexhaustible reserves of iron II [Fe(II)]-containing minerals to initiate an important geochemical process: serpentinization [34.Arndt N.T. Nisbet E.G. Processes on the young Earth and the habitats of early life.Annu. Rev. Earth Planet. Sci. 2012; 40: 521-549Crossref Scopus (0) Google Scholar, 35.Sleep N.H. Geological and geochemical constraints on the origin and evolution of life.Astrobiology. 2018; 18: 1-21Crossref PubMed Scopus (4) Google Scholar, 36.Preiner M. et al.Serpentinization: connecting geochemistry, ancient metabolism and industrial hydrogenation.Life. 2018; 8: 41Crossref Scopus (2) Google Scholar]. During serpentinization, Fe(II) minerals are oxidized by water (H2O) to generate Fe(III) and H2 gas. Serpentinization is exergonic in that it releases energy [4.McCollom T.M. Seewald J.S. Serpentinites, hydrogen, and life.Elements. 2013; 9: 129-134Crossref Scopus (0) Google Scholar, 5.Schrenk M.O. et al.Serpentinization, carbon and deep life.Rev. Mineral. Geochem. 2013; 75: 575-606Crossref Scopus (0) Google Scholar] in a process that continues to this day [37.Baross J.A. The rocky road to biomolecules.Nature. 2018; 564: 42-43Crossref PubMed Scopus (1) Google Scholar]. The effluent of modern hydrothermal vents often contains ~10 mM H2 [38.Kelley D.S. et al.A serpentinite-hosted ecosystem: the Lost City hydrothermal field.Science. 2005; 307: 1428-1434Crossref PubMed Scopus (0) Google Scholar], orders of magnitude more than H2-dependent microbes require for growth [11.Thauer R.K. et al.Methanogenic archaea: ecologically relevant differences in energy conservation.Nat. Rev. Microbiol. 2008; 6: 579-591Crossref PubMed Scopus (820) Google Scholar]. At some sites, hydrothermal effluent also contains abiotic methane and other reduced carbon compounds that result from H2 interacting with inorganic carbon, such as CO2, in the crust [4.McCollom T.M. Seewald J.S. Serpentinites, hydrogen, and life.Elements. 2013; 9: 129-134Crossref Scopus (0) Google Scholar, 5.Schrenk M.O. et al.Serpentinization, carbon and deep life.Rev. Mineral. Geochem. 2013; 75: 575-606Crossref Scopus (0) Google Scholar, 6.McDermott J.M. et al.Pathways for abiotic organic synthesis at submarine hydrothermal fields.Proc. Natl. Acad. Sci. U. S. A. 2015; 112: 7668-7672Crossref PubMed Google Scholar, 7.McCollom T.M. Abiotic methane formation during experimental serpentinization of olivine.Proc. Natl. Acad. Sci. U. S. A. 2016; 113: 13965-13970Crossref PubMed Scopus (38) Google Scholar, 34.Arndt N.T. Nisbet E.G. Processes on the young Earth and the habitats of early life.Annu. Rev. Earth Planet. Sci. 2012; 40: 521-549Crossref Scopus (0) Google Scholar, 35.Sleep N.H. Geological and geochemical constraints on the origin and evolution of life.Astrobiology. 2018; 18: 1-21Crossref PubMed Scopus (4) Google Scholar, 36.Preiner M. et al.Serpentinization: connecting geochemistry, ancient metabolism and industrial hydrogenation.Life. 2018; 8: 41Crossref Scopus (2) Google Scholar, 37.Baross J.A. The rocky road to biomolecules.Nature. 2018; 564: 42-43Crossref PubMed Scopus (1) Google Scholar, 38.Kelley D.S. et al.A serpentinite-hosted ecosystem: the Lost City hydrothermal field.Science. 2005; 307: 1428-1434Crossref PubMed Scopus (0) Google Scholar]. Whether with or without enzymes, in the reaction of H2 with CO2, the equilibrium lies on the side of reduced carbon compounds [3.Thauer R.K. et al.Energy-conservation in chemotrophic anaerobic bacteria.Bacteriol. Rev. 1977; 41: 100-180PubMed Google Scholar]. Among the many core bioenergetic reactions known [2.Amend J.P. Shock E.L. Energetics of overall metabolic reactions of thermophilic and hyperthermophilic Archaea and bacteria.FEMS Microbiol. Rev. 2001; 25: 175-243Crossref PubMed Google Scholar], only acetogens [10.Schuchmann K. Müller V. Autotrophy at the thermodynamic limit of life: a model for energy conservation in acetogenic bacteria.Nat. Rev. Microbiol. 2014; 12: 809-821Crossref PubMed Scopus (228) Google Scholar] and methanogens [11.Thauer R.K. et al.Methanogenic archaea: ecologically relevant differences in energy conservation.Nat. Rev. Microbiol. 2008; 6: 579-591Crossref PubMed Scopus (820) Google Scholar] are known to harness energy solely from the reduction of CO2 with H2. The deep biosphere of the Earth is replete with acetogens and methanogens [28.Silver B.J. et al.In situ cultivation of subsurface microorganisms in a deep mafic sill: implications for SLiMEs.Geomicrobiol J. 2010; 27: 329-27348Crossref Scopus (6) Google Scholar, 29.Takami H. et al.A deeply branching thermophilic bacterium with an ancient acetyl-CoA pathway dominates a subsurface ecosystem.PLoS One. 2012; 7e30559Crossref PubMed Scopus (63) Google Scholar, 30.Ijiri A. et al.Deep-biosphere methane production stimulated by geofluids in the Nankai accretionary complex.Sci. Adv. 2018; 4eaao4631Crossref PubMed Scopus (11) Google Scholar, 31.Rempfert K.R. et al.Geological and geochemical controls on subsurface microbial life in the Samail Ophiolite, Oman.Front. Microbiol. 2017; 8: 56Crossref PubMed Scopus (17) Google Scholar, 32.Suzuki S. et al.Genomic and in-situ transcriptomic characterization of the candidate phylum NPL-UPL2 from highly alkaline highly reducing serpentinized groundwater.Front. Microbiol. 2018; 9: 3141Crossref PubMed Google Scholar]. Considering the origins of ancient metabolism from the standpoint of geochemical constraints, the exergonic reduction of CO2 with H2 comes into focus as an ancient bioenergetic route [4.McCollom T.M. Seewald J.S. Serpentinites, hydrogen, and life.Elements. 2013; 9: 129-134Crossref Scopus (0) Google Scholar, 5.Schrenk M.O. et al.Serpentinization, carbon and deep life.Rev. Mineral. Geochem. 2013; 75: 575-606Crossref Scopus (0) Google Scholar, 6.McDermott J.M. et al.Pathways for abiotic organic synthesis at submarine hydrothermal fields.Proc. Natl. Acad. Sci. U. S. A. 2015; 112: 7668-7672Crossref PubMed Google Scholar, 7.McCollom T.M. Abiotic methane formation during experimental serpentinization of olivine.Proc. Natl. Acad. Sci. U. S. A. 2016; 113: 13965-13970Crossref PubMed Scopus (38) Google Scholar, 34.Arndt N.T. Nisbet E.G. Processes on the young Earth and the habitats of early life.Annu. Rev. Earth Planet. Sci. 2012; 40: 521-549Crossref Scopus (0) Google Scholar, 35.Sleep N.H. Geological and geochemical constraints on the origin and evolution of life.Astrobiology. 2018; 18: 1-21Crossref PubMed Scopus (4) Google Scholar, 36.Preiner M. et al.Serpentinization: connecting geochemistry, ancient metabolism and industrial hydrogenation.Life. 2018; 8: 41Crossref Scopus (2) Google Scholar, 37.Baross J.A. The rocky road to biomolecules.Nature. 2018; 564: 42-43Crossref PubMed Scopus (1) Google Scholar, 38.Kelley D.S. et al.A serpentinite-hosted ecosystem: the Lost City hydrothermal field.Science. 2005; 307: 1428-1434Crossref PubMed Scopus (0) Google Scholar]. CO2 fixation also constrains biochemical origins, because, as hinted at earlier, CO2 was the starting point for biological carbon. Autotrophs, whether they obtain their electrons from H2 like acetogens and methanogens do, or from other electron donors with the help of chlorophyll-based photosynthesis, comprise the basis of all food chains [39.Martin W.F. et al.A physiological perspective on the origin and evolution of photosynthesis.FEMS Microbiol. Rev. 2018; 42: 201-231Crossref Google Scholar], Among modern microbes, there are six known pathways of biological CO2 fixation in nature [40.Berg I.A. Ecological aspects of the distribution of different autotrophic CO2 fixation pathways.Appl. Environ. Microbiol. 2011; 77: 1925-1936Crossref PubMed Scopus (224) Google Scholar] the Calvin cycle, the reverse citric acid (TCA) cycle, and the acetyl-CoA (or Wood–Ljungdahl) pathway [41.Hügler M. Sievert S.M. Beyond the Calvin cycle: autotrophic carbon fixation in the ocean.Annu. Rev. Mar. Sci. 2011; 3: 261-289Crossref PubMed Scopus (0) Google Scholar, 42.Ragsdale S.W. Enzymology of the acetyl-CoA pathway of CO2 fixation.Crit. Rev. Biochem. Mol. Biol. 1991; 26: 261-300Crossref PubMed Google Scholar], as well as three pathways described by Georg Fuchs and colleagues: the dicarboxylate/4-hydroxybutyrate cycle, the 3-hydroxypropionate/4-hydroxybutyrate cycle, and the 3-hydroxypropionate bi-cycle [43.Fuchs G. Alternative pathways of carbon dioxide fixation: insights into the early evolution of life?.Annu. Rev. Microbiol. 2011; 65: 631-658Crossref PubMed Scopus (217) Google Scholar]. Among those six, the acetyl-CoA pathway is the only one that occurs in both archaea and bacteria [40.Berg I.A. Ecological aspects of the distribution of different autotrophic CO2 fixation pathways.Appl. Environ. Microbiol. 2011; 77: 1925-1936Crossref PubMed Scopus (224) Google Scholar, 43.Fuchs G. Alternative pathways of carbon dioxide fixation: insights into the early evolution of life?.Annu. Rev. Microbiol. 2011; 65: 631-658Crossref PubMed Scopus (217) Google Scholar], suggesting that it is the most ancient CO2 fixation pathway. Furthermore, its distribution among acetogens (bacteria) and methanogens (archaea) is not the result of lateral gene transfer (LGT); different C1 carriers are used in their pathways, and the enzymes of the methyl synthesis branch in bacteria are unrelated to those of archaea [44.Sousa F.L. Martin W.F. Biochemical fossils of the ancient transition from geoenergetics to bioenergetics in prokaryotic one carbon compound metabolism.Biochim. Biophys. Acta. 2014; 1837: 964-981Crossref PubMed Scopus (32) Google Scholar]. Thermodynamics also constrain biochemical origins. The acetyl-CoA pathway is exergonic [41.Hügler M. Sievert S.M. Beyond the Calvin cycle: autotrophic carbon fixation in the ocean.Annu. Rev. Mar. Sci. 2011; 3: 261-289Crossref PubMed Scopus (0) Google Scholar, 43.Fuchs G. Alternative pathways of carbon dioxide fixation: insights into the early evolution of life?.Annu. Rev. Microbiol. 2011; 65: 631-658Crossref PubMed Scopus (217) Google Scholar] and is used by acetogens and methanogens to generate ion gradients that are harnessed by ATPases to satisfy the core ATP needs of the cell while simultaneously supplying reduced carbon [43.Fuchs G. Alternative pathways of carbon dioxide fixation: insights into the early evolution of life?.Annu. Rev. Microbiol. 2011; 65: 631-658Crossref PubMed Scopus (217) Google Scholar]. Although the acetyl-CoA pathway as it occurs in acetogens entails consumption of one ATP at the formyltetrahydrofolate synthase reaction [10.Schuchmann K. Müller V. Autotrophy at the thermodynamic limit of life: a model for energy conservation in acetogenic bacteria.Nat. Rev. Microbiol. 2014; 12: 809-821Crossref PubMed Scopus (228) Google Scholar], one ATP is generated at the acetate kinase reaction [10.Schuchmann K. Müller V. Autotrophy at the thermodynamic limit of life: a model for energy conservation in acetogenic bacteria.Nat. Rev. Microbiol. 2014; 12: 809-821Crossref PubMed Scopus (228) Google Scholar], such that acetate synthesis from CO2 involves no net ATP input, while ions pumped during acetate synthesis reduction fuel ATP synthesis via the F1F0 ATP synthase at the plasma membrane [10.Schuchmann K. Müller V. Autotrophy at the thermodynamic limit of life: a model for energy conservation in acetogenic bacteria.Nat. Rev. Microbiol. 2014; 12: 809-821Crossref PubMed Scopus (228) Google Scholar]. Put simply, the acetyl-CoA pathway is carbon and energy metabolism in one, although its main role in acetogens and methanogens is energy. Approximately 95% of the CO2 that the acetyl-CoA pathway reduces in acetogens and methanogens leaves the cell in the form of acetate or methane as the end-product of energy harnessing, with CO2 incorporation as cell mass having a quantitatively lesser role [11.Thauer R.K. et al.Methanogenic archaea: ecologically relevant differences in energy conservation.Nat. Rev. Microbiol. 2008; 6: 579-591Crossref PubMed Scopus (820) Google Scholar, 45.Daniel S.L. et al.Characterization of the H2- and CO-dependent chemolithotrophic potentials of the acetogens Clostridium thermoaceticum and Acetogenium kivuit.J. Bacteriol. 1990; 172: 4464-4471Crossref PubMed Google Scholar]. For example, in acetogens, ~24 molecules of CO2 are excreted as ace
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