1932

Abstract

A decade ago, a novel mechanism to drive thermodynamically unfavorable redox reactions was discovered that is used in prokaryotes to drive endergonic electron transfer reactions by a direct coupling to an exergonic redox reaction in one soluble enzyme complex. This process is referred to as flavin-based electron bifurcation, or FBEB. An important function of FBEB is that it allows the generation of reduced low-potential ferredoxin (Fd) from comparably high-potential electron donors such as NADH or molecular hydrogen (H). Fd is then the electron donor for anaerobic respiratory chains leading to the synthesis of ATP. In many metabolic scenarios, Fd is reduced by metabolic oxidoreductases and Fd then drives endergonic metabolic reactions such as H production by the reverse, electron confurcation. FBEB is energetically more economical than ATP hydrolysis or reverse electron transport as a driving force for endergonic redox reactions; thus, it does “save” cellular ATP. It is essential for autotrophic growth at the origin of life and also allows for heterotrophic growth on certain low-energy substrates.

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2018-09-08
2024-03-28
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Literature Cited

  1. 1.  Bergdoll L, ten Brink F, Nitschke W, Picot D, Baymann F 2016. From low- to high-potential bioenergetic chains: Thermodynamic constraints of Q-cycle function. Biochem. Biophys. Acta Bioenerg. 1857:1569–79
    [Google Scholar]
  2. 2.  Bertsch J, Müller V 2015. Bioenergetic constraints for conversion of syngas to biofuels in acetogenic bacteria. Biotechnol. Biofuels 8:210
    [Google Scholar]
  3. 3.  Bertsch J, Öppinger C, Hess V, Langer JD, Müller V 2015. A heterotrimeric NADH-oxidizing methylenetetrahydrofolate reductase from the acetogenic bacterium Acetobacterium woodii. J. . Bacteriol 197:1681–89
    [Google Scholar]
  4. 4.  Bertsch J, Parthasarathy A, Buckel W, Müller V 2013. An electron-bifurcating caffeyl-CoA reductase. J. Biol. Chem. 288:11304–11
    [Google Scholar]
  5. 5.  Bertsch J, Siemund AL, Kremp F, Müller V 2015. A novel route for ethanol oxidation in the acetogenic bacterium Acetobacterium woodii: the AdhE pathway. Environ. Mirobiol. 18:2913–22
    [Google Scholar]
  6. 6.  Biegel E, Müller V 2010. Bacterial Na+-translocating ferredoxin:NAD+ oxidoreductase. PNAS 107:18138–42
    [Google Scholar]
  7. 7.  Biegel E, Müller V 2011. A Na+-translocating pyrophosphatase in the acetogenic bacterium Acetobacterium woodii. J. Biol. . Chem 286:6080–84
    [Google Scholar]
  8. 8.  Biegel E, Schmidt S, González JM, Müller V 2011. Biochemistry, evolution and physiological function of the Rnf complex, a novel ion-motive electron transport complex in prokaryotes. Cell. Mol. Life Sci. 68:613–34
    [Google Scholar]
  9. 9.  Biegel E, Schmidt S, Müller V 2009. Genetic, immunological and biochemical evidence of a Rnf complex in the acetogen Acetobacterium woodii. Environ. . Microbiol 11:1438–43
    [Google Scholar]
  10. 10.  Blaut M, Peinemann S, Deppenmeier U, Gottschalk G 1990. Energy transduction in vesicles of the methanogenic strain Gö1. FEMS Microbiol. Rev. 7:367–72
    [Google Scholar]
  11. 11.  Bobik TA, Dimarco AA, Wolfe RS 1990. Formyl-methanofuran synthesis in Methanobacterium thermoautotrophicum. FEMS Microbiol. . Rev 87:323–26
    [Google Scholar]
  12. 12.  Brandt K, Müller DB, Hoffmann J, Hübert C, Brutschy B et al. 2013. Functional production of the Na+ F1FO ATP synthase from Acetobacterium woodii in Escherichia coli requires the native AtpI. J. Bioenerg. Biomembr. 45:15–23
    [Google Scholar]
  13. 13.  Brandt U 1996. Bifurcated ubihydroquinone oxidation in the cytochrome bc1 complex by proton-gated charge transfer. FEBS Lett 387:1–6
    [Google Scholar]
  14. 14.  Buckel W, Thauer RK 2013. Energy conservation via electron bifurcating ferredoxin reduction and proton/Na+ translocating ferredoxin oxidation. Biochem. Biophys. Acta Bioenerg. 1827:94–113
    [Google Scholar]
  15. 15.  Buckel W, Thauer RK 2018. Flavin-based electron bifurcation, ferredoxin, flavodoxin, and anaerobic respiration with protons (Ech) or NAD+ (Rnf) as electron acceptors: a historical review. Front. Microbiol. 9:401
    [Google Scholar]
  16. 16.  Chowdhury NP, Kahnt J, Buckel W 2015. Reduction of ferredoxin or oxygen by flavin-based electron bifurcation in Megasphaera elsdenii. . FEBS J 282:3149–60
    [Google Scholar]
  17. 17.  Chowdhury NP, Klomann K, Seubert A, Buckel W 2016. Reduction of flavodoxin by electron bifurcation and sodium ion-dependent reoxidation by NAD+ catalyzed by ferredoxin-NAD+ reductase (Rnf). J. Biol. Chem. 291:11993–2002
    [Google Scholar]
  18. 18.  Chowdhury NP, Mowafy AM, Demmer JK, Upadhyay V, Koelzer S et al. 2014. Studies on the mechanism of electron bifurcation catalyzed by electron transferring flavoprotein (Etf) and butyryl-CoA dehydrogenase (Bcd) of Acidaminococcus fermentans. J. Biol. . Chem 289:5145–57
    [Google Scholar]
  19. 19.  Costa KC, Wong PM, Wang T, Lie TJ, Dodsworth JA et al. 2010. Protein complexing in a methanogen suggests electron bifurcation and electron delivery from formate to heterodisulfide reductase. PNAS 107:11050–55
    [Google Scholar]
  20. 20.  Demmer JK, Bertsch J, Öppinger C, Wohlers H, Kayastha K et al. 2018. Molecular basis of the flavin-based electron-bifurcating caffeyl-CoA reductase reaction. FEBS Lett 592:332–42
    [Google Scholar]
  21. 21.  Demmer JK, Huang H, Wang S, Demmer U, Thauer RK, Ermler U 2015. Insights into flavin-based electron bifurcation via the NADH-dependent reduced ferredoxin:NADP+ oxidoreductase structure. J. Biol. Chem. 290:21985–95
    [Google Scholar]
  22. 22.  Demmer JK, Chowdhury NP, Selmer T, Ermler U, Buckel W 2017. The semiquinone swing in the bifurcating electron transferring flavoprotein/butyryl-CoA dehydrogenase complex from Clostridium difficile. Nat. . Commun 8:1577
    [Google Scholar]
  23. 23.  Demmer JK, Rupprecht FA, Eisinger ML, Ermler U, Langer JD 2016. Ligand binding and conformational dynamics in a flavin-based electron-bifurcating enzyme complex revealed by hydrogen-deuterium exchange mass spectrometry. FEBS Lett 590:4472–79
    [Google Scholar]
  24. 24.  Deppenmeier U 2002. The unique biochemistry of methanogenesis. Prog. Nucleic. Acid. Res. Mol. Biol. 71:223–83
    [Google Scholar]
  25. 25.  Deppenmeier U, Blaut M, Mahlmann A, Gottschalk G 1990. Reduced coenzyme F420:heterodisulfide oxidoreductase, a proton-translocating redox system in methanogenic bacteria. PNAS 87:9449–53
    [Google Scholar]
  26. 26.  Deppenmeier U, Müller V 2008. Life close to the thermodynamic limit: how methanogenic archaea conserve energy. Results Probl. Cell. Differ. 45:123–52
    [Google Scholar]
  27. 27.  Dilling S, Imkamp F, Schmidt S, Müller V 2007. Regulation of caffeate respiration in the acetogenic bacterium Acetobacterium woodii. Appl. Environ. . Microbiol 73:3630–36
    [Google Scholar]
  28. 28.  Elbehti A, Brasseur G, Lemesle-Meunier D 2000. First evidence for existence of an uphill electron transfer through the bc1 and NADH-Q oxidoreductase complexes of the acidophilic obligate chemolithotrophic ferrous ion-oxidizing bacterium Thiobacillus ferrooxidans. J. . Bacteriol 182:3602–6
    [Google Scholar]
  29. 29.  Ermler U, Grabarse W, Shima S, Goubeaud M, Thauer RK 1997. Crystal structure of methyl coenzyme M reductase: the key enzyme of biological methane formation. Science 278:1457–62
    [Google Scholar]
  30. 30.  Ferry JG 2015. Acetate metabolism in anaerobes from the domain Archaea. Life 5:1454–71
    [Google Scholar]
  31. 31.  Fritz M, Müller V 2007. An intermediate step in the evolution of ATPases—the F1FO-ATPase from Acetobacterium woodii contains F-type and V-type rotor subunits and is capable of ATP synthesis. FEBS J 274:3421–28
    [Google Scholar]
  32. 32.  Gildemyn S, Molitor B, Usack JG, Nguyen M, Rabaey K, Angenent LT 2017. Upgrading syngas fermentation effluent using Clostridium kluyveri in a continuous fermentation. Biotechnol. Biofuels 10:83
    [Google Scholar]
  33. 33.  Gottschalk G, Thauer RK 2001. The Na+-translocating methyltransferase complex from methanogenic archaea. Biochem. Biophys. Acta Bioenerg. 1505:28–36
    [Google Scholar]
  34. 34.  Greening C, Constant P, Hards K, Morales S, Oakeshott JG et al. 2015. Atmospheric hydrogen scavenging: from enzymes to ecosystems. Appl. Environ. Microbiol. 81:1190–99
    [Google Scholar]
  35. 35.  Grüber G, Manimekalai MSS, Mayer F, Müller V 2014. ATP synthases from archaea: the beauty of a molecular motor. Biochem. Biophys. Acta Bioenerg 1837:940–52
    [Google Scholar]
  36. 36.  Gunsalus RP, Wolfe RS 1980. Methyl coenzyme M reductase from Methanobacterium thermoautotrophicum. J. Biol. . Chem 255:1891–95
    [Google Scholar]
  37. 37.  Hansen B, Bokranz M, Schönheit P, Kröger A 1988. ATP formation coupled to caffeate reduction by H2 in Acetobacterium woodii NZva16. Arch. Microbiol. 150:447–51
    [Google Scholar]
  38. 38.  Hedderich R 2004. Energy-converting [NiFe] hydrogenases from archaea and extremophiles: ancestors of complex I. J. Bioenerg. Biomembr. 36:65–75
    [Google Scholar]
  39. 39.  Hedderich R, Berkessel A, Thauer RK 1990. Purification and properties of heterodisulfide reductase from Methanobacterium thermoautotrophicum (strain Marburg). Eur. J. Biochem. 193:255–61
    [Google Scholar]
  40. 40.  Hedderich R, Koch J, Linder D, Thauer RK 1994. The heterodisulfide reductase from Methanobacterium thermoautotrophicum contains sequence motifs characteristic of pyridine-nucleotide-dependent thioredoxin reductases. Eur. J. Biochem. 225:253–61
    [Google Scholar]
  41. 41.  Herrmann G, Jayamani E, Mai G, Buckel W 2008. Energy conservation via electron-transferring flavoprotein in anaerobic bacteria. J. Bacteriol. 190:784–91
    [Google Scholar]
  42. 42.  Hess V, Gallegos R, Jones JA, Barquera B, Malamy MH, Müller V 2016. Occurrence of ferredoxin:NAD+ oxidoreductase activity and its ion specificity in several gram-positive and gram-negative bacteria. PeerJ 4:e1515
    [Google Scholar]
  43. 43.  Hess V, Gonzalez JM, Parthasarathy A, Buckel W, Müller V 2013. Caffeate respiration in the acetogenic bacterium Acetobacterium woodii: a coenzyme A loop saves energy for caffeate activation. Appl. Environ. Microbiol. 79:1942–47
    [Google Scholar]
  44. 44.  Hess V, Schuchmann K, Müller V 2013. The ferredoxin:NAD+ oxidoreductase (Rnf) from the acetogen Acetobacterium woodii requires Na+ and is reversibly coupled to the membrane potential. J. Biol. Chem. 288:31496–502
    [Google Scholar]
  45. 45.  Hess V, Vitt S, Müller V 2011. A caffeyl-coenzyme A synthetase initiates caffeate activation prior to caffeate reduction in the acetogenic bacterium Acetobacterium woodii. J. . Bacteriol 193:971–78
    [Google Scholar]
  46. 46.  Hoben JP, Lubner CE, Ratzloff MW, Schut GJ, Nguyen DMN et al. 2017. Equilibrium and ultrafast kinetic studies manipulating electron transfer: A short-lived flavin semiquinone is not sufficient for electron bifurcation. J. Biol. Chem. 292:14039–49
    [Google Scholar]
  47. 47.  Huang H, Wang S, Moll J, Thauer RK 2012. Electron bifurcation involved in the energy metabolism of the acetogenic bacterium Moorella thermoacetica growing on glucose or H2 plus CO2. J. Bacteriol. 194:3689–99
    [Google Scholar]
  48. 48.  Hugenholtz J, Ljungdahl LG 1990. Metabolism and energy generation in homoacetogenic clostridia. FEMS Microbiol. Rev. 87:383–89
    [Google Scholar]
  49. 49.  Ide T, Bäumer S, Deppenmeier U 1999. Energy conservation by the H2:heterodisulfide oxidoreductase from Methanosarcina mazei Gö1: identification of two proton-translocating segments. J. Bacteriol. 181:4076–80
    [Google Scholar]
  50. 50.  Imkamp F, Biegel E, Jayamani E, Buckel W, Müller V 2007. Dissection of the caffeate respiratory chain in the acetogen Acetobacterium woodii: indications for a Rnf-type NADH dehydrogenase as coupling site. J. Bacteriol. 189:8145–53
    [Google Scholar]
  51. 51.  Imkamp F, Müller V 2002. Chemiosmotic energy conservation with Na+ as the coupling ion during hydrogen-dependent caffeate reduction by Acetobacterium woodii. J. . Bacteriol 184:1947–51
    [Google Scholar]
  52. 52.  Imlay JA 2013. The molecular mechanisms and physiological consequences of oxidative stress: lessons from a model bacterium. Nat. Rev. Microbiol. 11:443–54
    [Google Scholar]
  53. 53.  Jenney FE Jr., Adams MW 2008. Hydrogenases of the model hyperthermophiles. Ann. N. Y. Acad. Sci. 1125:252–66
    [Google Scholar]
  54. 54.  Jeon JH, Lim JK, Kim MS, Yang TJ, Lee SH et al. 2015. Characterization of the frhAGB-encoding hydrogenase from a non-methanogenic hyperthermophilic archaeon. Extremophiles 19:109–18
    [Google Scholar]
  55. 55.  Jeong J, Bertsch J, Hess V, Choi S, Choi IG et al. 2015. Energy conservation model based on genomic and experimental analyses of a carbon monoxide-utilizing, butyrate-forming acetogen, Eubacterium limosum KIST612. Appl. Environ. Microbiol. 81:4782–90
    [Google Scholar]
  56. 56.  Jungermann K, Rupprecht E, Ohrloff C, Thauer R, Decker K 1971. Regulation of the reduced nicotinamide adenine dinucleotide-ferredoxin reductase system in Clostridium kluyveri. J. Biol. . Chem 246:960–63
    [Google Scholar]
  57. 57.  Kaster AK, Moll J, Parey K, Thauer RK 2011. Coupling of ferredoxin and heterodisulfide reduction via electron bifurcation in hydrogenotrophic methanogenic archaea. PNAS 108:2981–86
    [Google Scholar]
  58. 58.  Ledbetter RN, Garcia Costas AM, Lubner CE, Mulder DW, Tokmina-Lukaszewska M et al. 2017. The electron bifurcating FixABCX protein complex from Azotobacter vinelandii: generation of low-potential reducing equivalents for nitrogenase catalysis. Biochemistry 56:4177–90
    [Google Scholar]
  59. 59.  Leigh JA, Rinehart KL, Wolfe RS 1985. Methanofuran (carbon dioxide reducing factor), a formyl carrier in methane production from carbon dioxide in Methanobacterium. . Biochemistry 24:995–99
    [Google Scholar]
  60. 60.  Li F, Hinderberger J, Seedorf H, Zhang J, Buckel W, Thauer RK 2008. Coupled ferredoxin and crotonyl coenzyme A (CoA) reduction with NADH catalyzed by the butyryl-CoA dehydrogenase/Etf complex from Clostridium kluyveri. J. Bacteriol. 190:843–50
    [Google Scholar]
  61. 61.  Liew F, Henstra AM, Köpke M, Winzer K, Simpson SD, Minton NP 2017. Metabolic engineering of Clostridium autoethanogenum for selective alcohol production. Metab. Eng. 40:104–14
    [Google Scholar]
  62. 62.  Ljungdahl LG 1986. The autotrophic pathway of acetate synthesis in acetogenic bacteria. Annu. Rev. Microbiol. 40:415–50
    [Google Scholar]
  63. 63.  Lubner CE, Jennings DP, Mulder DW, Schut GJ, Zadvornyy OA et al. 2017. Mechanistic insights into energy conservation by flavin-based electron bifurcation. Nat. Chem. Biol. 13:655–59
    [Google Scholar]
  64. 64.  Mathies RA, Lin SW, Ames JB, Pollard WT 1991. From femtoseconds to biology: mechanism of bacteriorhodopsin's light-driven proton pump. Annu. Rev. Biophys. Biophys. Chem. 20:491–518
    [Google Scholar]
  65. 65.  May A, Hillmann F, Riebe O, Fischer RJ, Bahl H 2004. A rubrerythrin-like oxidative stress protein of Clostridium acetobutylicum is encoded by a duplicated gene and identical to the heat shock protein Hsp21. FEMS Microbiol. Lett. 238:249–54
    [Google Scholar]
  66. 66.  McMillan DG, Ferguson SA, Dey D, Schroder K, Aung HL et al. 2011. A1Ao-ATP synthase of Methanobrevibacter ruminantium couples sodium ions for ATP synthesis under physiological conditions. J. Biol. Chem. 286:39882–92
    [Google Scholar]
  67. 67.  McTernan PM, Chandrayan SK, Wu CH, Vaccaro BJ, Lancaster WA et al. 2014. Intact functional fourteen-subunit respiratory membrane-bound [NiFe]-hydrogenase complex of the hyperthermophilic archaeon Pyrococcus furiosus. J. Biol. . Chem 289:19364–72
    [Google Scholar]
  68. 68.  Mishra S, Imlay JA 2013. An anaerobic bacterium, Bacteroides thetaiotaomicron, uses a consortium of enzymes to scavenge hydrogen peroxide. Mol. Microbiol. 90:1356–71
    [Google Scholar]
  69. 69.  Misra HP, Fridovich I 1971. The generation of superoxide radical during the autoxidation of ferredoxins. J. Biol. Chem. 246:6886–90
    [Google Scholar]
  70. 70.  Mock J, Wang S, Huang H, Kahnt J, Thauer RK 2014. Evidence for a hexaheteromeric methylenetetrahydrofolate reductase in Moorella thermoacetica. J. . Bacteriol 196:3303–14
    [Google Scholar]
  71. 71.  Mock J, Zheng Y, Mueller AP, Ly S, Tran L et al. 2015. Energy conservation associated with ethanol formation from H2 and CO2 in Clostridium autoethanogenum involving electron bifurcation. J. Bacteriol. 197:2965–80
    [Google Scholar]
  72. 72.  Müller V, Blaut M, Gottschalk G 1988. The transmembrane electrochemical gradient of Na+ as driving force for methanol oxidation in Methanosarcina barkeri. Eur. J. . Biochem 172:601–6
    [Google Scholar]
  73. 73.  Müller V, Frerichs J 2013. Acetogenic bacteria. eLS G Pettis Chichester: John Wiley https://doi.org/10.1002/9780470015902.a0020086.pub2
    [Crossref] [Google Scholar]
  74. 74.  Müller V, Grüber G 2003. ATP synthases: structure, function and evolution of unique energy converters. Cell. Mol. Life Sci. 60:474–94
    [Google Scholar]
  75. 75.  Müller V, Hess V 2017. The minimum biological energy quantum. Front. Microbiol. 8:2019
    [Google Scholar]
  76. 76.  Müller V, Winner C, Gottschalk G 1988. Electron transport-driven sodium extrusion during methanogenesis from formaldehyde + H2 by Methanosarcina barkeri. Eur. J. Biochem 178:519–25
    [Google Scholar]
  77. 77.  Nakos G, Mortenson L 1971. Purification and properties of hydrogenase, an iron sulfur protein, from Clostridium pasteurianum W5. Biochem. Biophys. Acta Enzymol. 227:576–83
    [Google Scholar]
  78. 78.  Nitschke W, Russell MJ 2012. Redox bifurcations: mechanisms and importance to life now, and at its origin; a widespread means of energy conversion in biology unfolds. BioEssays 34:106–9
    [Google Scholar]
  79. 79.  Olausson T, Fjelstrom O, Meuller J, Rydstrom J 1995. Molecular biology of nicotinamide nucleotide transhydrogenase—a unique proton pump. Biochem. Biophys. Acta Bioenerg. 1231:1–19
    [Google Scholar]
  80. 80.  Pedersen A, Karlsson GB, Rydström J 2008. Proton-translocating transhydrogenase: an update of unsolved and controversial issues. J. Bioenerg. Biomembr. 40:463–73
    [Google Scholar]
  81. 81.  Pereira IA, Ramos AR, Grein F, Marques MC, da Silva SM, Venceslau SS 2011. A comparative genomic analysis of energy metabolism in sulfate reducing bacteria and archaea. Front. Microbiol. 2:69
    [Google Scholar]
  82. 82.  Perez JM, Richter H, Loftus SE, Angenent LT 2013. Biocatalytic reduction of short-chain carboxylic acids into their corresponding alcohols with syngas fermentation. Biotechnol. Bioeng. 110:1066–77
    [Google Scholar]
  83. 83.  Peters JW, Miller AF, Jones AK, King PW, Adams MW 2016. Electron bifurcation. Curr. Opin. Chem. Biol. 31:146–52
    [Google Scholar]
  84. 84.  Ragsdale SW 2008. Enzymology of the Wood-Ljungdahl pathway of acetogenesis. Ann. N. Y. Acad. Sci. 1125:129–36
    [Google Scholar]
  85. 85.  Ragsdale SW, Pierce E 2008. Acetogenesis and the Wood-Ljungdahl pathway of CO2 fixation. Biochim. Biophys. Acta 1784:1873–98
    [Google Scholar]
  86. 86.  Richter H, Molitor B, Diender M, Sousa DZ, Angenent LT 2016. A narrow pH range supports butanol, hexanol, and octanol production from syngas in a continuous co-culture of Clostridium ljungdahlii and Clostridium kluyveri with in-line product extraction. Front. Microbiol. 7:1773
    [Google Scholar]
  87. 87.  Riebe O, Fischer RJ, Bahl H 2007. Desulfoferrodoxin of Clostridium acetobutylicum functions as a superoxide reductase. FEBS Lett 581:5605–10
    [Google Scholar]
  88. 88.  Riebe O, Fischer RJ, Wampler DA, Kurtz DM Jr., Bahl H 2009. Pathway for H2O2 and O2 detoxification in Clostridium acetobutylicum. . Microbiology 155:16–24
    [Google Scholar]
  89. 89.  Schink B 2015. Electron confurcation in anaerobic lactate oxidation. Environ. Microbiol. 17:543
    [Google Scholar]
  90. 90.  Schlegel K, Welte C, Deppenmeier U, Müller V 2012. Electron transport during aceticlastic methanogenesis by Methanosarcina acetivorans involves a sodium-translocating Rnf complex. FEBS. J. 279:4444–52
    [Google Scholar]
  91. 91.  Schmehl M, Jahn A, Vilsendorf AMZ, Hennecke S, Masepohl B et al. 1993. Identification of a new class of nitrogen fixation genes in Rhodobacter capsulatus—a putative membrane complex involved in electron transport to nitrogenase. Mol. Gen. Genet. 241:602–15
    [Google Scholar]
  92. 92.  Schuchmann K, Müller V 2012. A bacterial electron bifurcating hydrogenase. J. Biol. Chem. 287:31165–71
    [Google Scholar]
  93. 93.  Schuchmann K, Müller V 2013. Direct and reversible hydrogenation of CO2 to formate by a bacterial carbon dioxide reductase. Science 342:1382–85
    [Google Scholar]
  94. 94.  Schuchmann K, Müller V 2014. Autotrophy at the thermodynamic limit of life: a model for energy conservation in acetogenic bacteria. Nat. Rev. Microbiol. 12:809–21
    [Google Scholar]
  95. 95.  Schut GJ, Adams MW 2009. The iron-hydrogenase of Thermotoga maritima utilizes ferredoxin and NADH synergistically: a new perspective on anaerobic hydrogen production. J. Bacteriol. 191:4451–57
    [Google Scholar]
  96. 96.  Setzke E, Hedderich R, Heiden S, Thauer RK 1994. H2:heterodisulfide oxidoreductase complex from Methanobacterium thermoautotrophicum—composition and properties. Eur. J. Biochem. 220:139–48
    [Google Scholar]
  97. 97.  Spahn S, Brandt K, Müller V 2015. A low phosphorylation potential in the acetogen Acetobacterium woodii reflects its lifestyle at the thermodynamic edge of life. Arch. Microbiol. 197:745–51
    [Google Scholar]
  98. 98.  Storz G, Imlay JA 1999. Oxidative stress. Curr. Opin. Microbiol. 2:188–94
    [Google Scholar]
  99. 99.  Thauer RK, Jungermann K, Henninger H, Wenning J, Decker K 1968. The energy metabolism of Clostridium kluyveri. Eur. J. . Biochem 4:173–80
    [Google Scholar]
  100. 100.  Thauer RK, Jungermann K, Rupprecht E, Decker K 1969. Hydrogen formation from NADH in cell-free extracts of Clostridium kluyveri: acetyl coenzyme A requirement and ferredoxin dependence. FEBS Lett 4:108–12
    [Google Scholar]
  101. 101.  Thauer RK, Kaster AK, Goenrich M, Schick M, Hiromoto T, Shima S 2010. Hydrogenases from methanogenic archaea, nickel, a novel cofactor, and H2 storage. Annu. Rev. Biochem. 79:507–36
    [Google Scholar]
  102. 102.  Thauer RK, Kaster AK, Seedorf H, Buckel W, Hedderich R 2008. Methanogenic archaea: ecologically relevant differences in energy conservation. Nat. Rev. Microbiol. 6:579–91
    [Google Scholar]
  103. 103.  Thauer RK, Rupprecht E, Ohrloff C, Jungermann K, Decker K 1971. Regulation of the reduced nicotinamide adenine dinucleotide phosphate-ferredoxin reductase system in Clostridium kluyveri. J. Biol. . Chem 246:954–59
    [Google Scholar]
  104. 104.  Tremblay PL, Zhang T, Dar SA, Leang C, Lovley DR 2012. The Rnf complex of Clostridium ljungdahlii is a proton-translocating ferredoxin:NAD+ oxidoreductase essential for autotrophic growth. mBio 4:e00406–12
    [Google Scholar]
  105. 105.  Tschech A, Pfennig N 1984. Growth yield increase linked to caffeate reduction in Acetobacterium woodii. Arch. . Microbiol 137:163–67
    [Google Scholar]
  106. 106.  Verhagen MFJM, O'Rourke T, Adams MWW 1999. The hyperthermophilic bacterium, Thermotoga maritima, contains an unusually complex iron-hydrogenase: amino acid sequence analyses versus biochemical characterization. Biochim. Biophys. Acta 1412:212–29
    [Google Scholar]
  107. 107.  Wagner T, Ermler U, Shima S 2016. The methanogenic CO2 reducing-and-fixing enzyme is bifunctional and contains 46 [4Fe-4S] clusters. Science 354:114–17
    [Google Scholar]
  108. 108.  Wagner T, Koch J, Ermler U, Shima S 2017. Methanogenic heterodisulfide reductase (HdrABC-MvhAGD) uses two noncubane [4Fe-4S] clusters for reduction. Science 357:699–703
    [Google Scholar]
  109. 109.  Wang S, Huang H, Kahnt J, Mueller AP, Köpke M, Thauer RK 2013. NADP-specific electron-bifurcating [FeFe]-hydrogenase in a functional complex with formate dehydrogenase in Clostridium autoethanogenum grown on CO. J. Bacteriol. 195:4373–86
    [Google Scholar]
  110. 110.  Wang S, Huang H, Kahnt J, Thauer RK 2013. Clostridium acidurici electron-bifurcating formate dehydrogenase. App. Environ. Microbiol. 79:6176–79
    [Google Scholar]
  111. 111.  Wang S, Huang H, Kahnt J, Thauer RK 2013. A reversible electron-bifurcating ferredoxin- and NAD-dependent [FeFe]-hydrogenase (HydABC) in Moorella thermoacetica. J. . Bacteriol 195:1267–75
    [Google Scholar]
  112. 112.  Wang S, Huang H, Moll J, Thauer RK 2010. NADP+ reduction with reduced ferredoxin and NADP+ reduction with NADH are coupled via an electron bifurcating enzyme complex in Clostridium kluyveri. J. . Bacteriol 192:5115–23
    [Google Scholar]
  113. 113.  Weghoff MC, Bertsch J, Müller V 2015. A novel mode of lactate metabolism in strictly anaerobic bacteria. Environ. Microbiol. 17:670–77
    [Google Scholar]
  114. 114.  Welte C, Kallnik V, Grapp M, Bender G, Ragsdale S, Deppenmeier U 2010. Function of Ech hydrogenase in ferredoxin-dependent, membrane-bound electron transport in Methanosarcina mazei. J. . Bacteriol 192:674–78
    [Google Scholar]
  115. 115.  Welte C, Krätzer C, Deppenmeier U 2010. Involvement of Ech hydrogenase in energy conservation of Methanosarcina mazei. . FEBS J 277:3396–403
    [Google Scholar]
  116. 116.  Wood PM 1988. The potential diagram for oxygen at pH 7. Biochem. J. 253:287–89
    [Google Scholar]
  117. 117.  Yan Z, Wang M, Ferry JG 2017. A ferredoxin- and F420H2-dependent, electron-bifurcating, heterodisulfide reductase with homologs in the domains Bacteria and Archaea. mBio 8:02285–16
    [Google Scholar]
  118. 118.  Yu H, Wu C-H, Schut GJ, Haja DK, Zhao G et al. 2018. Structure of an ancient respiratory system. Cell 173:1636–49.e16
    [Google Scholar]
  119. 119.  Zheng Y, Kahnt J, Kwon IH, Mackie RI, Thauer RK 2014. Hydrogen formation and its regulation in Ruminococcus albus: involvement of an electron-bifurcating [FeFe]-hydrogenase, of a non-electron-bifurcating [FeFe]-hydrogenase, and of a putative hydrogen-sensing [FeFe]-hydrogenase. J. Bacteriol. 196:3840–52
    [Google Scholar]
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