Skip to main content

Advertisement

Log in

Energy-converting hydrogenases: the link between H2 metabolism and energy conservation

  • Review
  • Published:
Cellular and Molecular Life Sciences Aims and scope Submit manuscript

Abstract

The reversible interconversion of molecular hydrogen and protons is one of the most ancient microbial metabolic reactions and catalyzed by hydrogenases. A widespread yet largely enigmatic group comprises multisubunit [NiFe] hydrogenases, that directly couple H2 metabolism to the electrochemical ion gradient across the membranes of bacteria and of archaea. These complexes are collectively referred to as energy-converting hydrogenases (Ech), as they reversibly transform redox energy into physicochemical energy. Redox energy is typically provided by a low potential electron donor such as reduced ferredoxin to fuel H2 evolution and the establishment of a transmembrane electrochemical ion gradient (\(\Delta \tilde{\mu }_{\text{ion}}\)). The \(\Delta \tilde{\mu }_{\text{ion}}\) is then utilized by an ATP synthase for energy conservation by generating ATP. This review describes the modular structure/function of Ech complexes, focuses on insights into the energy-converting mechanisms, describes the evolutionary context and delves into the implications of relying on an Ech complex as respiratory enzyme for microbial metabolism.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12
Fig. 13
Fig. 14

Similar content being viewed by others

Abbreviations

\(\Delta G_{0}{}^{\prime }\) :

Gibbs free energy change under standard conditions

\(\Delta \tilde{\mu }_{\text{ion}}\) :

Transmembrane electrochemical ion gradient

Δψ :

Membrane potential

Coo:

CO-oxidizing hydrogenase

\(E_{0}{}^{{\prime }}\) :

Redox potential under standard conditions but pH 7.0

Ech:

Energy-converting hydrogenase

Ech1:

CO-oxidizing energy-converting hydrogenase 1 from T. kivui

F420 :

Coenzyme F420

FBEB:

Flavin-based electron bifurcation

Fd:

Ferredoxin

Fhl:

Formate hydrogen lyase

Fpo:

F420H2 dehydrogenase

MAF:

Mixed acid fermentation

Mrp:

Multiple resistance and pH

Nuo/Nqo:

NADH:ubiquinone/quinone oxidoreductase

Pfl:

Pyruvate-formate lyase

pH2 :

Hydrogen partial pressure

Rnf:

Ferredoxin:NAD oxidoreductase

SLP:

Substrate-level-phosphorylation

WLP:

Wood–Ljungdahl pathway

References

  1. Wächtershäuser G (2007) On the chemistry and evolution of the pioneer organism. Chem Biodivers 4:584–602

    Article  PubMed  Google Scholar 

  2. Varma SJ, Muchowska KB, Chatelain P, Moran J (2018) Native iron reduces CO2 to intermediates and end-products of the acetyl-CoA pathway. Nat Ecol Evol 2:1019–1024

    Article  PubMed  PubMed Central  Google Scholar 

  3. Martin W, Russell MJ (2007) On the origin of biochemistry at an alkaline hydrothermal vent. Philos Trans R Soc Lond B Biol Sci 362:1887–1925

    Article  PubMed  CAS  Google Scholar 

  4. Mayhew LE, Ellison ET, McCollom TM, Trainor TP, Templeton AS (2013) Hydrogen generation from low-temperature water–rock reactions. Nat Geosci 6:478–484

    Article  CAS  Google Scholar 

  5. Schut GJ, Zadvornyy O, Wu CH, Peters JW, Boyd ES, Adams MW (2016) The role of geochemistry and energetics in the evolution of modern respiratory complexes from a proton-reducing ancestor. Biochim Biophys Acta 1857:958–970

    Article  PubMed  CAS  Google Scholar 

  6. Eck RV, Dayhoff MO (1966) Evolution of the structure of ferredoxin based on living relics of primitive amino acid sequences. Science 152:363–366

    Article  PubMed  CAS  Google Scholar 

  7. Thauer RK, Jungermann K, Decker K (1977) Energy conservation in chemotrophic anaerobic bacteria. Bacteriol Rev 41:100–180

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  8. Meuer J, Kuettner HC, Zhang JK, Hedderich R, Metcalf WW (2002) Genetic analysis of the archaeon Methanosarcina barkeri Fusaro reveals a central role for Ech hydrogenase and ferredoxin in methanogenesis and carbon fixation. Proc Natl Acad Sci USA 99:5632–5637

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  9. Mitchell P (1966) Chemiosmotic coupling in oxidative and photosynthetic phosphorylation. Biol Rev Camb Philos Soc 41:445–502

    Article  PubMed  CAS  Google Scholar 

  10. Grüber G, Manimekalai MS, Mayer F, Müller V (2014) ATP synthases from archaea: the beauty of a molecular motor. Biochim Biophys Acta 1837:940–952

    Article  PubMed  CAS  Google Scholar 

  11. Müller V (2003) Energy conservation in acetogenic bacteria. Appl Environ Microbiol 69:6345–6353

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  12. Oesterhelt D, Tittor J (1989) Two pumps, one principle: light-driven ion transport in halobacteria. Trends Biochem Sci 14:57–61

    Article  PubMed  CAS  Google Scholar 

  13. Krebs MP, Khorana HG (1993) Mechanism of light-dependent proton translocation by bacteriorhodopsin. J Bacteriol 175:1555–1560

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  14. Mukohata Y, Ihara K, Tamura T, Sugiyama Y (1999) Halobacterial rhodopsins. J Biochem 125:649–657

    Article  PubMed  CAS  Google Scholar 

  15. Maeshima M (2000) Vacuolar H+-pyrophosphatase. Biochim Biophys Acta 1465:37–51

    Article  PubMed  CAS  Google Scholar 

  16. Biegel E, Müller V (2011) A Na+-translocating pyrophosphatase in the acetogenic bacterium Acetobacterium woodii. J Biol Chem 286:6080–6084

    Article  PubMed  CAS  Google Scholar 

  17. Baykov AA, Malinen AM, Luoto HH, Lahti R (2013) Pyrophosphate-fueled Na+ and H+ transport in prokaryotes. Microbiol Mol Biol Rev 77:267–276

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  18. Dimroth P, Schink B (1998) Energy conservation in the decarboxylation of dicarboxylic acids by fermenting bacteria. Arch Microbiol 170:69–77

    Article  PubMed  CAS  Google Scholar 

  19. 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 172:601–606

    Article  PubMed  Google Scholar 

  20. Gottschalk G, Thauer RK (2001) The Na+-translocating methyltransferase complex from methanogenic archaea. Biochim Biophys Acta 1505:28–36

    Article  PubMed  CAS  Google Scholar 

  21. Deppenmeier U (2002) Redox-driven proton translocation in methanogenic archaea. Cell Mol Life Sci 59:1–21

    Article  Google Scholar 

  22. Brandt U, Kerscher S, Dröse S, Zwicker K, Zickermann V (2003) Proton pumping by NADH:ubiquinone oxidoreductase. A redox driven conformational change mechanism? FEBS Lett 545:9–17

    Article  PubMed  CAS  Google Scholar 

  23. 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 288:31496–31502

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  24. Vignais PM, Billoud B (2007) Occurrence, classification, and biological function of hydrogenases: an overview. Chem Rev 107:4206–4272

    Article  PubMed  CAS  Google Scholar 

  25. Vignais PM, Billoud B, Meyer J (2001) Classification and phylogeny of hydrogenases. FEMS Microbiol Rev 25:455–501

    Article  PubMed  CAS  Google Scholar 

  26. Tersteegen A, Hedderich R (1999) Methanobacterium thermoautotrophicum encodes two multisubunit membrane-bound [NiFe] hydrogenases. Transcription of the operons and sequence analysis of the deduced proteins. Eur J Biochem 264:930–943

    Article  PubMed  CAS  Google Scholar 

  27. Hedderich R (2004) Energy-converting [NiFe] hydrogenases from archaea and extremophiles: ancestors of complex I. J Bioenerg Biomembr 36:65–75

    Article  PubMed  CAS  Google Scholar 

  28. Hedderich R, Forzi L (2005) Energy-converting [NiFe] hydrogenases: more than just H2 activation. J Mol Microbiol Biotechnol 10:92–104

    Article  PubMed  CAS  Google Scholar 

  29. Greening C, Biswas A, Carere CR, Jackson CJ, Taylor MC, Stott MB, Cook GM, Morales SE (2016) Genomic and metagenomic surveys of hydrogenase distribution indicate H2 is a widely utilised energy source for microbial growth and survival. ISME J 10:761–777

    Article  PubMed  CAS  Google Scholar 

  30. Sondergaard D, Pedersen CN, Greening C (2016) HydDB: a web tool for hydrogenase classification and analysis. Sci Rep 6:1–8

    Article  CAS  Google Scholar 

  31. Böhm R, Sauter M, Böck A (1990) Nucleotide sequence and expression of an operon in Escherichia coli coding for formate hydrogen lyase components. Mol Microbiol 4:231–243

    Article  PubMed  CAS  Google Scholar 

  32. Sauter M, Böhm R, Böck A (1992) Mutational analysis of the operon (hyc) determining hydrogenase 3 formation in Escherichia coli. Mol Microbiol 6:1523–1532

    Article  PubMed  CAS  Google Scholar 

  33. Andrews SC, Berks BC, McClay J, Ambler A, Quail MA, Golby P, Guest JR (1997) A 12-cistron Escherichia coli operon (hyf) encoding a putative proton-translocating formate hydrogenlyase system. Microbiology 143:3633–3647

    Article  PubMed  CAS  Google Scholar 

  34. McDowall JS, Murphy BJ, Haumann M, Palmer T, Armstrong FA, Sargent F (2014) Bacterial formate hydrogenlyase complex. Proc Natl Acad Sci USA 111:E3948–E3956

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  35. Sargent F (2016) The model [NiFe]-hydrogenases of Escherichia coli. Adv Microb Physiol 68:433–507

    Article  PubMed  CAS  Google Scholar 

  36. Rossmann R, Maier T, Lottspeich F, Böck A (1995) Characterisation of a protease from Escherichia coli involved in hydrogenase maturation. Eur J Biochem 227:545–550

    Article  PubMed  CAS  Google Scholar 

  37. Sawers G (1994) The hydrogenases and formate dehydrogenases of Escherichia coli. Antonie van Leeuwenhoek 66:57–88

    Article  PubMed  CAS  Google Scholar 

  38. Trchounian A, Sawers G (2014) Novel insights into the bioenergetics of mixed-acid fermentation: can hydrogen and proton cycles combine to help maintain a proton motive force? IUBMB Life 66:1–7

    Article  PubMed  CAS  Google Scholar 

  39. Skibinski DA et al (2002) Regulation of the hydrogenase-4 operon of Escherichia coli by the sigma54-dependent transcriptional activators FhlA and HyfR. J Bacteriol 184:6453–6642

    Article  CAS  Google Scholar 

  40. Lee HS et al (2008) The complete genome sequence of Thermococcus onnurineus NA1 reveals a mixed heterotrophic and carboxydotrophic metabolism. J Bacteriol 190:7491–7499

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  41. Lim JK, Kang SG, Lebedinsky AV, Lee JH, Lee HS (2010) Identification of a novel class of membrane-bound [NiFe]-hydrogenases in Thermococcus onnurineus NA1 by in silico analysis. Appl Environ Microbiol 76:6286–6289

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  42. Lim JK, Bae SS, Kim TW, Lee JH, Lee HS, Kang SG (2012) Thermodynamics of formate-oxidizing metabolism and implications for H2 production. Appl Environ Microbiol 78:7393–7397

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  43. Kim YJ et al (2010) Formate-driven growth coupled with H2 production. Nature 467:352–355

    Article  PubMed  CAS  Google Scholar 

  44. Lim JK, Mayer F, Kang SG, Müller V (2014) Energy conservation by oxidation of formate to carbon dioxide and hydrogen via a sodium ion current in a hyperthermophilic archaeon. Proc Natl Acad Sci USA 111:11497–11502

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  45. Mayer F, Müller V (2013) Adaptations of anaerobic archaea to life under extreme energy limitation. FEMS Microbiol Rev 38:449–472

    Article  PubMed  CAS  Google Scholar 

  46. Mayer F, Lim JK, Langer JD, Kang SG, Müller V (2015) Na+ transport by the A1AO-ATP synthase purified from Thermococcus onnurineus and reconstituted into liposomes. J Biol Chem 290:6994–7002

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  47. Rodkey FL, O’Neal JD, Collison HA, Uddin DE (1974) Relative affinity of hemoglobin S and hemoglobin A for carbon monoxide and oxygen. Clin Chem 20:83–84

    Article  PubMed  CAS  Google Scholar 

  48. Ragsdale SW (2004) Life with carbon monoxide. Crit Rev Biochem Mol Biol 39:165–195

    Article  PubMed  CAS  Google Scholar 

  49. Goldet G, Brandmayr C, Stripp ST, Happe T, Cavazza C, Fontecilla-Camps JC, Armstrong FA (2009) Electrochemical kinetic investigations of the reactions of [FeFe]-hydrogenases with carbon monoxide and oxygen: comparing the importance of gas tunnels and active-site electronic/redox effects. J Am Chem Soc 131:14979–14989

    Article  PubMed  CAS  Google Scholar 

  50. Buckel W, Thauer RK (2013) Energy conservation via electron bifurcating ferredoxin reduction and proton/Na+ translocating ferredoxin oxidation. Biochim Biophys Acta 1827:94–113

    Article  PubMed  CAS  Google Scholar 

  51. Uffen RL (1983) Metabolism of carbon monoxide by Rhodopseudomonas gelatinosa: cell growth and properties of the oxidation system. J Bacteriol 155:956–965

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  52. Uffen RL (1976) Anaerobic growth of a Rhodopseudomonas species in the dark with carbon monoxide as sole carbon and energy substrate. Proc Natl Acad Sci USA 73:3298–3302

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  53. Daniels L, Fuchs G, Thauer RK, Zeikus JG (1977) Carbon monoxide oxidation by methanogenic bacteria. J Bacteriol 132:118–126

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  54. Bonam D, Lehman L, Roberts GP, Ludden PW (1989) Regulation of carbon monoxide dehydrogenase and hydrogenase in Rhodospirillum rubrum: effects of CO and oxygen on synthesis and activity. J Bacteriol 171:3102–3107

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  55. Kerby RL, Ludden PW, Roberts GP (1995) Carbon monoxide-dependent growth of Rhodospirillum rubrum. J Bacteriol 177:2241–2244

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  56. Fox JD, He Y, Shelver D, Roberts GP, Ludden PW (1996) Characterization of the region encoding the CO-induced hydrogenase of Rhodospirillum rubrum. J Bacteriol 178:6200–6208

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  57. Fox JD, Kerby RL, Roberts GP, Ludden PW (1996) Characterization of the CO-induced, CO-tolerant hydrogenase from Rhodospirillum rubrum and the gene encoding the large subunit of the enzyme. J Bacteriol 178:1515–1524

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  58. Shelver D, Kerby RL, He Y, Roberts GP (1997) CooA, a CO-sensing transcription factor from Rhodospirillum rubrum, is a CO-binding heme protein. Proc Natl Acad Sci USA 94:11216–11220

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  59. Svetlitchnyi VA, Sokolova TG, Gerhardt M, Ringpfeil M, Kostrikina NA, Zavarzin GA (1991) Carboxydothermus hydrogenoformans gen. nov. sp. nov., a CO-utilizing thermophilic anaerobic bacterium from hydrothermal environments of Kunashir Island. Syst Appl Microbiol 14:254–260

    Article  Google Scholar 

  60. Sokolova TG, Gonzalez JM, Kostrikina NA, Chernyh NA, Slepova TV, Bonch-Osmolovskaya EA, Robb FT (2004) Thermosinus carboxydivorans gen. nov., sp. nov., a new anaerobic, thermophilic, carbon-monoxide-oxidizing, hydrogenogenic bacterium from a hot pool of Yellowstone National Park. Int J Syst Evol Microbiol 54:2353–2359

    Article  PubMed  CAS  Google Scholar 

  61. Sokolova TG, Jeanthon C, Kostrikina NA, Chernyh NA, Lebedinsky AV, Stackebrandt E, Bonch-Osmolovskaya EA (2004) The first evidence of anaerobic CO oxidation coupled with H2 production by a hyperthermophilic archaeon isolated from a deep-sea hydrothermal vent. Extremophiles 8:317–323

    Article  PubMed  CAS  Google Scholar 

  62. Daniel SL, Hsu T, Dean SI, Drake HL (1990) Characterization of the H2-dependent and CO-dependent chemolithotrophic potentials of the acetogens Clostridium thermoaceticum and Acetogenium kivui. J Bacteriol 172:4464–4471

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  63. Rother M, Metcalf WW (2004) Anaerobic growth of Methanosarcina acetivorans C2A on carbon monoxide: an unusual way of life for a methanogenic archaeon. Proc Natl Acad Sci USA 101:16929–16934

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  64. Parshina SN et al (2005) Desulfotomaculum carboxydivorans sp. nov., a novel sulfate-reducing bacterium capable of growth at 100% CO. Int J Syst Evol Microbiol 55:2159–2165

    Article  PubMed  CAS  Google Scholar 

  65. Soboh B, Linder D, Hedderich R (2002) Purification and catalytic properties of a CO-oxidizing:H2-evolving enzyme complex from Carboxydothermus hydrogenoformans. Eur J Biochem 269:5712–5721

    Article  PubMed  CAS  Google Scholar 

  66. Bonam D, Ludden PW (1987) Purification and characterization of carbon monoxide dehydrogenase, a nickel, zinc, iron-sulfur protein, from Rhodospirillum rubrum. J Biol Chem 262:2980–2987

    Article  PubMed  CAS  Google Scholar 

  67. Drennan CL, Heo J, Sintchak MD, Schreiter E, Ludden PW (2001) Life on carbon monoxide: X-ray structure of Rhodospirillum rubrum Ni–Fe–S carbon monoxide dehydrogenase. Proc Natl Acad Sci USA 98:11973–11978

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  68. Ensign SA, Ludden PW (1991) Characterization of the CO oxidation/H2 evolution system of Rhodospirillum rubrum. J Biol Chem 266:18395–18403

    Article  PubMed  CAS  Google Scholar 

  69. Svetlitchnyi V, Peschel C, Acker G, Meyer O (2001) Two membrane-associated NiFeS-carbon monoxide dehydrogenases from the anaerobic carbon-monoxide-utilizing eubacterium Carboxydothermus hydrogenoformans. J Bacteriol 183:5134–5144

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  70. Schoelmerich MC, Müller V (2019) Energy conservation by a hydrogenase-dependent chemiosmotic mechanism in an ancient metabolic pathway. Proc Natl Acad Sci USA 116:6329–6334

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  71. Weghoff MC, Müller V (2016) CO metabolism in the thermophilic acetogen Thermoanaerobacter kivui. Appl Environ Microbiol 82:2312–2319

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  72. Hess V, Poehlein A, Weghoff MC, Daniel R, Müller V (2014) A genome-guided analysis of energy conservation in the thermophilic, cytochrome-free acetogenic bacterium Thermoanaerobacter kivui. BMC Genom 15:1139

    Article  CAS  Google Scholar 

  73. Maness PC, Huang J, Smolinski S, Tek V, Vanzin G (2005) Energy generation from the CO oxidation-hydrogen production pathway in Rubrivivax gelatinosus. Appl Environ Microbiol 71:2870–2874

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  74. Goris T et al (2011) A unique iron-sulfur cluster is crucial for oxygen tolerance of a [NiFe]-hydrogenase. Nat Chem Biol 7:310–318

    Article  PubMed  CAS  Google Scholar 

  75. Kanai T, Matsuoka R, Beppu H, Nakajima A, Okada Y, Atomi H, Imanaka T (2011) Distinct physiological roles of the three [NiFe]-hydrogenase orthologs in the hyperthermophilic archaeon Thermococcus kodakarensis. J Bacteriol 193:3109–3116

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  76. Bryant FO, Adams MW (1989) Characterization of hydrogenase from the hyperthermophilic archaebacterium, Pyrococcus furiosus. J Biol Chem 264:5070–5079

    Article  PubMed  CAS  Google Scholar 

  77. Sapra R, Verhagen MF, Adams MW (2000) Purification and characterization of a membrane-bound hydrogenase from the hyperthermophilic archaeon Pyrococcus furiosus. J Bacteriol 182:3423–3428

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  78. Silva PJ, van den Ban EC, Wassink H, Haaker H, de Castro B, Robb FT, Hagen WR (2000) Enzymes of hydrogen metabolism in Pyrococcus furiosus. Eur J Biochem 267:6541–6551

    Article  PubMed  CAS  Google Scholar 

  79. Sapra R, Bagramyan K, Adams MWW (2003) A simple energy-conserving system: proton reduction coupled to proton translocation. Proc Natl Acad Sci USA 100:7545–7550

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  80. McTernan PM et al (2014) Intact functional fourteen-subunit respiratory membrane-bound [NiFe]-hydrogenase complex of the hyperthermophilic archaeon Pyrococcus furiosus. J Biol Chem 289:19364–19372

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  81. Yu H, Wu CH, Schut GJ, Haja DK, Zhao G, Peters JW, Adams MWW, Li H (2018) Structure of an ancient respiratory system. Cell 173(1636–1649):e16

    Google Scholar 

  82. Pisa KY, Huber H, Thomm M, Müller V (2007) A sodium ion-dependent A1AO ATP synthase from the hyperthermophilic archaeon Pyrococcus furiosus. FEBS J 274:3928–3938

    Article  PubMed  CAS  Google Scholar 

  83. Künkel A, Vorholt JA, Thauer RK, Hedderich R (1998) An Escherichia coli hydrogenase-3-type hydrogenase in methanogenic archaea. Eur J Biochem 252:467–476

    Article  PubMed  Google Scholar 

  84. Meuer J, Bartoschek S, Koch J, Künkel A, Hedderich R (1999) Purification and catalytic properties of Ech hydrogenase from Methanosarcina barkeri. Eur J Biochem 265:325–335

    Article  PubMed  CAS  Google Scholar 

  85. Forzi L, Koch J, Guss AM, Radosevich CG, Metcalf WW, Hedderich R (2005) Assignment of the [4Fe–4S] clusters of Ech hydrogenase from Methanosarcina barkeri to individual subunits via the characterization of site-directed mutants. FEBS J 272:4741–4753

    Article  PubMed  CAS  Google Scholar 

  86. Welte C, Krätzer C, Deppenmeier U (2010) Involvement of Ech hydrogenase in energy conservation of Methanosarcina mazei. FEBS J 277:3396–3403

    Article  PubMed  CAS  Google Scholar 

  87. Soboh B, Linder D, Hedderich R (2004) A multisubunit membrane-bound [NiFe] hydrogenase and an NADH-dependent Fe-only hydrogenase in the fermenting bacterium Thermoanaerobacter tengcongensis. Microbiology 150:2451–2463

    Article  PubMed  CAS  Google Scholar 

  88. Rodrigues R, Valente FM, Pereira IAC, Oliveira S, Rodrigues-Pousada C (2003) A novel membrane-bound Ech [NiFe] hydrogenase in Desulfovibrio gigas. Biochem Biophys Res Commun 306:366–375

    Article  PubMed  CAS  Google Scholar 

  89. Heidelberg JF et al (2004) The genome sequence of the anaerobic, sulfate-reducing bacterium Desulfovibrio vulgaris Hildenborough. Nat Biotechnol 22:554–559

    Article  PubMed  CAS  Google Scholar 

  90. Pereira IAC, 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 2:1–22

    Google Scholar 

  91. Pereira PM, He Q, Valente FM, Xavier AV, Zhou J, Pereira IAC, Louro RO (2008) Energy metabolism in Desulfovibrio vulgaris Hildenborough: insights from transcriptome analysis. Antonie Van Leeuwenhoek 93:347–362

    Article  PubMed  CAS  Google Scholar 

  92. Hackmann TJ, Firkins JL (2015) Electron transport phosphorylation in rumen butyrivibrios: unprecedented ATP yield for glucose fermentation to butyrate. Front Microbiol 6:1–11

    Google Scholar 

  93. Porat I et al (2006) Disruption of the operon encoding Ehb hydrogenase limits anabolic CO2 assimilation in the archaeon Methanococcus maripaludis. J Bacteriol 188:1373–1380

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  94. Major TA, Liu Y, Whitman WB (2010) Characterization of energy-conserving hydrogenase B in Methanococcus maripaludis. J Bacteriol 192:4022–4030

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  95. Lie TJ, Costa KC, Lupa B, Korpole S, Whitman WB, Leigh JA (2012) Essential anaplerotic role for the energy-converting hydrogenase Eha in hydrogenotrophic methanogenesis. Proc Natl Acad Sci USA 109:15473–15478

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  96. Bettenbrock K et al (2014) Towards a systems level understanding of the oxygen response of Escherichia coli. Adv Microb Physiol 64:65–114

    Article  PubMed  CAS  Google Scholar 

  97. Doberenz C et al (2014) Pyruvate formate-lyase interacts directly with the formate channel FocA to regulate formate translocation. J Mol Biol 426:2827–2839

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  98. Sawers RG (2005) Formate and its role in hydrogen production in Escherichia coli. Biochem Soc Trans 33:42–46

    Article  PubMed  CAS  Google Scholar 

  99. 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 190:843–850

    Article  PubMed  CAS  Google Scholar 

  100. 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 191:4451–4457

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  101. Schuchmann K, Müller V (2012) A bacterial electron bifurcating hydrogenase. J Biol Chem 287:31165–31171

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  102. Müller V, Chowdhury NP, Basen M (2018) Electron bifurcation: a long-hidden energy-coupling mechanism. Annu Rev Microbiol 72:331–353

    Article  PubMed  CAS  Google Scholar 

  103. Morris BE, Henneberger R, Huber H, Moissl-Eichinger C (2013) Microbial syntrophy: interaction for the common good. FEMS Microbiol Rev 37:384–406

    Article  PubMed  CAS  Google Scholar 

  104. Montag D, Schink B (2018) Formate and hydrogen as electron shuttles in terminal fermentations in an oligotrophic freshwater lake sediment. Appl Environ Microbiol 84:e01572-18

    Article  PubMed  PubMed Central  Google Scholar 

  105. Walker CB et al (2009) The electron transfer system of syntrophically grown Desulfovibrio vulgaris. J Bacteriol 191:5793–5801

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  106. 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 192:674–678

    Article  PubMed  CAS  Google Scholar 

  107. Jackson BE, McInerney MJ (2002) Anaerobic microbial metabolism can proceed close to thermodynamic limits. Nature 415:454–456

    Article  PubMed  CAS  Google Scholar 

  108. Stams AJ, Plugge CM (2009) Electron transfer in syntrophic communities of anaerobic bacteria and archaea. Nat Rev Microbiol 7:568–577

    Article  PubMed  CAS  Google Scholar 

  109. Jung HC, Lee SH, Lee SM, An YJ, Lee JH, Lee HS, Kang SG (2017) Adaptive evolution of a hyperthermophilic archaeon pinpoints a formate transporter as a critical factor for the growth enhancement on formate. Sci Rep 7:1–9

    Article  CAS  Google Scholar 

  110. Schuchmann K, Müller V (2014) Autotrophy at the thermodynamic limit of life: a model for energy conservation in acetogenic bacteria. Nat Rev Microbiol 12:809–821

    Article  PubMed  CAS  Google Scholar 

  111. Biegel E, Müller V (2010) Bacterial Na+-translocating ferredoxin:NAD+ oxidoreductase. Proc Natl Acad Sci USA 107:18138–18142

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  112. 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 68:613–634

    Article  PubMed  CAS  Google Scholar 

  113. Fritz M, Müller V (2007) An intermediate step in the evolution of ATPases -the F1F0-ATPase from Acetobacterium woodii contains F-type and V-type rotor subunits and is capable of ATP synthesis. FEBS J 274:3421–3428

    Article  PubMed  CAS  Google Scholar 

  114. Leigh JA, Mayer F, Wolfe RS (1981) Acetogenium kivui, a new thermophilic hydrogen-oxidizing, acetogenic bacterium. Arch Microbiol 129:275–280

    Article  CAS  Google Scholar 

  115. Basen M, Müller V (2017) “Hot” acetogenesis. Extremophiles 21:15–26

    Article  PubMed  CAS  Google Scholar 

  116. Friedrich T, Scheide D (2000) The respiratory complex I of bacteria, archaea and eukarya and its module common with membrane-bound multisubunit hydrogenases. FEBS Lett 479:1–5

    Article  PubMed  CAS  Google Scholar 

  117. Backiel J, Juárez O, Zagorevski DV, Wang Z, Nilges MJ, Barquera B (2008) Covalent binding of flavins to RnfG and RnfD in the Rnf complex from Vibrio cholerae. Biochemistry 47:11273–11284

    Article  PubMed  CAS  Google Scholar 

  118. Drake HL, Daniel SL (2004) Physiology of the thermophilic acetogen Moorella thermoacetica. Res Microbiol 155:869–883

    Article  PubMed  Google Scholar 

  119. Bertoldo C, Antranikian G (2006) The order thermococcales. In: Dworkin M, Falkow S, Rosenberg E, Schleifer KH, Stackebrandt E (eds) The prokaryotes. Springer Science + Business Media, LLC, New York, pp 69–81

    Chapter  Google Scholar 

  120. Calteau A, Gouy M, Perriere G (2005) Horizontal transfer of two operons coding for hydrogenases between bacteria and archaea. J Mol Evol 60:557–565

    Article  PubMed  CAS  Google Scholar 

  121. Sazanov LA (2015) A giant molecular proton pump: structure and mechanism of respiratory complex I. Nat Rev Mol Cell Biol 16:375–388

    Article  PubMed  CAS  Google Scholar 

  122. Welte C, Deppenmeier U (2014) Bioenergetics and anaerobic respiratory chains of aceticlastic methanogens. Biochim Biophys Acta 1837:1130–1147

    Article  PubMed  CAS  Google Scholar 

  123. Laughlin TG, Bayne AN, Trempe JF, Savage DF, Davies KM (2019) Structure of the complex I-like molecule NDH of oxygenic photosynthesis. Nature 566:411–414

    Article  PubMed  CAS  Google Scholar 

  124. Zickermann V, Wirth C, Nasiri H, Siegmund K, Schwalbe H, Hunte C, Brandt U (2015) Mechanistic insight from the crystal structure of mitochondrial complex I. Science 347:44–49

    Article  PubMed  CAS  Google Scholar 

  125. Baradaran R, Berrisford JM, Minhas GS, Sazanov LA (2013) Crystal structure of the entire respiratory complex I. Nature 494:443–448

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  126. Brandt U (2006) Energy converting NADH:quinone oxidoreductase (complex I). Annu Rev Biochem 75:69–92

    Article  PubMed  CAS  Google Scholar 

  127. Castro PJ, Silva AF, Marreiros BC, Batista AP, Pereira MM (2016) Respiratory complex I: a dual relation with H+ and Na+? Biochim Biophys Acta 1857:928–937

    Article  PubMed  CAS  Google Scholar 

  128. Wikström M (1984) Two protons are pumped from the mitochondrial matrix per electron transferred between NADH and ubiquinone. FEBS Lett 169:300–304

    Article  PubMed  Google Scholar 

  129. Galkin AS, Grivennikova VG, Vinogradov AD (1999) H+/2e stoichiometry in NADH-quinone reductase reactions catalyzed by bovine heart submitochondrial particles. FEBS Lett 451:157–161

    Article  PubMed  CAS  Google Scholar 

  130. Wikström M, Hummer G (2012) Stoichiometry of proton translocation by respiratory complex I and its mechanistic implications. Proc Natl Acad Sci USA 109:4431–4436

    Article  PubMed  PubMed Central  Google Scholar 

  131. Steuber J, Schmid C, Rufibach M, Dimroth P (2000) Na+ translocation by complex I (NADH:quinone oxidoreductase) of Escherichia coli. Mol Microbiol 35:428–434

    Article  PubMed  CAS  Google Scholar 

  132. Gemperli AC, Dimroth P, Steuber J (2003) Sodium ion cycling mediates energy coupling between complex I and ATP synthase. Proc Natl Acad Sci USA 100:839–844

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  133. Krebs W, Steuber J, Gemperli AC, Dimroth P (1999) Na+-translocation by the NADH:ubiquinone oxidoreductase (complex I) from Klebsiella pneumoniae. Mol Microbiol 33:590–598

    Article  PubMed  CAS  Google Scholar 

  134. Stolpe S, Friedrich T (2004) The Escherichia coli NADH:ubiquinone oxidoreductase (complex I) is a primary proton pump but may be capable of secondary sodium antiport. J Biol Chem 279:18377–18383

    Article  PubMed  CAS  Google Scholar 

  135. Batista AP, Fernandes AS, Louro RO, Steuber J, Pereira MM (2010) Energy conservation by Rhodothermus marinus respiratory complex I. Biochim Biophys Acta 1797:509–515

    Article  PubMed  CAS  Google Scholar 

  136. Batista AP, Pereira MM (2011) Sodium influence on energy transduction by complexes I from Escherichia coli and Paracoccus denitrificans. Biochim Biophys Acta 1807:286–292

    Article  PubMed  CAS  Google Scholar 

  137. Batista AP, Marreiros BC, Louro RO, Pereira MM (2012) Study of ion translocation by respiratory complex I. A new insight using 23Na NMR spectroscopy. Biochim Biophys Acta 1817:1810–1816

    Article  PubMed  CAS  Google Scholar 

  138. Markowitz VM et al (2012) IMG: the integrated microbial genomes database and comparative analysis system. Nucleic Acids Res 40:D115–D122

    Article  PubMed  CAS  Google Scholar 

  139. Rieu-Lesme F, Dauga C, Fonty G, Dore J (1998) Isolation from the rumen of a new acetogenic bacterium phylogenetically closely related to Clostridium difficile. Anaerobe 4:89–94

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

Work from the authors’ laboratory was supported by the Deutsche Forschungsgemeinschaft. MCS is a recipient of a fellowship by the Claussen-Simon-Stiftung (DE).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Volker Müller.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Schoelmerich, M.C., Müller, V. Energy-converting hydrogenases: the link between H2 metabolism and energy conservation. Cell. Mol. Life Sci. 77, 1461–1481 (2020). https://doi.org/10.1007/s00018-019-03329-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00018-019-03329-5

Keywords

Navigation