Bioenergetics and anaerobic respiratory chains of aceticlastic methanogens

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1837, Issue 7, 2014, Pages 1130-1147

  Welte, Cornelia ^a,b   Deppenmeier, Uwe ^a  

^a UNIVERSITY OF BONN   (Germany)

^b RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

Author keywords

Anaerobic respiration; Energy conservation; Ion translocation; Methane; Methanogenesis; NADH dehydrogenase

Indexed keywords

ACETIC ACID; ADENOSINE TRIPHOSPHATE; COENZYME B; DISULFIDE; FERREDOXIN; FOSSIL FUEL; HYDROGEN; HYDROGENASE; MESNA; QUINONE DERIVATIVE; THIOREDOXIN REDUCTASE; UNCLASSIFIED DRUG;

ACETICLASTIC METHANOGEN; ANAEROBIC METABOLISM; BACTERIAL GROWTH; BIOENERGY; BIOFUEL PRODUCTION; CHEMICAL REACTION; COENZYME; ELECTRON TRANSPORT; ENERGY CONVERSION; ENZYME STRUCTURE; MEMBRANE BINDING; METHANOGEN; METHANOGENESIS; METHANOSAETA; METHANOSARCINA; MICROBIAL RESPIRATION; NONHUMAN; OXIDATION; PRIORITY JOURNAL; RESPIRATORY CHAIN; REVIEW; THERMODYNAMICS;

METHANOSAETA; METHANOSARCINA;

ANAEROBIC RESPIRATION; ENERGY CONSERVATION; ION TRANSLOCATION; METHANE; METHANOGENESIS; NADH DEHYDROGENASE;

ACETATES; AMINO ACID SEQUENCE; ANAEROBIOSIS; ARCHAEAL PROTEINS; ENERGY METABOLISM; METHANE; METHANOSARCINA; MOLECULAR SEQUENCE DATA; NADH DEHYDROGENASE;

EID: 84901851838     PISSN: 00052728     EISSN: 18792650     Source Type: Journal    
DOI: 10.1016/j.bbabio.2013.12.002     Document Type: Review

References (204)

1. J.G. Ferry Fundamentals of methanogenic pathways that are key to the biomethanation of complex biomass Curr. Opin. Biotechnol. 22 2011 351 357
2. M. Morita, and K. Sasaki Factors influencing the degradation of garbage in methanogenic bioreactors and impacts on biogas formation Appl. Microbiol. Biotechnol. 94 2012 575 582
3. J.L. Garcia, B.K. Patel, and B. Ollivier Taxonomic, phylogenetic, and ecological diversity of methanogenic archaea Anaerobe 6 2000 205 226 (Pubitemid 30604012)
4. B. Schink Energetics of syntrophic cooperation in methanogenic degradation Microbiol. Mol. Biol. Rev. 61 1997 262 280 (Pubitemid 27283803)
5. M.J. McInerney, J.R. Sieber, and R.P. Gunsalus Syntrophy in anaerobic global carbon cycles Curr. Opin. Biotechnol. 20 2009 623 632
6. A.J. Stams, and C.M. Plugge Electron transfer in syntrophic communities of anaerobic bacteria and archaea Nat. Rev. Microbiol. 7 2009 568 577
7. U. Deppenmeier The unique biochemistry of methanogenesis Prog. Nucleic Acid Res. Mol. Biol. 71 2002 223 283
8. 2 storage Ann. Rev. Biochem. 79 2010 507 536
9. Y. Liu, and W.B. Whitman Metabolic, phylogenetic, and ecological diversity of the methanogenic archaea Ann. N. Y. Acad. Sci. 1125 2008 171 189 (Pubitemid 351451164)
10. J.R. Marchesi, A.J. Weightman, B.A. Cragg, R.J. Parkes, and J.C. Fry Methanogen and bacterial diversity and distribution in deep gas hydrate sediments from the Cascadia Margin as revealed by 16S rRNA molecular analysis FEMS Microbiol. Ecol. 34 2001 221 228
11. W.J. Winters, S.R. Dallimore, T.S. Collett, K.A. Jenner, J.T. Katsube, R.E. Cranston, J.F. Wright, F.M. Nixon, and T. Uchida Relation between gas hydrate and physical properties at the Mallik 2 L-38 research well in the Mackenzie Delta Ann. N. Y. Acad. Sci. 912 2000 94 100 (Pubitemid 30465674)
12. C.D. Ruppel Methane hydrates and contemporary climate change Nat. Educ. Knowl. 3 2011 29
13. C. Welte, and U. Deppenmeier Blackbox für Biogas LaborPraxis 37 2013 14 16
14. K. Paul, J.O. Nonoh, L. Mikulski, and A. Brune "Methanoplasmatales, " Thermoplasmatales-related archaea in termite guts and other environments, are the seventh order of methanogens Appl. Environ. Microbiol. 78 2012 8245 8253
15. S.H. Zinder Physiological ecology of methanogens J.G. Ferry, Methanogenesis 1993 Chapman & Hall New York-London 128 206
16. + translocating ferredoxin oxidation Biochim. Biophys. Acta 1827 2013 94 113
17. J.G. Ferry Enzymology of one-carbon metabolism in methanogenic pathways FEMS Microbiol. Rev. 23 1999 13 38 (Pubitemid 29094690)
18. R.K. Thauer Biochemistry of methanogenesis: a tribute to Marjory Stephenson Microbiology 144 1998 2377 2406
19. U. Deppenmeier Redox-driven proton translocation in methanogenic archaea Cell. Mol. Life Sci. 59 2002 1513 1533 (Pubitemid 35239307)
20. J.G. Ferry How to make a living by exhaling methane Ann. Rev. Microbiol. 64 2010 453 473
21. D.R. Boone, W.B. Whitman, and P.E. Rouvière Diversity and taxonomy of methanogens J.G. Ferry, Methanogenesis 1993 Chapman & Hall New York 35 80
22. L.E. Mayerhofer, A.J. Macario, and E.C. de Macario Lamina, a novel multicellular form of Methanosarcina mazei S-6 J. Bacteriol. 174 1992 309 314
23. U. Deppenmeier, A. Johann, T. Hartsch, R. Merkl, R.A. Schmitz, R. Martinez-Arias, A. Henne, A. Wiezer, S. Bäumer, C. Jacobi, H. Brüggemann, T. Lienard, A. Christmann, M. Bomeke, S. Steckel, A. Bhattacharyya, A. Lykidis, R. Overbeek, H.P. Klenk, R.P. Gunsalus, H.J. Fritz, and G. Gottschalk The genome of Methanosarcina mazei: evidence for lateral gene transfer between bacteria and archaea J. Mol. Microbiol. Biotechnol. 4 2002 453 461 (Pubitemid 34784706)
24. J.E. Galagan, C. Nusbaum, A. Roy, M.G. Endrizzi, P. Macdonald, W. FitzHugh, S. Calvo, R. Engels, S. Smirnov, D. Atnoor, A. Brown, N. Allen, J. Naylor, N. Stange-Thomann, K. DeArellano, R. Johnson, L. Linton, P. McEwan, K. McKernan, J. Talamas, A. Tirrell, W. Ye, A. Zimmer, R.D. Barber, I. Cann, D.E. Graham, D.A. Grahame, A.M. Guss, R. Hedderich, C. Ingram-Smith, H.C. Kuettner, J.A. Krzycki, J.A. Leigh, W. Li, J. Liu, B. Mukhopadhyay, J.N. Reeve, K. Smith, T.A. Springer, L.A. Umayam, O. White, R.H. White, E. Conway de Macario, J.G. Ferry, K.F. Jarrell, H. Jing, A.J. Macario, I. Paulsen, M. Pritchett, K.R. Sowers, R.V. Swanson, S.H. Zinder, E. Lander, W.W. Metcalf, and B. Birren The genome of M. acetivorans reveals extensive metabolic and physiological diversity Genome Res. 12 2002 532 542 (Pubitemid 34308633)
25. D.L. Maeder, I. Anderson, T.S. Brettin, D.C. Bruce, P. Gilna, C.S. Han, A. Lapidus, W.W. Metcalf, E. Saunders, R. Tapia, and K.R. Sowers The Methanosarcina barkeri genome: comparative analysis with Methanosarcina acetivorans and Methanosarcina mazei reveals extensive rearrangement within methanosarcinal genomes J. Bacteriol. 188 2006 7922 7931 (Pubitemid 44764528)
26. S. Nelson-Sathi, T. Dagan, G. Landan, A. Janssen, M. Steel, J.O. McInerney, U. Deppenmeier, and W.F. Martin Acquisition of 1,000 eubacterial genes physiologically transformed a methanogen at the origin of Haloarchaea Proc. Natl. Acad. Sci. U. S. A. 109 2012 20537 20542
27. B.A. Huser, K. Wuhrmann, and A.J.B. Zehnder Methanothrix soehngenii gen. nov. sp. nov., a new acetotrophic non-hydrogen-oxidizing methane bacterium Arch. Microbiol. 132 1982 1 9 (Pubitemid 12008588)
28. S. Berger, C. Welte, and U. Deppenmeier Acetate activation in Methanosaeta thermophila: characterization of the key enzymes pyrophosphatase and acetyl-CoA synthetase Archaea 2012 2012 315153
29. M.S.M. Jetten, A.J.M. Stams, and A.J.B. Zehnder Methanogenesis from acetate - a comparison of the acetate metabolism in Methanothrix soehngenii and Methanosarcina spp. FEMS Microbiol. Rev. 88 1992 181 197
30. K.S. Smith, and C. Ingram-Smith Methanosaeta, the forgotten methanogen? Trends Microbiol. 15 2007 150 155 (Pubitemid 46528250)
31. J. Zhu, H. Zheng, G. Ai, G. Zhang, D. Liu, X. Liu, and X. Dong The genome characteristics and predicted function of methyl-group oxidation pathway in the obligate aceticlastic methanogens, Methanosaeta spp. PloS ONE 7 2012 e36756
32. R.D. Barber, L. Zhang, M. Harnack, M.V. Olson, R. Kaul, C. Ingram-Smith, and K.S. Smith Complete genome sequence of Methanosaeta concilii, a specialist in aceticlastic methanogenesis J. Bacteriol. 193 2011 3668 3669
33. C. Welte, and U. Deppenmeier Membrane-bound electron transport in Methanosaeta thermophila J. Bacteriol. 193 2011 2868 2870
34. R.K. Thauer, A.K. Kaster, H. Seedorf, W. Buckel, and R. Hedderich Methanogenic archaea: ecologically relevant differences in energy conservation Nat. Rev. Microbiol. 6 2008 579 591
35. U. Deppenmeier, and V. Müller Life close to the thermodynamic limit: how methanogenic archaea conserve energy Results Probl. Cell Differ. 45 2008 123 152
36. M.A. Gaston, R. Jiang, and J.A. Krzycki Functional context, biosynthesis, and genetic encoding of pyrrolysine Curr. Opin. Microbiol. 14 2011 342 349
37. R.S. Wolfe Unusual coenzymes of methanogenesis Trends Biochem. Sci. 10 1985 396 399 (Pubitemid 16228220)
38. 430 and of its enzyme, methyl coenzyme M reductase FEMS Microbiol. Rev. 7 1990 339 348
39. U. Ermler n the mechanism of methyl-coenzyme M reductase Dalton Trans. 2005 3451 3458
40. U. Ermler, W. Grabarse, S. Shima, M. Goubeaud, and R.K. Thauer Crystal structure of methyl-coenzyme M reductase: the key enzyme of biological methane formation Science 278 1997 1457 1462 (Pubitemid 27509817)
41. 430 from methanogenic bacteria - structure of the protein-free factor Helv. Chim. Acta 67 1984 334 351
42. R.K. Thauer Enzymology - nickel to the fore Science 293 2001 1264 1265
43. C. Walsh Naturally occurring 5-deazaflavin coenzymes - biological redox roles Acc. Chem. Res. 19 1986 216 221
44. K.M. Noll, K.L. Rinehart, R.S. Tanner, and R.S. Wolfe Structure of component-B (7-mercaptoheptanoylthreonine phosphate) of the methylcoenzyme M methylreductase system of Methanobacterium thermoautotrophicum Proc. Natl. Acad. Sci. U. S. A. 83 1986 4238 4242 (Pubitemid 16057027)
45. A. Kobelt, A. Pfaltz, D. Ankelfuchs, and R.K. Thauer The L-form of N-7-mercaptoheptanoyl-O-phosphothreonine is the enantiomer active as component B in methyl-CoM reduction to methane FEBS Lett. 214 1987 265 268
46. 2 dehydrogenase from Methanosarcina mazei is a redox-driven proton pump closely related to NADH dehydrogenases J. Biol. Chem. 275 2000 17968 17973 (Pubitemid 30414741)
47. U. Beifuss, M. Tietze, S. Bäumer, and U. Deppenmeier Methanophenazine: structure, total synthesis, and function of a new cofactor from methanogenic archaea Angew. Chem. Int. Ed. Engl. 39 2000 2470 2472 (Pubitemid 30602514)
48. M. Tietze, A. Beuchle, I. Lamla, N. Orth, M. Dehler, G. Greiner, and U. Beifuss Redox potentials of methanophenazine and CoB-S-S-CoM, factors involved in electron transport in methanogenic archaea Chembiochem 4 2003 333 335 (Pubitemid 36505202)
49. J.G. Ferry Enzymology of the fermentation of acetate to methane by Methanosarcina thermophila Biofactors 6 1997 25 35 (Pubitemid 27287121)
50. M.S. Jetten, T.J. Fluit, A.J. Stams, and A.J. Zehnder A fluoride-insensitive inorganic pyrophosphatase isolated from Methanothrix soehngenii Arch. Microbiol. 157 1992 284 289
51. M.S. Jetten, A.J. Stams, and A.J. Zehnder Isolation and characterization of acetyl-coenzyme A synthetase from Methanothrix soehngenii J. Bacteriol. 171 1989 5430 5435 (Pubitemid 19252427)
52. Y.L. Teh, and S. Zinder Acetyl-coenzyme A synthetase in the thermophilic, acetate-utilizing methanogen Methanothrix sp. strain CALS-1 FEMS Microbiol. Lett. 98 1992 1 8
53. R.D. Miles, P.P. Iyer, and J.G. Ferry Site-directed mutational analysis of active site residues in the acetate kinase from Methanosarcina thermophila J. Biol. Chem. 276 2001 45059 45064
54. K.C. Terlesky, M.J.K. Nelson, and J.G. Ferry Isolation of an enzyme complex with carbon monoxide dehydrogenase activity containing corrinoid and nickel from acetate-grown Methanosarcina thermophila J. Bacteriol. 168 1986 1053 1058 (Pubitemid 17226782)
55. D.A. Grahame Catalysis of acetyl-CoA cleavage and tetrahydrosarcinapterin methylation by a carbon monoxide dehydrogenase corrinoid enzyme complex J. Biol. Chem. 266 1991 22227 22233 (Pubitemid 21908639)
56. J.G. Ferry CO dehydrogenase Ann. Rev. Microbiol. 49 1995 305 333
57. E. Oelgeschläger, and M. Rother Carbon monoxide-dependent energy metabolism in anaerobic bacteria and archaea Arch. Microbiol. 190 2008 257 269
58. W. Gong, B. Hao, Z. Wei, D.J. Ferguson, T. Tallant, J.A. Krzycki, and M.K. Chan Structure of the alpha(2)epsilon(2) Ni-dependent CO dehydrogenase component of the Methanosarcina barkeri acetyl-CoA decarbonylase/synthase complex Proc. Natl. Acad. Sci. U. S. A. 105 2008 9558 9563 (Pubitemid 352031340)
59. +-translocating methyltransferase complex from methanogenic archaea Biochim. Biophys. Acta 1505 2001 28 36 (Pubitemid 32204456)
60. V. Müller, C. Winner, and G. Gottschalk Electron transport driven sodium extrusion during methanogenesis from formaldehyde and molecular hydrogen by Methanosarcina barkeri Eur. J. Biochem. 178 1988 519 525
61. +-translocating membrane protein J. Bacteriol. 174 1992 7656 7660
62. T.A. Bobik, K.D. Olson, K.M. Noll, and R.S. Wolfe Evidence that the heterodisulfide of coenzyme M and 7-mercaptoheptanoylthreonine phosphate is a product of the methylreductase reaction in Methanobacterium Biochem. Biophys. Res. Commun. 149 1987 455 460 (Pubitemid 18023001)
63. J. Ellermann, R. Hedderich, R. Böcher, and R.K. Thauer The final step in methane formation. Investigations with highly purified methyl-CoM reductase (component C) from Methanobacterium thermoautotrophicum (strain Marburg) Eur. J. Biochem. 172 1988 669 677
64. J.A. Krzycki Function of genetically encoded pyrrolysine in corrinoid-dependent methylamine methyltransferases Curr. Opin. Chem. Biol. 8 2004 484 491 (Pubitemid 39278344)
65. P.A. Bertram, and R.K. Thauer Thermodynamics of the formylmethanofuran dehydrogenase reaction in Methanobacterium thermoautotrophicum Eur. J. Biochem. 226 1994 811 818
66. R. Michel, C. Massanz, S. Kostka, M. Richter, and K. Fiebig Biochemical characterization of the 8-hydroxy-5-deazaflavin-reactive hydrogenase from Methanosarcina barkeri Fusaro Eur. J. Biochem. 233 1995 727 735
67. F. Li, J. Hinderberger, H. Seedorf, J. Zhang, W. Buckel, and R.K. Thauer Coupled ferredoxin and crotonyl coenzyme A (CoA) reduction with NADH catalyzed by the butyryl-CoA dehydrogenase/Etf complex from Clostridium kluyveri J. Bacteriol. 190 2008 843 850 (Pubitemid 351170927)
68. A.K. Kaster, J. Moll, K. Parey, and R.K. Thauer Coupling of ferredoxin and heterodisulfide reduction via electron bifurcation in hydrogenotrophic methanogenic archaea Proc. Natl. Acad. Sci. U. S. A. 108 2011 2981 2986
69. K.C. Costa, P.M. Wong, T. Wang, T.J. Lie, J.A. Dodsworth, I. Swanson, J.A. Burn, M. Hackett, and J.A. Leigh Protein complexing in a methanogen suggests electron bifurcation and electron delivery from formate to heterodisulfide reductase Proc. Natl. Acad. Sci. U. S. A. 107 2010 11050 11055
70. 2 or formate to heterodisulfide reductase in Methanococcus maripaludis J. Bacteriol. 195 2013 5160 5165
71. 5-methyltetrahydromethanopterin: coenzyme M methyltransferase from Methanosarcina mazei Gö1 reconstituted in ether lipid liposomes Eur. J. Biochem. 239 1996 857 864 (Pubitemid 26253064)
72. + bioenergetics in methanogenic archaea Biochem. Soc. Trans. 41 2013 421 426
73. J.G. Ferry The chemical biology of methanogenesis Planet. Space Sci. 58 2010 1775 1783
74. V. Müller, T. Lemker, A. Lingl, C. Weidner, U. Coskun, and G. Grüber Bioenergetics of archaea: ATP synthesis under harsh environmental conditions J. Mol. Microbiol. Biotechnol. 10 2005 167 180 (Pubitemid 43800691)
75. V. Müller, and G. Grüber ATP synthases: structure, function and evolution of unique energy converters Cell. Mol. Life Sci. 60 2003 474 494 (Pubitemid 36459527)
76. +/ATP coupling ratio FEBS Lett. 576 2004 1 4 (Pubitemid 39330446)
77. V. Müller, A. Lingl, K. Lewalter, and M. Fritz ATP synthases with novel rotor subunits: new insights into structure, function and evolution of ATPases J. Bioenerg. Biomembr. 37 2005 455 460 (Pubitemid 43725176)
78. + translocation Proc. Natl. Acad. Sci. U. S. A. 109 2012 947 952
79. R. Jasso-Chavez, E.E. Apolinario, K.R. Sowers, and J.G. Ferry MrpA functions in energy conversion during acetate-dependent growth of Methanosarcina acetivorans J. Bacteriol. 195 2013 3987 3994
80. M. Blaut, and G. Gottschalk Coupling of ATP synthesis and methane formation from methanol and molecular hydrogen in Methanosarcina barkeri Eur. J. Biochem. 141 1984 217 222
81. S. Peinemann Kopplung von ATP-Synthese und Methanogenese in Vesikelpräparationen des methanogenen Bakteriums Stamm Gö1 [PhD thesis] 1989 Georg-August-Universität Göttingen Germany
82. + in Methanosarcina barkeri Eur. J. Biochem. 162 1987 461 466 (Pubitemid 17003750)
83. 2: heterodisulfide oxidoreductase, a 2nd energy-conserving system in the methanogenic strain Gö1 Arch. Microbiol. 155 1991 272 277
84. 2:heterodisulfide oxidoreductase from Methanosarcina mazei Gö1: identification of two proton-translocating segments J. Bacteriol. 181 1999 4076 4080 (Pubitemid 29295927)
85. 420: heterodisulfide oxidoreductase, a proton- translocating redox system in methanogenic bacteria Proc. Natl. Acad. Sci. U. S. A. 87 1990 9449 9453 (Pubitemid 120030644)
86. 420 dehydrogenase in electron transport in Methanosarcina mazei FEBS J. 278 2011 1277 1287
87. G. Kulkarni, D.M. Kridelbaugh, A.M. Guss, and W.W. Metcalf Hydrogen is a preferred intermediate in the energy-conserving electron transport chain of Methanosarcina barkeri Proc. Natl. Acad. Sci. U. S. A. 106 2009 15915 15920
88. F.M. Harald The Vital Force: A Study of Bioenergetics 1986 W.H. Freeman and Company New York
89. R.K. Thauer, and S. Shima Methane as fuel for anaerobic microorganisms Ann. N. Y. Acad. Sci. 1125 2008 158 170 (Pubitemid 351451146)
90. J.A. Vorholt, M. Vaupel, and R.K. Thauer A polyferredoxin with eight [4Fe-4S] clusters as a subunit of molybdenum formylmethanofuran dehydrogenase from Methanosarcina barkeri Eur. J. Biochem. 236 1996 309 317 (Pubitemid 26075661)
91. R. Fischer, and R.K. Thauer Ferredoxin-dependent methane formation from acetate in cell extracts of Methanosarcina barkeri (strain MS) FEBS Lett. 269 1990 368 372 (Pubitemid 20273828)
92. J. Meuer, H.C. Kuettner, J.K. Zhang, R. Hedderich, and W.W. Metcalf 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. U. S. A. 99 2002 5632 5637 (Pubitemid 34411601)
93. J. Meuer, S. Bartoschek, J. Koch, A. Künkel, and R. Hedderich Purification and catalytic properties of Ech hydrogenase from Methanosarcina barkeri Eur. J. Biochem. 265 1999 325 335 (Pubitemid 29466042)
94. C. Welte, V. Kallnik, M. Grapp, G. Bender, S. Ragsdale, and U. Deppenmeier Function of Ech hydrogenase in ferredoxin-dependent, membrane-bound electron transport in Methanosarcina mazei J. Bacteriol. 192 2010 674 678
95. C. Welte, C. Krätzer, and U. Deppenmeier Involvement of Ech hydrogenase in energy conservation of Methanosarcina mazei FEBS J. 277 2010 3396 3403
96. M. Wang, J.F. Tomb, and J.G. Ferry Electron transport in acetate-grown Methanosarcina acetivorans BMC Microbiol. 11 2011 165
97. K. Schlegel, C. Welte, U. Deppenmeier, and V. Müller Electron transport during aceticlastic methanogenesis by Methanosarcina acetivorans involves a sodium-translocating Rnf complex FEBS J. 279 2012 4444 4452
98. 2 in Methanosarcina barkeri Eur. J. Biochem. 179 1989 469 472
99. A. Tersteegen, and R. Hedderich Methanobacterium thermoautotrophicum encodes two multisubunit membrane-bound [NiFe] hydrogenases. Transcription of the operons and sequence analysis of the deduced proteins Eur. J. Biochem. 264 1999 930 943 (Pubitemid 29437225)
100. D.A. Grahame, and E. DeMoll Substrate and accessory protein requirements and thermodynamics of acetyl-CoA synthesis and cleavage in Methanosarcina barkeri Biochemistry 34 1995 4617 4624
101. A.K. Bock, J. Kunow, J. Glasemacher, and P. Schönheit Catalytic properties, molecular composition and sequence alignments of pyruvate:ferredoxin oxidoreductase from the methanogenic archaeon Methanosarcina barkeri (strain Fusaro) Eur. J. Biochem. 237 1996 35 44 (Pubitemid 26110271)
102. 2 activation J. Mol. Microbiol. Biotechnol. 10 2005 92 104 (Pubitemid 43800685)
103. J.G. Ferry, and D.J. Lessner Methanogenesis in marine sediments Ann. N. Y. Acad. Sci. 1125 2008 147 157 (Pubitemid 351451153)
104. 2 metabolism between closely related species Mol. Microbiol. 55 2005 1671 1680 (Pubitemid 40445205)
105. Q. Li, L. Li, T. Rejtar, D.J. Lessner, B.L. Karger, and J.G. Ferry Electron transport in the pathway of acetate conversion to methane in the marine archaeon Methanosarcina acetivorans J. Bacteriol. 188 2006 702 710 (Pubitemid 43100558)
106. A.M. Guss, G. Kulkarni, and W.W. Metcalf Differences in hydrogenase gene expression between Methanosarcina acetivorans and Methanosarcina barkeri J. Bacteriol. 191 2009 2826 2833
107. L. Rohlin, and R.P. Gunsalus Carbon-dependent control of electron transfer and central carbon pathway genes for methane biosynthesis in the Archaean, Methanosarcina acetivorans strain C2A BMC Microbiol. 10 2010 62
108. + oxidoreductase Proc. Natl. Acad. Sci. U. S. A. 107 2010 18138 18142
109. + and is reversibly coupled to the membrane potential J. Biol. Chem. 288 2013 [31496-13502]
110. P.M. Vignais, and B. Billoud Occurrence, classification, and biological function of hydrogenases: an overview Chem. Rev. 107 2007 4206 4272 (Pubitemid 350041744)
111. J.C. Fontecilla-Camps, P. Amara, C. Cavazza, Y. Nicolet, and A. Volbeda Structure-function relationships of anaerobic gas-processing metalloenzymes Nature 460 2009 814 822
112. J.C. Fontecilla-Camps, A. Volbeda, C. Cavazza, and Y. Nicolet Structure/function relationships of [NiFe]- and [FeFe]-hydrogenases Chem. Rev. 107 2007 4273 4303 (Pubitemid 350041745)
113. A. Volbeda, M.H. Charon, C. Piras, E.C. Hatchikian, M. Frey, and J.C. Fontecilla-Camps Crystal structure of the nickel-iron hydrogenase from Desulfovibrio gigas Nature 373 1995 580 587
114. 420-reducing hydrogenases in Methanosarcina barkeri Arch. Microbiol. 169 1998 201 205 (Pubitemid 28098690)
115. 420-nonreactive, membrane-bound hydrogenase from Methanosarcina strain Gö1 Arch. Microbiol. 157 1992 505 511
116. J.M. Kemner, and J.G. Zeikus Purification and characterization of membrane-bound hydrogenase from Methanosarcina barkeri MS Arch. Microbiol. 161 1994 47 54 (Pubitemid 24003531)
117. U. Deppenmeier Different structure and expression of the operons encoding the membrane-bound hydrogenases from Methanosarcina mazei Gö1 Arch. Microbiol. 164 1995 370 376
118. B. Kamlage, and M. Blaut Characterization of cytochromes from Methanosarcina strain Gö1 and their involvement in electron transport during growth on methanol J. Bacteriol. 174 1992 3921 3927
119. J.M. Kemner, J.A. Krzycki, R.C. Prince, and J.G. Zeikus Spectroscopic and enzymatic evidence for membrane-bound electron transport carriers and hydrogenase and their relation to cytochrome b function in Methanosarcina barkeri FEMS Microbiol. Lett. 48 1987 267 272
120. J. Brodersen, S. Bäumer, H.J. Abken, G. Gottschalk, and U. Deppenmeier Inhibition of membrane-bound electron transport of the methanogenic archaeon Methanosarcina mazei Gö1 by diphenyleneiodonium Eur. J. Biochem. 259 1999 218 224 (Pubitemid 29030839)
121. K. Eismann, K. Mlejnek, D. Zipprich, M. Hoppert, H. Gerberding, and F. Mayer Antigenic determinants of the membrane-bound hydrogenase in Alcaligenes eutrophus are exposed toward the periplasm J. Bacteriol. 177 1995 6309 6312
122. P.M. Vignais, B. Billoud, and J. Meyer Classification and phylogeny of hydrogenases FEMS Microbiol. Rev. 25 2001 455 501 (Pubitemid 32778469)
123. F.L. Sousa, T. Thiergart, G. Landan, S. Nelson-Sathi, I.A. Pereira, J.F. Allen, N. Lane, and W.F. Martin Early bioenergetic evolution Philos. Trans. R. Soc. Lond. B Biol. Sci. 368 2013 20130088
124. J.D. Fox, R.L. Kerby, G.P. Roberts, and P.W. Ludden Characterization of the CO-induced, CO-tolerant hydrogenase from Rhodospirillum rubrum and the gene encoding the large subunit of the enzyme J. Bacteriol. 178 1996 1515 1524 (Pubitemid 26085598)
125. 2-evolving enzyme complex from Carboxydothermus hydrogenoformans Eur. J. Biochem. 269 2002 5712 5721 (Pubitemid 35365560)
126. R. Böhm, M. Sauter, and A. Böck Nucleotide sequence and expression of an operon in Escherichia coli coding for formate hydrogenlyase components Mol. Microbiol. 4 1990 231 243
127. M. Sauter, R. Böhm, and A. Böck Mutational analysis of the operon hyc determining hydrogenase 3 formation in Escherichia coli Mol. Microbiol. 6 1992 1523 1532
128. R. Sapra, K. Bagramyan, and M.W. Adams A simple energy-conserving system: proton reduction coupled to proton translocation Proc. Natl. Acad. Sci. U. S. A. 100 2003 7545 7550 (Pubitemid 36760006)
129. R. Hovey, S. Lentes, A. Ehrenreich, K. Salmon, K. Saba, G. Gottschalk, R.P. Gunsalus, and U. Deppenmeier DNA microarray analysis of Methanosarcina mazei Gö1 reveals adaptation to different methanogenic substrates Mol. Genet. Genomics 273 2005 225 239 (Pubitemid 40768510)
130. S. Kurkin, J. Meuer, J. Koch, R. Hedderich, and S.P. Albracht The membrane-bound [NiFe]-hydrogenase (Ech) from Methanosarcina barkeri: unusual properties of the iron-sulphur clusters Eur. J. Biochem. 269 2002 6101 6111 (Pubitemid 35461822)
131. L. Forzi, J. Koch, A.M. Guss, C.G. Radosevich, W.W. Metcalf, and R. Hedderich 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 2005 4741 4753 (Pubitemid 41366996)
132. A. Künkel, J.A. Vorholt, R.K. Thauer, and R. Hedderich An Escherichia coli hydrogenase-3-type hydrogenase in methanogenic archaea Eur. J. Biochem. 252 1998 467 476 (Pubitemid 28156870)
133. R. Hedderich Energy-converting [NiFe] hydrogenases from archaea and extremophiles: ancestors of complex I J. Bioenerg. Biomembr. 36 2004 65 75 (Pubitemid 38500761)
134. 2 with the phosphorylation of ADP in acetate-grown Methanosarcina barkeri Eur. J. Biochem. 159 1986 393 398
135. 2 reduction to the level of formylmethanofuran in Methanosarcina barkeri is non-energy driven when CO is the electron donor FEMS Microbiol. Lett. 235 2004 163 167 (Pubitemid 38668652)
136. R.G. Efremov, and L.A. Sazanov The coupling mechanism of respiratory complex I - a structural and evolutionary perspective Biochim. Biophys. Acta 1817 2012 1785 1795
137. T. Friedrich, and H. Weiss Modular evolution of the respiratory NADH:ubiquinone oxidoreductase and the origin of its modules J. Theor. Biol. 187 1997 529 540
138. V.K. Moparthi, and C. Hägerhäll The evolution of respiratory chain complex I from a smaller last common ancestor consisting of 11 protein subunits J. Mol. Evol. 72 2011 484 497
139. B.C. Marreiros, A.P. Batista, A.M. Duarte, and M.M. Pereira A missing link between complex I and group 4 membrane-bound [NiFe] hydrogenases Biochim. Biophys. Acta 1827 2013 198 209
140. R.G. Efremov, R. Baradaran, and L.A. Sazanov The architecture of respiratory complex I Nature 465 2010 441 445
141. R.G. Efremov, and L.A. Sazanov Structure of the membrane domain of respiratory complex I Nature 476 2011 414 420
142. R. Baradaran, J.M. Berrisford, G.S. Minhas, and L.A. Sazanov Crystal structure of the entire respiratory complex I Nature 494 2013 443 448
143. N. Kashani-Poor, K. Zwicker, S. Kerscher, and U. Brandt A central functional role for the 49-kDa subunit within the catalytic core of mitochondrial complex I J. Biol. Chem. 276 2001 24082 24087
144. J.M. Berrisford, and L.A. Sazanov Structural basis for the mechanism of respiratory complex I J. Biol. Chem. 284 2009 29773 29783
145. H. Ogata, W. Lubitz, and Y. Higuchi [NiFe] hydrogenases: structural and spectroscopic studies of the reaction mechanism Dalton Trans. 2009 7577 7587
146. M. Finel Does NADH play a central role in energy metabolism in Helicobacter pylori? Trends Biochem. Sci. 23 1998 412 413
147. M. Schmehl, A. Jahn, A. Meyer zu Vilsendorf, S. Hennecke, B. Masepohl, M. Schuppler, M. Marxer, J. Oelze, and W. Klipp 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 1993 602 615 (Pubitemid 24003880)
148. F. Imkamp, E. Biegel, E. Jayamani, W. Buckel, and V. Müller Dissection of the caffeate respiratory chain in the acetogen Acetobacterium woodii: identification of an Rnf-type NADH dehydrogenase as a potential coupling site J. Bacteriol. 189 2007 8145 8153 (Pubitemid 350178926)
149. E. Biegel, S. Schmidt, and V. Müller Genetic, immunological and biochemical evidence for a Rnf complex in the acetogen Acetobacterium woodii Environ. Microbiol. 11 2009 1438 1443
150. +-oxidoreductase (Rnf) in Acetobacterium woodii: a novel potential coupling site in acetogens Ann. N. Y. Acad. Sci. 1125 2008 137 146 (Pubitemid 351451157)
151. + oxidoreductase essential for autotrophic growth mBio 4 2012 e00406 e00412
152. H. Seedorf, W.F. Fricke, B. Veith, H. Brüggemann, H. Liesegang, A. Strittmatter, M. Miethke, W. Buckel, J. Hinderberger, F. Li, C. Hagemeier, R.K. Thauer, and G. Gottschalk The genome of Clostridium kluyveri, a strict anaerobe with unique metabolic features Proc. Natl. Acad. Sci. U. S. A. 105 2008 2128 2133 (Pubitemid 351439476)
153. P. Worm, A.J. Stams, X. Cheng, and C.M. Plugge Growth- and substrate-dependent transcription of formate dehydrogenase and hydrogenase coding genes in Syntrophobacter fumaroxidans and Methanospirillum hungatei Microbiology 157 2011 280 289
154. I.A. Pereira, A.R. Ramos, F. Grein, M.C. Marques, S.M. da Silva, and S.S. Venceslau A comparative genomic analysis of energy metabolism in sulfate reducing bacteria and archaea Front. Microbiol. 2 2011 69
155. E. Biegel, S. Schmidt, J.M. Gonzalez, and V. Müller Biochemistry evolution and physiological function of the Rnf complex, a novel ion-motive electron transport complex in prokaryotes Cell. Mol. Life Sci. 68 2011 613 634
156. M.J. McInerney, L. Rohlin, H. Mouttaki, U. Kim, R.S. Krupp, L. Rios-Hernandez, J. Sieber, C.G. Struchtemeyer, A. Bhattacharyya, J.W. Campbell, and R.P. Gunsalus The genome of Syntrophus aciditrophicus: life at the thermodynamic limit of microbial growth Proc. Natl. Acad. Sci. U. S. A. 104 2007 7600 7605 (Pubitemid 47185952)
157. H. Kumagai, T. Fujiwara, H. Matsubara, and K. Saeki Membrane localization, topology, and mutual stabilization of the rnfABC gene products in Rhodobacter capsulatus and implications for a new family of energy-coupling NADH oxidoreductases Biochemistry 36 1997 5509 55021
158. + translocation by bacterial NADH:quinone oxidoreductases: an extension to the complex-I family of primary redox pumps Biochim. Biophys. Acta 1505 2001 45 56 (Pubitemid 32204458)
159. A. Saaf, M. Johansson, E. Wallin, and G. von Heijne Divergent evolution of membrane protein topology: the Escherichia coli RnfA and RnfE homologues Proc. Natl. Acad. Sci. U. S. A. 96 1999 8540 8544 (Pubitemid 29354827)
160. J. Backiel, O. Juárez, D.V. Zagorevski, Z. Wang, M.J. Nilges, and B. Barquera Covalent binding of flavins to RnfG and RnfD in the Rnf complex from Vibrio cholerae Biochemistry 47 2008 11273 11284
161. M. Punta, P.C. Coggill, R.Y. Eberhardt, J. Mistry, J. Tate, C. Boursnell, N. Pang, K. Forslund, G. Ceric, J. Clements, A. Heger, L. Holm, E.L. Sonnhammer, S.R. Eddy, A. Bateman, and R.D. Finn The PFAM protein families database Nucleic Acids Res. 40 2012 D290 D301
162. Y. Jouanneau, H.S. Jeong, N. Hugo, C. Meyer, and J.C. Willison Overexpression in Escherichia coli of the rnf genes from Rhodobacter capsulatus - characterization of two membrane-bound iron-sulfur proteins Eur. J. Biochem. 251 1998 54 64 (Pubitemid 28080898)
163. T. Yagi The bacterial energy-transducing NADH-quinone oxidoreductases Biochim. Biophys. Acta 1141 1993 1 17 (Pubitemid 23051546)
164. T. Yagi, T. Yano, and A. Matsuno-Yagi Characteristics of the energy-transducing NADH-quinone oxidoreductase of Paracoccus denitrificans as revealed by biochemical, biophysical, and molecular biological approaches J. Bioenerg. Biomembr. 25 1993 339 345
165. S. Malki, I. Saimmaime, G. De Luca, M. Rousset, Z. Dermoun, and J.P. Belaich Characterization of an operon encoding an NADP-reducing hydrogenase in Desulfovibrio fructosovorans J. Bacteriol. 177 1995 2628 2636
166. O. Schmitz, G. Boison, R. Hilscher, B. Hundeshagen, W. Zimmer, F. Lottspeich, and H. Bothe Molecular biological analysis of a bidirectional hydrogenase from cyanobacteria Eur. J. Biochem. 233 1995 266 276
167. A. Tran-Betcke, U. Warnecke, C. Böcker, C. Zaborosch, and B. Friedrich Cloning and nucleotide sequences of the genes for the subunits of NAD-reducing hydrogenase of Alcaligenes eutrophus H16 J. Bacteriol. 172 1990 2920 2929 (Pubitemid 20179737)
168. I.M. Fearnley, and J.E. Walker Conservation of sequences of subunits of mitochondrial complex I and their relationships with other proteins Biochim. Biophys. Acta 1140 1992 105 134
169. J.E. Walker The NADH:ubiquinone oxidoreductase (complex I) of respiratory chains Q. Rev. Biophys. 25 1992 253 324 (Pubitemid 23014370)
170. 2 dehydrogenase from Methanosarcina mazei Gö1 FEMS Microbiol. Lett. 154 1997 231 237 (Pubitemid 27405182)
171. L.A. Sazanov, and P. Hinchliffe Structure of the hydrophilic domain of respiratory complex I from Thermus thermophilus Science 311 2006 1430 1436 (Pubitemid 43376691)
172. Y. Wang, L.Y. Geer, C. Chappey, J.A. Kans, and S.H. Bryant Cn3D: sequence and structure views for Entrez Trends Biochem. Sci. 25 2000 300 302 (Pubitemid 30333390)
173. M. Kallberg, H.P. Wang, S. Wang, J. Peng, Z.Y. Wang, H. Lu, and J.B. Xu Template-based protein structure modeling using the RaptorX web server Nat. Protoc. 7 2012 1511 1522
174. 420-non-reducing types Mol. Gen. Genet. 233 1992 217 224
175. 420-reducing [NiFe]-hydrogenase from a methanogenic archaeon by cryo-electron microscopy eLife 2 2013 e00218
176. A. Dupuis, I. Prieur, and J. Lunardi Toward a characterization of the connecting module of complex I J. Bioenerg. Biomembr. 33 2001 159 168 (Pubitemid 32994983)
177. M. Sato, P.K. Sinha, J. Torres-Bacete, A. Matsuno-Yagi, and T. Yagi Energy transducing roles of antiporter-like subunits in Escherichia coli NDH-1 with main focus on subunit NuoN (ND2) J. Biol. Chem. 288 2013 24705 24716
178. M. Simianu, E. Murakami, J.M. Brewer, and S.W. Ragsdale Purification and properties of the heme- and iron-sulfur-containing heterodisulfide reductase from Methanosarcina thermophila Biochemistry 37 1998 10027 10039 (Pubitemid 28366357)
179. 2:heterodisulfide oxidoreductase complex from membranes of Methanosarcina barkeri Eur. J. Biochem. 213 1993 529 535 (Pubitemid 23106087)
180. S. Heiden, R. Hedderich, E. Setzke, and R.K. Thauer Purification of a 2-subunit cytochrome b containing heterodisulfide reductase from methanol-grown Methanosarcina barkeri Eur. J. Biochem. 221 1994 855 861 (Pubitemid 24128057)
181. E. Murakami, U. Deppenmeier, and S.W. Ragsdale Characterization of the intramolecular electron transfer pathway from 2-hydroxyphenazine to the heterodisulfide reductase from Methanosarcina thermophila J. Biol. Chem. 276 2001 2432 2439
182. R. Hedderich, N. Hamann, and M. Bennati Heterodisulfide reductase from methanogenic archaea: a new catalytic role for an iron-sulfur cluster Biol. Chem. 386 2005 961 970 (Pubitemid 41548728)
183. E.C. Duin, S. Madadi-Kahkesh, R. Hedderich, M.D. Clay, and M.K. Johnson Heterodisulfide reductase from Methanothermobacter marburgensis contains an active-site [4Fe-4S] cluster that is directly involved in mediating heterodisulfide reduction FEBS Lett. 512 2002 263 268 (Pubitemid 34164492)
184. +-pyrophosphatase: a novel primary sodium pump Biochemistry 46 2007 8872 8878 (Pubitemid 47204451)
185. S. Bäumer, S. Lentes, G. Gottschalk, and U. Deppenmeier Identification and analysis of proton-translocating pyrophosphatases in the methanogenic archaeon Methansarcina mazei Archaea 1 2002 1 7 (Pubitemid 38871625)
186. V.N. Khmelenina, O.N. Rozova, and Y.A. Trotsenko Characterization of the recombinant pyrophosphate-dependent 6-phosphofructokinases from Methylomicrobium alcaliphilum 20Z and Methylococcus capsulatus Bath Methods Enzymol. 495 2011 1 14
187. B. Tjaden, A. Plagens, C. Dörr, B. Siebers, and R. Hensel Phosphoenolpyruvate synthetase and pyruvate, phosphate dikinase of Thermoproteus tenax: key pieces in the puzzle of archaeal carbohydrate metabolism Mol. Microbiol. 60 2006 287 298
188. J.M. Davies, R.J. Poole, P.A. Rea, and D. Sanders Potassium transport into plant vacuoles energized directly by a proton-pumping inorganic pyrophosphatase Proc. Natl. Acad. Sci. U. S. A. 89 1992 11701 11705 (Pubitemid 23004711)
189. T. Friedrich, K. Steinmüller, and H. Weiss The proton-pumping respiratory complex I of bacteria and mitochondria and its homolog in chloroplasts FEBS Lett. 367 1995 107 111
190. H.L. Mi, T. Endo, T. Ogawa, and K. Asada Thylakoid membrane-bound, NADPH-specific pyridine-nucleotide dehydrogenase complex mediates cyclic electron-transport in the cyanobacterium Synechocystis sp. PCC-68038 Plant Cell Physiol. 36 1995 661 668
191. N. Battchikova, M. Eisenhut, and E.M. Aro Cyanobacterial NDH-1 complexes: novel insights and remaining puzzles Biochim. Biophys. Acta 1807 2011 935 944
192. 2 dehydrogenase to heterodisulfide reductase FEBS Lett. 428 1998 295 298 (Pubitemid 28319702)
193. 2:quinone oxidoreductase from Archaeoglobus fulgidus - characterization of a membrane-bound multisubunit complex containing FAD and iron-sulfur clusters Eur. J. Biochem. 223 1994 503 511
194. H. Brüggemann, F. Falinski, and U. Deppenmeier Structure of the F420H2: quinone oxidoreductase of Archaeoglobus fulgidus - identification and overproduction of the F420H2-oxidizing subunit Eur. J. Biochem. 267 2000 5810 5814
195. Y.J. Park, C.B. Yoo, S.Y. Choi, and H.B. Lee Purifications and characterizations of a ferredoxin and its related 2-oxoacid:ferredoxin oxidoreductase from the hyperthermophilic archaeon, Sulfolobus solfataricus P1 J. Biochem. Mol. Biol. 39 2006 46 54 (Pubitemid 43232731)
196. P.L. Hagedoorn, T. Chen, I. Schröder, S.R. Piersma, S. de Vries, and W.R. Hagen Purification and characterization of the tungsten enzyme aldehyde:ferredoxin oxidoreductase from the hyperthermophilic denitrifier Pyrobaculum aerophilum J. Biol. Inorg. Chem. 10 2005 259 269 (Pubitemid 40768090)
197. A. Tersteegen, D. Linder, R.K. Thauer, and R. Hedderich Structures and functions of four anabolic 2-oxoacid oxidoreductases in Methanobacterium thermoautotrophicum Eur. J. Biochem. 244 1997 862 868 (Pubitemid 27130524)
198. L. Kerscher, and D. Oesterhelt Purification and properties of two 2-oxoacid:ferredoxin oxidoreductases from Halobacterium halobium Eur. J. Biochem. 116 1981 587 594 (Pubitemid 11055735)
199. H. Sakuraba, and T. Ohshima Novel energy metabolism in anaerobic hyperthermophilic archaea: a modified Embden-Meyerhof pathway J. Biosci. Bioeng. 93 2002 441 448 (Pubitemid 34665024)
200. A. Kletzin, and M.W. Adams Tungsten in biological systems FEMS Microbiol. Rev. 18 1996 5 63 (Pubitemid 26163588)
201. R. Roy, and M.W. Adams Characterization of a fourth tungsten-containing enzyme from the hyperthermophilic archaeon Pyrococcus furiosus J. Bacteriol. 184 2002 6952 6956 (Pubitemid 36356129)
202. F. Mayer, and V. Müller Adaptations of anaerobic archaea to life under extreme energy limitation FEMS Microbiol. Rev. 2013 10.1111/1574-6976. 12043
203. Z. Mladenovska, and B.K. Ahring Growth kinetics of thermophilic Methanosarcina spp. isolated from full-scale biogas plants treating animal manures FEMS Microbiol. Ecol. 31 2000 225 229 (Pubitemid 30136213)
204. Q.S. Jin Energy conservation of anaerobic respiration Am. J. Sci. 312 2012 573 628