Unifying concepts in anaerobic respiration: Insights from dissimilatory sulfur metabolism

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1827, Issue 2, 2013, Pages 145-160

  Grein, Fabian ^a,b   Ramos, Ana Raquel ^a   Venceslau, Sofia S ^a   Pereira, Inês A C ^a  

^a INSTITUTO DE TECNOLOGIA QUÍMICA E BIOLÓGICA   (Portugal)

^b UNIVERSITY OF BONN   (Germany)

Author keywords

Anaerobic respiration; Dissimilatory sulfur metabolism; Redox module; Respiratory membrane complex; Sulfate reducing bacteria; Sulfur oxidizing bacteria

Indexed keywords

ADENOSINE 5' PHOSPHOSULFATE; APRBA REDUCTASE; BACTERIUM PROTEIN QMOA; BACTERIUM PROTEIN QMOB; BACTERIUM PROTEIN QMOC; CYSTEINE; CYTOCHROME C; DISULFIDE; DSRAB SULFITE REDUCTASE; ENZYME; GLYCINE; HDRA PROTEIN; HDRD PROTEIN; HETERODISULFIDE REDUCTASE; HMC PROTEIN; IRON; IRON SULFUR MOLYBDOENZYME; OXIDOREDUCTASE; PERIPLASMIC PROTEIN; QUINONE REDUCTASE COMPLEX A; QUINONE REDUCTASE COMPLEX B; QUINONE REDUCTASE COMPLEX C; QUINONE REDUCTASE COMPLEX D; SULFATE ADENYLYLTRANSFERASE; SULFUR; THIOL; TMC PROTEIN; UNCLASSIFIED DRUG;

ANAEROBIC CAPACITY; ANAEROBIC RESPIRATION; ARCHAEOGLOBUS; ARCHAEOGLOBUS FULGIDUS; ARCHAEOGLOBUS VINOSUM; BACTERIAL GENE; BACTERIAL MEMBRANE; BIOENERGY; BREATHING; CYTOPLASM; DESULFOVIBRIO DESULFURICANS; ELECTRON TRANSPORT; ENERGY CONSERVATION; ENERGY METABOLISM; ENZYME STRUCTURE; GENE IDENTIFICATION; GENETIC CODE; METHANOGENIC ARCHAEON; MOLECULAR EVOLUTION; NONHUMAN; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN ISOLATION; PROTEIN PROTEIN INTERACTION; REDUCTION KINETICS; REVIEW; SULFATE REDUCING ARCHAEON; SULFATE REDUCING BACTERIUM; SULFUR OXIDIZING BACTERIUM;

AEROBIOSIS; ARCHAEA; BIOLOGICAL EVOLUTION; SULFUR;

PROKARYOTA;

EID: 84871714638     PISSN: 00052728     EISSN: 18792650     Source Type: Journal    
DOI: 10.1016/j.bbabio.2012.09.001     Document Type: Review

References (197)

1. D.E. Canfield, and R. Raiswell The evolution of the sulfur cycle Am. J. Sci. 299 1999 697 723
2. D.E. Canfield, M.T. Rosing, and C. Bjerrum Early anaerobic metabolisms Philos. Trans. R. Soc. Lond. B Biol. Sci. 361 2006 1819 1834
3. 2 photolysis: implications for the early atmosphere J. Geophys. Res. 106 2001 32829 32839
4. A.A. Pavlov, and J.F. Kasting Mass-independent fractionation of sulfur isotopes in Archean sediments: strong evidence for an anoxic Archean atmosphere Astrobiology 2 2002 27 41
5. M.F. Hohmann-Marriott, and R.E. Blankenship Evolution of photosynthesis Annu. Rev. Plant Biol. 62 2011 515 548
6. M.M. Tice, and D.R. Lowe Photosynthetic microbial mats in the 3,416-Myr-old ocean Nature 431 2004 549 552
7. P. Philippot, M. Van Zuilen, K. Lepot, C. Thomazo, J. Farquhar, and M.J. Van Kranendonk Early Archaean microorganisms preferred elemental sulfur, not sulfate Science 317 2007 1534 1537
8. Y. Shen, R. Buick, and D.E. Canfield Isotopic evidence for microbial sulphate reduction in the early Archaean era Nature 410 2001 77 81
9. D. Wacey, N. McLoughlin, M.J. Whitehouse, and M.R. Kilburn Two coexisting sulfur metabolisms in a ca. 3400 Ma sandstone Geology 38 2010 1115 1118
10. D. Wacey, M.R. Kilburn, M. Saunders, J. Cliff, and M.D. Brasier Microfossils of sulphur-metabolizing cells in 3.4-billion-year-old rocks of Western Australia Nat. Geosci. 4 2011 698 702
11. J. Farquhar, H.M. Bao, and M. Thiemens Atmospheric influence of Earth's earliest sulfur cycle Science 289 2000 756 758
12. D.E. Canfield A new model for Proterozoic ocean chemistry Nature 396 1998 450 453
13. D.E. Canfield, K.S. Habicht, and B. Thamdrup The Archean sulfur cycle and the early history of atmospheric oxygen Science 288 2000 658 661
14. J. Farquhar, M. Peters, D.T. Johnston, H. Strauss, A. Masterson, U. Wiechert, and A.J. Kaufman Isotopic evidence for Mesoarchaean anoxia and changing atmospheric sulphur chemistry Nature 449 2007 706 709
15. K.S. Habicht, M. Gade, B. Thamdrup, P. Berg, and D.E. Canfield Calibration of sulfate levels in the Archean Ocean Science 298 2002 2372 2374
16. F.U. Battistuzzi, A. Feijao, and S.B. Hedges A genomic timescale of prokaryote evolution: insights into the origin of methanogenesis, phototrophy, and the colonization of land BMC Evol. Biol. 4 2004
17. D.F. Feng, G. Cho, and R.F. Doolittle Determining divergence times with a protein clock: update and reevaluation Proc. Natl. Acad. Sci. 94 1997 13028 13033
18. B. Rasmussen, I.R. Fletcher, J.J. Brocks, and M.R. Kilburn Reassessing the first appearance of eukaryotes and cyanobacteria Nature 455 2008 1101 U1109
19. A.D. Anbar, and A.H. Knoll Proterozoic ocean chemistry and evolution: a bioinorganic bridge? Science 297 2002 1137 1142
20. D.E. Canfield, S.W. Poulton, and G.M. Narbonne Late-Neoproterozoic deep-ocean oxygenation and the rise of animal life Science 315 2007 92 95
21. C. Scott, T.W. Lyons, A. Bekker, Y. Shen, S.W. Poulton, X. Chu, and A.D. Anbar Tracing the stepwise oxygenation of the Proterozoic ocean Nature 452 2008 456 459
22. D.T. Johnston, F. Wolfe-Simon, A. Pearson, and A.H. Knoll Anoxygenic photosynthesis modulated Proterozoic oxygen and sustained Earth's middle age Proc. Natl. Acad. Sci. 106 2009 16925 16929
23. B.B. Jørgensen Mineralization of organic matter in the sea-bed - the role of sulphate reduction Nature 390 1982 364 370
24. J. Farquhar, N.P. Wu, D.E. Canfield, and H. Oduro Connections between sulfur cycle evolution, sulfur isotopes, sediments, and base metal sulfide deposits Econ. Geol. 105 2010 509 533
25. T.W. Lyons, and B.C. Gill Ancient sulfur cycling and oxygenation of the early biosphere Elements 6 2010 93 99
26. D.T. Johnston Multiple sulfur isotopes and the evolution of Earth's surface sulfur cycle Earth Sci. Rev. 106 2011 161 183
27. C.E. Blank Evolutionary timing of the origins of mesophilic sulphate reduction and oxygenic photosynthesis: a phylogenomic dating approach Geobiology 2 2004 1 20
28. C.E. Blank Phylogenomic dating - the relative antiquity of archaeal metabolic and physiological traits Astrobiology 9 2009 193 219
29. L.A. David, and E.J. Alm Rapid evolutionary innovation during an Archaean genetic expansion Nature 469 2011 93 96
30. F. Baymann, E. Lebrun, M. Brugna, B. Schoepp-Cothenet, M.T. Giudici-Orticoni, and W. Nitschke The redox protein construction kit: pre-last universal common ancestor evolution of energy-conserving enzymes Philos. Trans. R. Soc. Lond. B Biol. Sci. 358 2003 267 274
31. C.R. Woese Interpreting the universal phylogenetic tree Proc. Natl. Acad. Sci. 97 2000 8392 8396
32. Y. Boucher, C.J. Douady, R.T. Papke, D.A. Walsh, M.E.R. Boudreau, C.L. Nesbo, R.J. Case, and W.F. Doolittle Lateral gene transfer and the origins of prokaryotic groups Annu. Rev. Genet. 37 2003 283 328
33. I.A.C. 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
34. T. Leustek, M.N. Martin, J.A. Bick, and J.P. Davies Pathways and regulation of sulfur metabolism revealed through molecular and genetic studies Annu. Rev. Plant Physiol. Plant Mol. Biol. 51 2000 141 165
35. L.L. Barton, and G.D. Fauque Biochemistry, physiology and biotechnology of sulfate-reducing bacteria Adv. Appl. Microbiol. 68 2009 41 98
36. G. Muyzer, and A.J. Stams The ecology and biotechnology of sulphate-reducing bacteria Nat. Rev. Microbiol. 6 2008 441 454
37. R. Rabus, T. Hansen, and F. Widdel Dissimilatory sulfate- and sulfur-reducing prokaryotes M.e.a. Dworkin, The Prokaryotes vol. 2 2007 Springer-Verlag New York 659 768 http://link.springer-ny.com/link/service/books/ 10125/
38. Y. Taguchi, M. Sugishima, and K. Fukuyama Crystal structure of a novel zinc-binding ATP sulfurylase from Thermus thermophilus HB8 Biochemistry 43 2004 4111 4118
39. T.C. Ullrich, M. Blaesse, and R. Huber Crystal structure of ATP sulfurylase from Saccharomyces cerevisiae, a key enzyme in sulfate activation EMBO J. 20 2001 316 329
40. B.R. Crane, and E.D. Getzoff The relationship between structure and function for the sulfite reductases Curr. Opin. Struct. Biol. 6 1996 744 756
41. G. Fritz, T. Büchert, and P.M.H. Kroneck The function of the [4Fe4S] clusters and FAD in bacterial and archaeal adenylylsulfate reductases. Evidence for flavin-catalyzed reduction of adenosine 5′-phosphosulfate J. Biol. Chem. 277 2002 26066 26073
42. G. Fritz, A. Roth, A. Schiffer, T. Buchert, G. Bourenkov, H.D. Bartunik, H. Huber, K.O. Stetter, P.M. Kroneck, and U. Ermler Structure of adenylylsulfate reductase from the hyperthermophilic Archaeoglobus fulgidus at 1.6-A resolution Proc. Natl. Acad. Sci. 99 2002 1836 1841
43. J. Lampreia, A.S. Pereira, and J.J.G. Moura Adenylylsulfate reductases from sulfate-reducing bacteria Methods Enzymol. 243 1994 241 260
44. N. Speich, C. Dahl, P. Heisig, A. Klein, F. Lottspeich, K.O. Stetter, and H.G. Trüper Adenylylsulphate reductase from the sulfate-reducing archaeon Archaeoglobus fulgidus - cloning and characterization of the genes and comparison of the enzyme with other iron-sulfur flavoproteins Microbiology 140 1994 1273 1284
45. C. Dahl, N.M. Kredich, R. Deutzmann, and H.G. Trüper Dissimilatory sulphite reductase from Archaeoglobus fulgidus: physico-chemical properties of the enzyme and cloning, sequencing and analysis of the reductase genes J. Gen. Microbiol. 139 1993 1817 1828
46. I. Moura, J. LeGall, A.R. Lino, H.D. Peck, G. Fauque, A.V. Xavier, D.V. Dervartanian, J.J.G. Moura, and B.H. Huynh Characterization of two dissimilatory sulfite reductases (desulforubidin and desulfoviridin) from the sulfate-reducing bacteria - mossbauer and EPR studies J. Am. Chem. Soc. 110 1988 1075 1082
47. J.R. Cort, S.V. Mariappan, C.Y. Kim, M.S. Park, T.S. Peat, G.S. Waldo, T.C. Terwilliger, and M.A. Kennedy Solution structure of Pyrobaculum aerophilum DsrC, an archaeal homologue of the gamma subunit of dissimilatory sulfite reductase Eur. J. Biochem. 268 2001 5842 5850
48. C. Dahl, S. Engels, A.S. Pott-Sperling, A. Schulte, J. Sander, Y. Lübbe, O. Deuster, and D.C. Brune Novel genes of the dsr gene cluster and evidence for close interaction of Dsr proteins during sulfur oxidation in the phototrophic sulfur bacterium Allochromatium vinosum J. Bacteriol. 187 2005 1392 1404
49. G.J. Mander, M.S. Weiss, R. Hedderich, J. Kahnt, U. Ermler, and E. Warkentin X-ray structure of the gamma-subunit of a dissimilatory sulfite reductase: fixed and flexible C-terminal arms FEBS Lett. 579 2005 4600 4604
50. T.F. Oliveira, C. Vonrhein, P.M. Matias, S.S. Venceslau, I.A.C. Pereira, and M. Archer The crystal structure of Desulfovibrio vulgaris dissimilatory sulfite reductase bound to DsrC provides novel insights into the mechanism of sulfate respiration J. Biol. Chem. 283 2008 34141 34149
51. R.H. Pires, S.S. Venceslau, F. Morais, M. Teixeira, A.V. Xavier, and I.A. Pereira Characterization of the Desulfovibrio desulfuricans ATCC 27774 DsrMKJOP complex- A membrane-bound redox complex involved in the sulfate respiratory pathway Biochemistry 45 2006 249 262
52. N. Mizuno, G. Voordouw, K. Miki, A. Sarai, and Y. Higuchi Crystal structure of dissimilatory sulfite reductase D (DsrD) protein - possible interaction with B- and Z-DNA by its winged-helix motif Structure 11 2003 1133 1140
53. S.M. Caffrey, and G. Voordouw Effect of sulfide on growth physiology and gene expression of Desulfovibrio vulgaris Hildenborough Antonie Van Leeuwenhoek 97 2010 11 20
54. N.U. Frigaard, and C. Dahl Sulfur metabolism in phototrophic sulfur bacteria Adv. Microb. Physiol. 54 2009 103 200
55. D. Sperling, U. Kappler, A. Wynen, C. Dahl, and H.G. Trüper Dissimilatory ATP sulfurylase from the hyperthermophilic sulfate reducer Archaeoglobus fulgidus belongs to the group of homo-oligomeric ATP sulfurylases FEMS Microbiol. Lett. 162 1998 257 264
56. M.W. Friedrich Phylogenetic analysis reveals multiple lateral transfers of adenosine-5′-phosphosulfate reductase genes among sulfate-reducing microorganisms J. Bacteriol. 184 2002 278 289
57. W.M. Hipp, A.S. Pott, N. Thum-Schmitz, I. Faath, C. Dahl, and H.G. Truper Towards the phylogeny of APS reductases and sirohaem sulfite reductases in sulfate-reducing and sulfur-oxidizing prokaryotes Microbiology 143 Pt. 9 1997 2891 2902
58. B. Meyer, and J. Kuever Molecular analysis of the distribution and phylogeny of dissimilatory adenosine-5′-phosphosulfate reductase-encoding genes (aprBA) among sulfur-oxidizing prokaryotes Microbiology 153 2007 3478 3498
59. B. Meyer, and J. Kuever Phylogeny of the alpha and beta subunits of the dissimilatory adenosine-5′-phosphosulfate (APS) reductase from sulfate-reducing prokaryotes - origin and evolution of the dissimilatory sulfate-reduction pathway Microbiology 153 2007 2026 2044
60. M. Klein, M. Friedrich, A.J. Roger, P. Hugenholtz, S. Fishbain, H. Abicht, L.L. Blackall, D.A. Stahl, and M. Wagner Multiple lateral transfers of dissimilatory sulfite reductase genes between major lineages of sulfate-reducing prokaryotes J. Bacteriol. 183 2001 6028 6035
61. O. Larsen, T. Lien, and N.K. Birkeland Dissimilatory sulfite reductase from Archaeoglobus profundus and Desulfotomaculum thermocisternum: phylogenetic and structural implications from gene sequences Extremophiles 3 1999 63 70
62. A. Loy, S. Duller, C. Baranyi, M. Mussmann, J. Ott, I. Sharon, O. Beja, D. Le Paslier, C. Dahl, and M. Wagner Reverse dissimilatory sulfite reductase as phylogenetic marker for a subgroup of sulfur-oxidizing prokaryotes Environ. Microbiol. 11 2009 289 299
63. A. Loy, S. Duller, and M. Wagner Evolution and ecology of microbes dissimilating sulfur compounds: insights from siroheme sulfite reductases C. Dahl, C. Friedrich, Microbial Sulfur Metabolism 2007 Springer Heidelberg 46 59
64. M. Molitor, C. Dahl, I. Molitor, U. Schafer, N. Speich, R. Huber, R. Deutzmann, and H.G. Truper A dissimilatory sirohaem-sulfite-reductase-type protein from the hyperthermophilic archaeon Pyrobaculum islandicum Microbiology 144 Pt. 2 1998 529 541
65. M. Wagner, A.J. Roger, J.L. Flax, G.A. Brusseau, and D.A. Stahl Phylogeny of dissimilatory sulfite reductases supports an early origin of sulfate respiration J. Bacteriol. 180 1998 2975 2982
66. R.H. Pires, A.I.C. Lourenco, F. Morais, M. Teixeira, A.V. Xavier, L.M. Saraiva, and I.A. Pereira A novel membrane-bound respiratory complex from Desulfovibrio desulfuricans ATCC 27774 Biochim. Biophys. Acta 1605 2003 67 82
67. B. Meyer, and J. Kuever Homology modeling of dissimilatory APS reductases (AprBA) of sulfur-oxidizing and sulfate-reducing prokaryotes PLoS One 3 2008 e1514
68. A. Schiffer, K. Parey, E. Warkentin, K. Diederichs, H. Huber, K.O. Stetter, P.M. Kroneck, and U. Ermler Structure of the dissimilatory sulfite reductase from the hyperthermophilic archaeon Archaeoglobus fulgidus J. Mol. Biol. 379 2008 1063 1074
69. A. Dhillon, S. Goswami, M. Riley, A. Teske, and M. Sogin Domain evolution and functional diversification of sulfite reductases Astrobiology 5 2005 18 29
70. B.R. Crane, L.M. Siegel, and E.D. Getzoff Sulfite reductase structure at 1.6 Angstrom - evolution and catalysis for reduction of inorganic anions Science 270 1995 59 67
71. J.M. Akagi Respiratory sulfate reduction L.L. Barton, Sulfate-reducing Bacteria 1995 Plenum Press New York 89 111
72. A.S. Pott, and C. Dahl Sirohaem sulfite reductase and other proteins encoded by genes at the dsr locus of Chromatium vinosum are involved in the oxidation of intracellular sulfur Microbiology 144 1998 1881 1894
73. C. Holkenbrink, S.O. Barbas, A. Mellerup, H. Otaki, and N.U. Frigaard Sulfur globule oxidation in green sulfur bacteria is dependent on the dissimilatory sulfite reductase system Microbiology 157 2011 1229 1239
74. M. Mussmann, M. Richter, T. Lombardot, A. Meyerdierks, J. Kuever, M. Kube, F.O. Glockner, and R. Amann Clustered genes related to sulfate respiration in uncultured prokaryotes support the theory of their concomitant horizontal transfer J. Bacteriol. 187 2005 7126 7137
75. A. Magalon, J.G. Fedor, A. Walburger, and J.H. Weiner Molybdenum enzymes in bacteria and their maturation Coord. Chem. Rev. 255 2011 1159 1178
76. R.A. Rothery, G.J. Workun, and J.H. Weiner The prokaryotic complex iron-sulfur molybdoenzyme family Biochim. Biophys. Acta 1778 2008 1897 1929
77. D.J. Richardson Bacterial respiration: a flexible process for a changing environment Microbiology 146 2000 551 571
78. B. Schoepp-Cothenet, R. van Lis, P. Philippot, A. Magalon, M.J. Russell, and W. Nitschke The ineluctable requirement for the trans-iron elements molybdenum and/or tungsten in the origin of life Sci. Rep. 2 2012
79. B.C. Berks, M.D. Page, D.J. Richardson, A. Reilly, A. Cavill, F. Outen, and S.J. Ferguson Sequence analysis of subunits of the membrane-bound nitrate reductase from a denitrifying bacterium: the integral membrane subunit provides a prototype for the dihaem electron-carrying arm of a redox loop Mol. Microbiol. 15 1995 319 331
80. M.G. Bertero, R.A. Rothery, M. Palak, C. Hou, D. Lim, F. Blasco, J.H. Weiner, and N.C. Strynadka Insights into the respiratory electron transfer pathway from the structure of nitrate reductase A Nat. Struct. Biol. 10 2003 681 687
81. M. Jormakka, S. Tornroth, B. Byrne, and S. Iwata Molecular basis of proton motive force generation: structure of formate dehydrogenase-N Science 295 2002 1863 1868
82. M. Jormakka, K. Yokoyama, T. Yano, M. Tamakoshi, S. Akimoto, T. Shimamura, P. Curmi, and S. Iwata Molecular mechanism of energy conservation in polysulfide respiration Nat. Struct. Mol. Biol. 15 2008 730 737
83. J. Simon, and M. Kern Quinone-reactive proteins devoid of haem b form widespread membrane-bound electron transport modules in bacterial respiration Biochem. Soc. Trans. 36 2008 1011 1016
84. F. Grein, I.A.C. Pereira, and C. Dahl Biochemical characterization of individual components of the Allochromatium vinosum DsrMKJOP transmembrane complex aids understanding of complex function in vivo J. Bacteriol. 192 2010 6369 6377
85. G. Cecchini, I. Schroder, R.P. Gunsalus, and E. Maklashina Succinate dehydrogenase and fumarate reductase from Escherichia coli Biochim. Biophys. Acta 1553 2002 140 157
86. P.M. Vignais, and B. Billoud Occurrence, classification, and biological function of hydrogenases: an overview Chem. Rev. 107 2007 4206 4272
87. J. Simon, R.J. van Spanning, and D.J. Richardson The organisation of proton motive and non-proton motive redox loops in prokaryotic respiratory systems Biochim. Biophys. Acta 1777 2008 1480 1490
88. M. Jormakka, B. Byrne, and S. Iwata Proton motive force generation by a redox loop mechanism FEBS Lett. 545 2003 25 30
89. 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
90. R. Hedderich, O. Klimmek, A. Kroger, R. Dirmeier, M. Keller, and K.O. Stetter Anaerobic respiration with elemental sulfur and with disulfides FEMS Microbiol. Rev. 22 1999 353 381
91. 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
92. W. Badziong, R.K. Thauer, and J.G. Zeikus Isolation and characterization of Desulfovibrio growing on hydrogen plus sulfate as the sole energy source Arch. Microbiol. 116 1978 41 49
93. R.K. Thauer, E. Stackebrandt, and W.A. Hamilton Energy metabolism and phylogenetic diversity of sulphate-reducing bacteria L.L. Barton, W.A. Hamilton, Sulphate Reducing Bacteria - Environmental and Engineered Systems 2007 Cambridge University Press Cambridge 1 37
94. M.D. Collins, and F. Widdel Respiratory quinones of sulfate-reducing and sulfur-reducing bacteria - a systematic investigation Syst. Appl. Microbiol. 8 1986 8 18
95. K.L. Keller, and J.D. Wall Genetics and molecular biology of the electron flow for sulfate respiration in Desulfovibrio Front. Microbiol. 2 2011 135
96. I.A.C. Pereira Membrane complexes in Desulfovibrio C. Friedrich, C. Dahl, Microbial Sulfur Metabolism 2008 Springer-Verlag 24 35
97. J.Z. Zhou, Q. He, C.L. Hemme, A. Mukhopadhyay, K. Hillesland, A.F. Zhou, Z.L. He, J.D. Van Nostrand, T.C. Hazen, D.A. Stahl, J.D. Wall, and A.P. Arkin How sulphate-reducing microorganisms cope with stress: lessons from systems biology Nat. Rev. Microbiol. 9 2011 452 466
98. A.S. Bradley, W.D. Leavitt, and D.T. Johnston Revisiting the dissimilatory sulfate reduction pathway Geobiology 9 2011 446 457
99. 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. 108 2011 2981 2986
100. A. Stojanowic, G.J. Mander, E.C. Duin, and R. Hedderich Physiological role of the F420-non-reducing hydrogenase (Mvh) from Methanothermobacter marburgensis Arch. Microbiol. 180 2003 194 203
101. G.M. Zane, H.C. Yen, and J.D. Wall Effect of the deletion of qmoABC and the promoter-distal gene encoding a hypothetical protein on sulfate reduction in Desulfovibrio vulgaris Hildenborough Appl. Environ. Microbiol. 76 2010 5500 5509
102. P. Junier, T. Junier, S. Podell, D.R. Sims, J.C. Detter, A. Lykidis, C.S. Han, N.S. Wigginton, T. Gaasterland, and R. Bernier-Latmani The genome of the Gram-positive metal- and sulfate-reducing bacterium Desulfotomaculum reducens strain MI-1 Environ. Microbiol. 12 2010 2738 2754
103. L.K. Chan, T.S. Weber, R.M. Morgan-Kiss, and T.E. Hanson A genomic region required for phototrophic thiosulfate oxidation in the green sulfur bacterium Chlorobium tepidum (syn. Chlorobaculum tepidum) Microbiology 154 2008 818 829
104. J. Rodriguez, J. Hiras, and T.E. Hanson Sulfite oxidation in Chlorobaculum tepidum Front. Microbiol. 2 2011 112
105. A.R. Ramos, K.L. Keller, J.D. Wall, and I.A.C. Pereira The membrane QmoABC complex interacts directly with the dissimilatory adenosine 5′-phosphosulfate reductase in sulfate reducing bacteria Front. Microbiol. 3 2012 137
106. G. Herrmann, E. Jayamani, G. Mai, and W. Buckel Energy conservation via electron-transferring flavoprotein in anaerobic bacteria J. Bacteriol. 190 2008 784 791
107. W. Nitschke, and M.J. Russell Redox bifurcations: mechanisms and importance to life now, and at its origin: a widespread means of energy conversion in biology unfolds Bioessays 34 2011 106 109
108. 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
109. W.F. Martin Hydrogen, metals, bifurcating electrons, and proton gradients: the early evolution of biological energy conservation FEBS Lett. 2012 485 493
110. W. Nitschke, and M.J. Russell Hydrothermal focusing of chemical and chemiosmotic energy, supported by delivery of catalytic Fe, Ni, Mo/W, Co, S and Se, forced life to emerge J. Mol. Evol. 69 2009 481 496
111. G.J. Schut, and M.W. Adams The iron-hydrogenase of Thermotoga maritima utilizes ferredoxin and NADH synergistically: a new perspective on anaerobic hydrogen production J. Bacteriol. 191 2009 4451 4457
112. + reduction with NADH are coupled via an electron-bifurcating enzyme complex in Clostridium kluyveri J. Bacteriol. 192 2010 5115 5123
113. G.J. Mander, E.C. Duin, D. Linder, K.O. Stetter, and R. Hedderich Purification and characterization of a membrane-bound enzyme complex from the sulfate-reducing archaeon Archaeoglobus fulgidus related to heterodisulfide reductase from methanogenic archaea Eur. J. Biochem. 269 2002 1895 1904
114. J. Sander, S. Engels-Schwarzlose, and C. Dahl Importance of the DsrMKJOP complex for sulfur oxidation in Allochromatium vinosum and phylogenetic analysis of related complexes in other prokaryotes Arch. Microbiol. 186 2006 357 366
115. S. Heiden, R. Hedderich, E. Setzke, and R.K. Thauer Purification of a two-subunit cytochrome b-containing heterodisulfide reductase from methanol-grown Methanosarcina barkeri Eur. J. Biochem. 221 1994 855 861
116. A. Kunkel, M. Vaupel, S. Heim, R.K. Thauer, and R. Hedderich Heterodisulfide reductase from methanol-grown cells of Methanosarcina barkeri is not a flavoenzyme Eur. J. Biochem. 244 1997 226 234
117. G.J. Mander, A.J. Pierik, H. Huber, and R. Hedderich Two distinct heterodisulfide reductase-like enzymes in the sulfate-reducing archaeon Archaeoglobus profundus Eur. J. Biochem. 271 2004 1106 1116
118. F. Grein, S.S. Venceslau, L. Schneider, P. Hildebrandt, S. Todorovic, I.A.C. Pereira, and C. Dahl DsrJ, an essential part of the DsrMKJOP transmembrane complex in the purple sulfur bacterium Allochromatium vinosum, is an unusual triheme cytochrome c Biochemistry 49 2010 8290 8299
119. V.A. Bamford, S. Bruno, T. Rasmussen, C. Appia-Ayme, M.R. Cheesman, B.C. Berks, and A.M. Hemmings Structural basis for the oxidation of thiosulfate by a sulfur cycle enzyme EMBO J. 21 2002 5599 5610
120. M.R. Cheesman, P.J. Little, and B.C. Berks Novel heme ligation in a c-type cytochrome involved in thiosulfate oxidation: EPR and MCD of SoxAX from Rhodovulum sulfidophilum Biochemistry 40 2001 10562 10569
121. J.R. Kilmartin, M.J. Maher, K. Krusong, C.J. Noble, G.R. Hanson, P.V. Bernhardt, M.J. Riley, and U. Kappler Insights into structure and function of the active site of SoxAX cytochromes J. Biol. Inorg. Chem. 286 2011 24872 24881
122. S.M. da Silva, I. Pacheco, and I.A.C. Pereira Electron transfer between periplasmic formate dehydrogenase and cytochromes c in Desulfovibrio desulfuricans ATCC 27774 J. Biol. Inorg. Chem. 17 2012 831 838
123. J.R. Cort, U. Selan, A. Schulte, F. Grimm, M.A. Kennedy, and C. Dahl Allochromatium vinosum DsrC: solution-state NMR structure, redox properties, and interaction with DsrEFH, a protein essential for purple sulfur bacterial sulfur oxidation J. Mol. Biol. 382 2008 692 707
124. S.A. Haveman, V. Brunelle, J.K. Voordouw, G. Voordouw, J.F. Heidelberg, and R. Rabus Gene expression analysis of energy metabolism mutants of Desulfovibrio vulgaris Hildenborough indicates an important role for alcohol dehydrogenase J. Bacteriol. 185 2003 4345 4353
125. J.D. Wall, A.P. Arkin, N.C. Balci, and B. Rapp-Giles Genetics and genomics of sulfate respiration in Desulfovibrio C. Dahl, C.G. Friedrich, Microbial Sulfur Metabolism 2008 Springer-Verlag Heidelbeg 1 12
126. D.E. Canfield, F.J. Stewart, B. Thamdrup, L. De Brabandere, T. Dalsgaard, E.F. Delong, N.P. Revsbech, and O. Ulloa A cryptic sulfur cycle in oxygen-minimum-zone waters off the Chilean coast Science 330 2010 1375 1378
127. F.J. Stewart, A.K. Sharma, J.A. Bryant, J.M. Eppley, and E.F. DeLong Community transcriptomics reveals universal patterns of protein sequence conservation in natural microbial communities Genome Biol. 12 2011
128. Y. Ikeuchi, N. Shigi, J. Kato, A. Nishimura, and T. Suzuki Mechanistic insights into multiple sulfur mediators sulfur relay by involved in thiouridine biosynthesis at tRNA wobble positions Mol. Cell 21 2006 97 108
129. Y. Stockdreher, S.S. Venceslau, M. Josten, H.G. Sahl, I.A.C. Pereira, and C. Dahl Cytoplasmic sulfurtransferases in the purple sulfur bacterium Allochromatium vinosum: evidence for sulfur transfer from DsrEFH to DsrC PLoS One 7 2012 e40785
130. Y.C. Hsieh, M.Y. Liu, V.C.C. Wang, Y.L. Chiang, E.H. Liu, W.G. Wu, S.I. Chan, and C.J. Chen Structural insights into the enzyme catalysis from comparison of three forms of dissimilatory sulphite reductase from Desulfovibrio gigas Mol. Microbiol. 78 2010 1101 1116
131. T.F. Oliveira, E. Franklin, J.P. Afonso, A.R. Khan, N.J. Oldham, I.A.C. Pereira, and M. Archer Structural insights into dissimilatory sulfite reductases: structure of desulforubidin from Desulfomicrobium norvegicum Front. Microbiol. 2 2011 71
132. U. Deppenmeier The membrane-bound electron transport system of Methanosarcina species J. Bioenerg. Biomembr. 36 2004 55 64
133. P.M. Matias, I.A.C. Pereira, C.M. Soares, and M.A. Carrondo Sulphate respiration from hydrogen in Desulfovibrio bacteria: a structural biology overview Prog. Biophys. Mol. Biol. 89 2005 292 329
134. C.V. Romão, M. Archer, S.A. Lobo, R.O. Louro, I.A.C. Pereira, L.M. Saraiva, M. Teixeira, and M.P.M. Diversity of heme proteins in sulfate reducing bacteria K.M. Kadish, K.M. Smith, R. Guilard, Handbook of Porphyrin Science vol. 19 (89) 2012 World Scientific Publishing Co. Singapore 139 230
135. J.R. Postgate Presence of cytochrome in an obligate anaerobe Biochem. J. 56 1954 xi
136. M. Ishimoto, J. Koyama, and Y. Nagai Role of a cytochrome in thiosulfate reduction by a sulfate reducing bacterium Seikagaku Zasshi 26 1954 303
137. J.M. Odom, and H.D. Peck Jr. Hydrogen cycling as a general mechanism for energy coupling in the sulfate-reducing bacteria, Desulfovibrio sp. FEMS Microbiol. Lett. 12 1981 47 50
138. R. Rabus, A. Ruepp, T. Frickey, T. Rattei, B. Fartmann, M. Stark, M. Bauer, A. Zibat, T. Lombardot, I. Becker, J. Amann, K. Gellner, H. Teeling, W.D. Leuschner, F.O. Glockner, A.N. Lupas, R. Amann, and H.P. Klenk The genome of Desulfotalea psychrophila, a sulfate-reducing bacterium from permanently cold Arctic sediments Environ. Microbiol. 6 2004 887 902
139. 2-tolerance? Biochim. Biophys. Acta 1817 2012 1565 1575
140. J.F. Heidelberg, R. Seshadri, S.A. Haveman, C.L. Hemme, I.T. Paulsen, J.F. Kolonay, J.A. Eisen, N. Ward, B. Methe, L.M. Brinkac, S.C. Daugherty, R.T. Deboy, R.J. Dodson, A.S. Durkin, R. Madupu, W.C. Nelson, S.A. Sullivan, D. Fouts, D.H. Haft, J. Selengut, J.D. Peterson, T.M. Davidsen, N. Zafar, L.W. Zhou, D. Radune, G. Dimitrov, M. Hance, K. Tran, H. Khouri, J. Gill, T.R. Utterback, T.V. Feldblyum, J.D. Wall, G. Voordouw, and C.M. Fraser The genome sequence of the anaerobic, sulfate-reducing bacterium Desulfovibrio vulgaris Hildenborough Nat. Biotechnol. 22 2004 554 559
141. I.A.C. Pereira, S.A. Haveman, and G. Voordouw Biochemical, genetic and genomic characterization of anaerobic electron transport pathways in sulphate-reducing delta-proteobacteria L.L. Barton, W.A. Allan Hamilton, Sulphate-reducing Bacteria: Environmental and Engineered Systems 2007 Cambridge University Press 215 240
142. S.A. Caffrey, H.S. Park, J.K. Voordouw, Z. He, J. Zhou, and G. Voordouw Function of periplasmic hydrogenases in the sulfate-reducing bacterium Desulfovibrio vulgaris Hildenborough J. Bacteriol. 189 2007 6159 6167
143. F.M.A. Valente, C.C. Almeida, I. Pacheco, J. Carita, L.M. Saraiva, and I.A.C. Pereira Selenium is involved in regulation of periplasmic hydrogenase gene expression in Desulfovibrio vulgaris Hildenborough J. Bacteriol. 188 2006 3228 3235
144. S.M. da Silva, C. Pimentel, F.M.A. Valente, C. Rodrigues-Pousada, and I.A.C. Pereira Tungsten and molybdenum regulation of formate dehydrogenase expression in Desulfovibrio vulgaris Hildenborough J. Bacteriol. 193 2011 2909 2916
145. 3 J. Biol. Inorg. Chem. 12 2007 1 10
146. A.V. Xavier Thermodynamic and choreographic constraints for energy transduction by cytochrome c oxidase Biochim. Biophys. Acta 1658 2004 23 30
147. I.A.C. Pereira, M. Teixeira, and A.V. Xavier Hemeproteins in anaerobes Struct. Bond. 91 1998 65 89
148. P.M. Matias, A.V. Coelho, F.M.A. Valente, P.D., J. LeGall, A.V. Xavier, I.A.C. Pereira, and M.A. Carrondo Sulfate respiration in Desulfovibrio vulgaris Hildenborough: structure of the 16-heme cytochrome c HmcA at 2.5 A resolution and a view of its role in transmembrane electron transfer J. Biol. Chem. 277 2002 47907 47916
149. P.M. Matias, R. Coelho, I.A.C. Pereira, A.V. Coelho, A.W. Thompson, L.C. Sieker, J.L. Gall, and M.A. Carrondo The primary and three-dimensional structures of a nine-haem cytochrome c from Desulfovibrio desulfuricans ATCC 27774 reveal a new member of the Hmc family Structure 7 1999 119 130
150. 3 complex: an electron transfer link in the hydrogen-sulfate reduction pathway J. Mol. Biol. 354 2005 73 90
151. 3 from Desulfovibrio vulgaris Hildenborough Chembiochem 2 2001 895 905
152. 3 from Desulfovibrio africanus J. Mol. Biol. 290 1999 881 902
153. 3 from Desulfuromonas acetoxidans Eur. J. Biochem. 269 2002 5722 5730
154. L. Morgado, M. Bruix, M. Pessanha, Y.Y. Londer, and C.A. Salgueiro Thermodynamic characterization of a triheme cytochrome family from Geobacter sulfurreducens reveals mechanistic and functional diversity Biophys. J. 99 2010 293 301
155. S.S. Venceslau, R.R. Lino, and I.A.C. Pereira The Qrc membrane complex, related to the alternative complex III, is a menaquinone reductase involved in sulfate respiration J. Biol. Chem. 285 2010 22774 22783
156. G. Voordouw Carbon monoxide cycling by Desulfovibrio vulgaris Hildenborough J. Bacteriol. 184 2002 5903 5911
157. S.H. Thomas, R.D. Wagner, A.K. Arakaki, J. Skolnick, J.R. Kirby, L.J. Shimkets, R.A. Sanford, and F.E. Loffler The mosaic genome of Anaeromyxobacter dehalogenans strain 2CP-C suggests an aerobic common ancestor to the delta-proteobacteria PLoS One 3 2008 e2103
158. A. Esteve-Nunez, J. Sosnik, P. Visconti, and D.R. Lovley Fluorescent properties of c-type cytochromes reveal their potential role as an extracytoplasmic electron sink in Geobacter sulfurreducens Environ. Microbiol. 10 2008 497 505
159. 2-utilizing methanogenic bacteria Appl. Environ. Microbiol. 33 1977 1162 1169
160. K.L. Hillesland, and D.A. Stahl Rapid evolution of stability and productivity at the origin of a microbial mutualism Proc. Natl. Acad. Sci. 107 2010 2124 2129
161. C.M. Plugge, W. Zhang, J.C. Scholten, and A.J. Stams Metabolic flexibility of sulfate-reducing bacteria Front. Microbiol. 2 2011 81
162. J. Leloup, H. Fossing, K. Kohls, L. Holmkvist, C. Borowski, and B.B. Jorgensen Sulfate-reducing bacteria in marine sediment (Aarhus Bay, Denmark): abundance and diversity related to geochemical zonation Environ. Microbiol. 11 2009 1278 1291
163. 2 oxidation in Desulfovibrio desulfuricans G20 J. Bacteriol. 191 2009 2675 2682
164. X. Gao, Y. Xin, and R.E. Blankenship Enzymatic activity of the alternative complex III as a menaquinol:auracyanin oxidoreductase in the electron transfer chain of Chloroflexus aurantiacus FEBS Lett. 583 2009 3275 3279
165. M.M. Pereira, P.N. Refojo, G.O. Hreggvidsson, S. Hjorleifsdottir, and M. Teixeira The alternative complex III from Rhodothermus marinus - a prototype of a new family of quinol:electron acceptor oxidoreductases FEBS Lett. 581 2007 4831 4835
166. M.F. Yanyushin, M.C. del Rosario, D.C. Brune, and R.E. Blankenship New class of bacterial membrane oxidoreductases Biochemistry 44 2005 10037 10045
167. L.A. Sazanov, and P. Hinchliffe Structure of the hydrophilic domain of respiratory complex I from Thermus thermophilus Science 311 2006 1430 1436
168. 3 FEBS Lett. 585 2011 2177 2181
169. 2 by Desulfovibrio alaskensis G20 during syntrophic growth on lactate Microbiology 157 2011 2912 2921
170. C.B. Walker, Z.L. He, Z.K. Yang, J.A. Ringbauer, Q. He, J.H. Zhou, G. Voordouw, J.D. Wall, A.P. Arkin, T.C. Hazen, S. Stolyar, and D.A. Stahl The electron transfer system of syntrophically grown Desulfovibrio vulgaris J. Bacteriol. 191 2009 5793 5801
171. M. Rossi, W.B.R. Pollock, M.W. Reij, R.G. Keon, R. Fu, and G. Voordouw The hmc operon of Desulfovibrio vulgaris subsp. vulgaris Hildenborough encodes a potential transmembrane redox protein complex J. Bacteriol. 175 1993 4699 4711
172. I.A.C. Pereira, C.V. Romão, A.V. Xavier, J. LeGall, and M. Teixeira Electron transfer between hydrogenases and mono and multiheme cytochromes in Desulfovibrio spp. J. Biol. Inorg. Chem. 3 1998 494 498
173. A. Dolla, B.K.J. Pohorelic, J.K. Voordouw, and G. Voordouw Deletion of the hmc operon of Desulfovibrio vulgaris subsp. vulgaris Hildenborough hampers hydrogen metabolism and low-redox-potential niche establishment Arch. Microbiol. 174 2000 143 151
174. R.G. Keon, R. Fu, and G. Voordouw Deletion of two downstream genes alters expression of the hmc operon of Desulfovibrio vulgaris subsp. vulgaris Hildenborough Arch. Microbiol. 167 1997 376 383
175. P.M. Pereira, Q. He, F.M.A. Valente, A.V. Xavier, J.Z. Zhou, I.A.C. Pereira, and R.O. Louro Energy metabolism in Desulfovibrio vulgaris Hildenborough: insights from transcriptome analysis Antonie Van Leeuwenhoek 93 2008 347 362
176. 2 activation J. Mol. Microbiol. Biotechnol. 10 2005 92 104
177. P.M. Pereira, M. Teixeira, A.V. Xavier, R.O. Louro, and I.A.C. Pereira The Tmc complex from Desulfovibrio vulgaris Hildenborough is involved in transmembrane electron transfer from periplasmic hydrogen oxidation Biochemistry 45 2006 10359 10367
178. F.M.A. Valente, A.S.F. Oliveira, N. Gnadt, I. Pacheco, A.V. Coelho, A.V. Xavier, M. Teixeira, C.M. Soares, and I.A.C. Pereira Hydrogenases in Desulfovibrio vulgaris Hildenborough: structural and physiologic characterisation of the membrane-bound [NiFeSe] hydrogenase J. Biol. Inorg. Chem. 10 2005 667 682
179. A.V. Callaghan, B.E.L. Morris, I.A.C. Pereira, M.J. McInerney, R.N. Austin, J.T. Groves, J.J. Kukor, J.M. Suflita, L.Y. Young, G.J. Zylstra, and B. Wawrik The genome sequence of Desulfatibacillum alkenivorans AK-01: a blueprint for anaerobic alkane oxidation Environ. Microbiol. 14 2012 101 113
180. A.W. Strittmatter, H. Liesegang, R. Rabus, I. Decker, J. Amann, S. Andres, A. Henne, W.F. Fricke, R. Martinez-Arias, D. Bartels, A. Goesmann, L. Krause, A. Puhler, H.P. Klenk, M. Richter, M. Schuler, F.O. Glockner, A. Meyerdierks, G. Gottschalk, and R. Amann Genome sequence of Desulfobacterium autotrophicum HRM2, a marine sulfate reducer oxidizing organic carbon completely to carbon dioxide Environ. Microbiol. 11 2009 1038 1055
181. H.P. Klenk, R.A. Clayton, J.F. Tomb, O. White, K.E. Nelson, K.A. Ketchum, R.J. Dodson, M. Gwinn, E.K. Hickey, J.D. Peterson, D.L. Richardson, A.R. Kerlavage, D.E. Graham, N.C. Kyrpides, R.D. Fleischmann, J. Quackenbush, N.H. Lee, G.G. Sutton, S. Gill, E.F. Kirkness, B.A. Dougherty, K. McKenney, M.D. Adams, B. Loftus, and J.C. Venter The complete genome sequence of the hyperthermophilic, sulphate-reducing archaeon Archaeoglobus fulgidus Nature 390 1997 364 370
182. S. Spring, A. Lapidus, M. Schroder, D. Gleim, D. Sims, L. Meincke, T.G. Del Rio, H. Tice, A. Copeland, J.F. Cheng, S. Lucas, F. Chen, M. Nolan, D. Bruce, L. Goodwin, S. Pitluck, N. Ivanova, K. Mavromatis, N. Mikhailova, A. Pati, A. Chen, K. Palaniappan, M. Land, L. Hauser, Y.J. Chang, C.D. Jeffries, P. Chain, E. Saunders, T. Brettin, J.C. Detter, M. Goker, J. Bristow, J.A. Eisen, V. Markowitz, P. Hugenholtz, N.C. Kyrpides, H.P. Klenk, and C. Han Complete genome sequence of Desulfotomaculum acetoxidans type strain (5575(T)) Stand. Genomic Sci. 1 2009 242 252
183. E. Pierce, G. Xie, R.D. Barabote, E. Saunders, C.S. Han, J.C. Detter, P. Richardson, T.S. Brettin, A. Das, L.G. Ljungdahl, and S.W. Ragsdale The complete genome sequence of Moorella thermoacetica (f. Clostridium thermoaceticum) Environ. Microbiol. 10 2008 2550 2573
184. T. Ide, S. Baumer, and U. Deppenmeier Energy conservation by the H2: heterodisulfide oxidoreductase from Methanosarcina mazei Go1: identification of two proton-translocating segments J. Bacteriol. 181 1999 4076 4080
185. J.W. Kung, C. Loffler, K. Dorner, D. Heintz, S. Gallien, A. Van Dorsselaer, T. Friedrich, and M. Boll Identification and characterization of the tungsten-containing class of benzoyl-coenzyme A reductases Proc. Natl. Acad. Sci. 106 2009 17687 17692
186. C. Loffler, K. Kuntze, J.R. Vazquez, A. Rugor, J.W. Kung, A. Bottcher, and M. Boll Occurrence, genes and expression of the W/Se-containing class II benzoyl-coenzyme A reductases in anaerobic bacteria Environ. Microbiol. 13 2011 696 709
187. S. Wischgoll, D. Heintz, F. Peters, A. Erxleben, E. Sarnighausen, R. Reski, A. Van Dorsselaer, and M. Boll Gene clusters involved in anaerobic benzoate degradation of Geobacter metallireducens Mol. Microbiol. 58 2005 1238 1252
188. N. Hamann, G.J. Mander, J.E. Shokes, R.A. Scott, M. Bennati, and R. Hedderich Cysteine-rich CCG domain contains a novel [4Fe4S] cluster binding motif as deduced from studies with subunit B of heterodisulfide reductase from Methanothermobacter marburgensis Biochemistry 46 2007 12875 12885
189. S.T. Cole, K. Eiglmeier, S. Ahmed, N. Honore, L. Elmes, W.F. Anderson, and J.H. Weiner Nucleotide-sequence and gene-polypeptide relationships of the glpABC operon encoding the anaerobic Sn-glycerol-3-phosphate dehydrogenase of Escherichia coli K12 J. Bacteriol. 170 1988 2448 2456
190. N. Hamann, E. Bill, J.E. Shokes, R.A. Scott, M. Bennati, and R. Hedderich The CCG-domain-containing subunit SdhE of succinate:quinone oxidoreductase from Sulfolobus solfataricus P2 binds a [4Fe4S] cluster J. Biol. Inorg. Chem. 14 2009 457 470
191. R.S. Lemos, A.S. Fernandes, M.M. Pereira, C.M. Gomes, and M. Teixeira Quinol:fumarate oxidoreductases and succinate:quinone oxidoreductases: phylogenetic relationships, metal centres and membrane attachment Biochim. Biophys. Acta 1553 2002 158 170
192. S. Heim, A. Künkel, R.K. Thauer, and R. Hedderich Thiol:fumarate reductase (Tfr) from Methanobacterium thermoautotrophicum - identification of the catalytic sites for fumarate reduction and thiol oxidation Eur. J. Biochem. 253 1998 292 299
193. Y.R. Chai, R. Kolter, and R. Losick A widely conserved gene cluster required for lactate utilization in Bacillus subtilis and its involvement in biofilm formation J. Bacteriol. 191 2009 2423 2430
194. G.E. Pinchuk, D.A. Rodionov, C. Yang, X.Q. Li, A.L. Osterman, E. Dervyn, O.V. Geydebrekht, S.B. Reed, M.F. Romine, F.R. Collart, J.H. Scott, J.K. Fredrickson, and A.S. Beliaev Genomic reconstruction of Shewanella oneidensis MR-1 metabolism reveals a previously uncharacterized machinery for lactate utilization Proc. Natl. Acad. Sci. 106 2009 2874 2879
195. M.T. Thomas, M. Shepherd, R.K. Poole, A.H. van Vliet, D.J. Kelly, and B.M. Pearson Two respiratory enzyme systems in Campylobacter jejuni NCTC 11168 contribute to growth on l-lactate Environ. Microbiol. 13 2011 48 61
196. H. Ogata, P. Kellers, and W. Lubitz The crystal structure of the [NiFe] hydrogenase from the photosynthetic bacterium Allochromatium vinosum: characterization of the oxidized enzyme (Ni-A state) J. Mol. Biol. 402 2010 428 444
197. L.S. Palagyi-Meszaros, J. Maroti, D. Latinovics, T. Balogh, E. Klement, K.F. Medzihradszky, G. Rakhely, and K.L. Kovacs Electron-transfer subunits of the NiFe hydrogenases in Thiocapsa roseopersicina BBS FEBS J. 276 2009 164 174