Sulphate respiration from hydrogen in Desulfovibrio bacteria: A structural biology overview

Progress in Biophysics and Molecular Biology

Volumn 89, Issue 3, 2005, Pages 292-329

  Matias, Pedro M ^a   Pereira, Inês A C ^a   Soares, Cláudio M ^a   Carrondo, Maria Arménia ^a  

^a INSTITUTO DE TECNOLOGIA QUÍMICA E BIOLÓGICA   (Portugal)

Author keywords

Desulfovibrio bacteria; Electron transfer; Hydrogen metabolism; Sulphate respiration

Indexed keywords

CYTOCHROME; HYDROGEN; OXYGEN; SULFATE;

BACTERIAL PHENOMENA AND FUNCTIONS; BIOLOGICAL MODEL; BIOPHYSICS; CHEMICAL STRUCTURE; CHEMISTRY; DESULFOVIBRIO; ELECTRON; ELECTRON TRANSPORT; KINETICS; METABOLISM; METHODOLOGY; OXIDATION REDUCTION REACTION; PROTEIN CONFORMATION; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; REVIEW;

BACTERIAL PHYSIOLOGY; BIOPHYSICS; CYTOCHROMES; DESULFOVIBRIO; ELECTRON TRANSPORT; ELECTRONS; HYDROGEN; KINETICS; MODELS, BIOLOGICAL; MODELS, MOLECULAR; OXIDATION-REDUCTION; OXYGEN; PROTEIN CONFORMATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SULFATES;

ANIMALIA; BACTERIA (MICROORGANISMS); DESULFOVIBRIO;

EID: 20444385906     PISSN: 00796107     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbiomolbio.2004.11.003     Document Type: Review

References (156)

1. J.M. Akagi Respiratory sulfate reduction L.L. Barton Sulfate-Reducing Bacteria 1995 Plenum Press New York 89 111
2. 3 (Mr=26,000) from Desulfovibrio desulfuricans Norway Biochemistry 37 1998 2120 2130
3. C. Aubert, M. Brugna, A. Dolla, M. Bruschi, and M.T. Giudici-Orticoni A sequential electron transfer from hydrogenases to cytochromes in sulfate-reducing bacteria Biochim. Biophys. Acta 1476 2000 85 92
4. 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
5. 3 using continuum electrostatics Biophys. J. 76 1999 2978 2998
6. D. Bashford An object-oriented programming suite for electrostatic effects in biological molecules. Scientific computing in object-oriented parallel environments I. Ishikawa R.R. Oldehoeft J.V.W. Reinders M. Tholburn Lecture Notes in Computer Science vol. 1343 1997 Springer Berlin 233 240
7. G.R. Bell, J.P. Lee, H.D. Peck Jr., and J.L. Gall Reactivity of Desulfovibrio gigas hydrogenase toward artificial and natural electron donors or acceptors Biochimie 60 1978 315 320
8. I. Bento, V.H. Teixeira, A.M. Baptista, C.M. Soares, P.M. Matias, and M.A. Carrondo Redox-Bohr and other cooperativity effects in the nine heme cytochrome c from Desulfovibrio desulfuricans ATCC 27774 crystallographic and modeling studies J. Biol. Chem. 278 2003 36455 36469
9. 3 from Desulfovibrio desulfuricans ATCC 27774 crystallographic and modelling studies of oxidised and reduced high resolution structures at pH 7.6 Proteins 54 2004 135 152
10. 3 Biochem. Biophys. Res. Commun. 189 1992 633 639
11. 553 from Desulfovibrio vulgaris studied by NMR spectroscopy and restrained molecular dynamics J. Mol. Biol. 245 1995 661 681
12. A. Brandis, and R.K. Thauer Growth of Desulfovibrio species on hydrogen and sulphate as sole energy source J. Gen. Microbiol. 126 1981 249 252
13. 3 from Desulfovibrio gigas solution structures of the oxidised and reduced states J. Mol. Biol. 298 2000 61 82
14. W. Brent, and G. Voordouw Cloning, sequencing and expression of the gene encoding the high-molecular-weight cytochrome c from Desulfovibrio vulgaris Hildenborough J. Bacteriol. 173 1991 220 228
15. 3 and Fe-only hydrogenase from Desulfovibrio vulgaris Hildenborough Proteins 33 1998 590 600
16. r 26,000) isolated from sulfate-reducing bacteria and its relationship to other polyhemic cytochromes from Desulfovibrio Methods Enzymol. 243 1994 140 155
17. M. Bruschi, P. Bertrand, C. More, G. Leroy, J. Bonicel, J. Haladjian, G. Chottard, W.B. Pollock, and G. Voordouw Biochemical and spectroscopic characterization of the high molecular weight cytochrome c from Desulfovibrio vulgaris Hildenborough expressed in Desulfovibrio desulfuricans G200 Biochemistry 31 1992 3281 3288
18. L. Chen, M.M. Pereira, M. Teixeira, A.V. Xavier, and J. LeGall Isolation and characterization of a high molecular weight cytochrome from the sulfate reducing bacterium Desulfovibrio gigas FEBS Lett. 347 1994 295 299
19. A.V. Coelho, P.M. Matias, L.C. Sieker, J. Morais, M.A. Carrondo, J. Lampreia, C. Costa, J.J.G. Moura, I. Moura, and J. LeGall Preliminary crystallographic analysis and further characterization of a dodecaheme cytochrome c from Desulfovibrio desulfuricans ATCC 27774 Acta Crystallogr. D 52 1996 1202 1209
20. 3 fro Desulfovibrio gigas Eur. J. Biochem. 202 1991 1101 1106
21. P.B. Crowley, and M.A. Carrondo The architecture of the binding site in redox protein complexes implications for fast dissociation Proteins: Structure, Function and Bioinformatics 55 2004 603 612
22. P.B. Crowley, G. Otting, B.G. Schlarb-Ridley, G.W. Canters, and M. Ubbink Hydrophobic interactions in a cyanobacterial plastocyanin-cytochrome f complex J. Am. Chem. Soc. 123 2001 10444 10453
23. 6 and cytochrome f, characterized by NMR J. Biol. Chem. 277 2002 48685 48689
24. P.B. Crowley, K.S. Rabe, J.A.R. Worrall, G.W. Canters, and M. Ubbink The ternary complex of cytochrome f and cytochrome c identification of a second binding site and competition for plastocyanin binding ChemBioChem 3 2002 526 533
25. C.A. Cunha, M.J. Romão, S.J. Sadeghi, F. Valetti, G. Gilardi, and C.M. Soares Modelling of electron transfer complexes between flavodoxin and c-type cytochromes J. Biol. Inorg. Chem. 4 1999 360 374
26. 3 from Desulfovibrio desulfuricans Norway at 1.7 Å resolution J. Mol. Biol. 243 1994 653 667
27. r 26,000) from Desulfovibrio desulfuricans Norway Structure 4 1996 395 404
28. 3 Structure 10 2002 1677 1686
29. 3 from Desulfovibrio gigas Biochim. Biophys. Acta 1492 2000 271 275
30. W.L. DeLano The PyMOL Molecular Graphics System 2002 DeLano Scientific San Carlos, CA, USA
31. H.T. Dinh, J. Kuever, M. Mussmann, A.W. Hassel, M. Stratmann, and F. Widdel Iron corrosion by novel anaerobic microorganisms Nature 427 2004 829 832
32. 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
33. E.C. Duin, C. Bauer, B. Jaun, and R. Hedderich Coenzyme M binds to a [4Fe-4S] cluster in the active site of heterodisulfide reductase as deduced from EPR studies with the [33S]coenzyme M-treated enzyme FEBS Lett. 538 2003 81 84
34. 3 from Desulfovibrio desulfuricans Essex 6 Eur. J. Biochem. 268 2001 3028 3035
35. 3-[Fe]-hydrogenase electron-transfer complex structural model by NMR restrained docking FEBS Lett. 548 2003 1 4
36. G. Fauque, H.D. Peck Jr., J.J. Moura, B.H. Huynh, Y. Berlier, D.V. DerVartanian, M. Teixeira, A.E. Przybyla, P.A. Lespinat, and I. Moura The three classes of hydrogenases from sulfate-reducing bacteria of the genus Desulfovibrio FEMS Microbiol. Rev. 4 1988 299 344
37. 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
38. 3 from Desulfovibrio gigas containing disulfide bridges J. Biol. Inorg. Chem. 4 1999 162 165
39. E. Garcin, X. Vernede, E.C. Hatchikian, A. Volbeda, M. Frey, and J.C. Fontecilla-Camps The crystal structure of a reduced [NiFeSe] hydrogenase provides an image of the activated catalytic center Structure 7 1999 557 566
40. J. Gibson, and S.H. C Metabolic diversity in aromatic compound utilization by anaerobic microbes Annu. Rev. Microbiol. 56 2002 345 369
41. D.S. Goodsell, and A.J. Olson Automated docking of substrates to proteins by simulated annealing Proteins 8 1990 195 202
42. D.S. Goodsell, H. Lauble, C.D. Stout, and A.J. Olson Automated docking in crystallography analysis of the substrates of aconitase Proteins 17 1993 1 10
43. F. Guerlesquin, A. Dolla, and M. Bruschi Involvement of electrostatic interactions in cytochrome c complex formation Biochimie 76 1994 515 523
44. R.D. Guiles, S. Sarma, R.J. DiGate, D. Banville, V.J. Basus, I.D. Kuntz, and L. Waskell Pseudocontact shifts used in the restraint of the solution structures of electron transfer complexes Nat. Struct. Biol. 3 1996 333 339
45. 3 and hydrogenase from Desulfovibrio desulfuricans Norway Biochem. Biophys. Res. Commun. 147 1987 1289 1294
46. 3 (Mr 26,000) and the hydrogenase from Desulfovibrio desulfuricans Norway Biochem. Biophys. Res. Commun. 179 1991 605 610
47. P.C. Hallenbeck, and J.R. Benemann Biological hydrogen production; fundamentals and limiting processes Int. J. Hydrogen Energy 27 2002 1185 1193
48. W.A. Hamilton Bioenergetics of sulphate-reducing bacteria in relation to their environmental impact Biodegradation 9 1998 201 212
49. W.A. Hamilton Microbially influenced corrosion as a model system for the study of metal microbe interactions a unifying electron transfer hypothesis Biofouling 19 2003 65 76
50. R.P. Happe, W. Rosenboom, A.J. Pierik, S.P.J. Albracht, and K. Bagley Biological activation of hydrogen Nature 385 1997 126
51. 3 from D. vulgaris Miyazaki F on the basis of its reduced solution structure J. Mol. Biol. 319 2002 767 778
52. 3 Nature 282 1979 806 810
53. 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
54. 3 at 1.8 Å J. Mol. Biol. 172 1984 109 139
55. Y. Higuchi, K. Inaka, N. Yasuoka, and T. Yagi Isolation and crystallization of high molecular weight cytochrome from Desulfovibrio vulgaris Hildenborough Biochem. Biophys. Acta 911 1987 341 348
56. Y. Higuchi, T. Yagi, and N. Yasuoka Unusual ligand structure in Ni-Fe active center and an additional Mg site in hydrogenase revealed by high resolution X-ray structure analysis Structure 5 1997 1671 1680
57. 2, as revealed by X-ray structure analysis at 1.4 Å resolution Structure 7 1999 549 556
58. 554 from Nitrosomonas europaea J. Biol. Inorg. Chem. 6 2001 390 397
59. V.C. Kalia, S. Lal, R. Ghai, M. Mandal, and A. Chauhan Mining genomic databases to identify novel hydrogen producers Trends Biotechnol. 21 2003 152 156
60. R.G. Keon, and G. Voordouw Identification of the HmcF and topology of the HmcB subunit of the Hmc complex of Desulfovibrio vulgaris Anaerobe 2 1996 231
61. 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
62. L. Krippahl, J.J. Moura, and P.N. Palma Modeling protein complexes with BiGGER Proteins 52 2003 19 23
63. M.-C. Liu, C. Costa, I.B. Coutinho, J.J.G. Moura, I. Moura, A.V. Xavier, and J. LeGall Cytochrome components of nitrate- and sulfate-respiring Desulfovibrio desulfuricans ATCC 27774 J. Bacteriol. 170 1988 5545 5551
64. J.R. Lloyd Microbial reduction of metals and radionuclides FEMS Microbiol. Rev. 27 2003 411 425
65. L. Lo Conte, C. Chothia, and J. Janin The atomic structure of protein-protein recognition sites J. Mol. Biol. 285 1999 2177 2198
66. J. Loubinoux, J.-P. Bronowicki, I.A.C. Pereira, J.-L. Mougenel, and A.E. Le Faou Sulfate-reducing bacteria in human feces and their association with inflammatory bowel diseases FEMS Microbiol. Lett. 40 2002 107 112
67. 3 from Desulfovibrio vulgaris a model for energy transduction mechanisms J. Biol. Inorg. Chem. 1 1996 34 38
68. 1H-NMR FEBS Lett. 390 1996 59 62
69. 3 coupled to hydrogenase works as a 'proton thruster' in Desulfovibrio vulgaris J. Biol. Inorg. Chem. 2 1997 488 491
70. 3 coupled to hydrogenase works as a "proton thruster" in Desulfovibrio vulgaris J. Biol. Inorg. Chem. 2 1997 488 491
71. 3 from Desulfovibrio gigas thermodynamics of a "proton thruster" Biochemistry 37 1998 15808 15815
72. R.O. Louro, I. Bento, P.M. Matias, T. Catarino, A.M. Baptista, C.M. Soares, M.A. Carrondo, D.L. Turner, and A.V. Xavier Conformational component in the coupled transfer of multiple electrons and protons in a monomeric tetraheme cytochrome J. Biol. Chem. 276 2001 44044 44051
73. 3 the importance of mechano-chemical coupling for energy transduction ChemBioChem 2 2001 831 837
74. D.R. Lovley Cleaning up with genomics applying molecular biology to bioremediation Nat. Rev. Microbiol. 1 2003 35 44
75. E.J. Lyon, S. Shima, G. Buurman, S. Chowdhuri, A. Batschauer, K. Steinbach, and R.K. Thauer UV-A/blue-light inactivation of the 'metal-free' hydrogenase (Hmd) from methanogenic archaea Eur. J. Biochem. 271 2004 195 204
76. 3 from Desulfovibrio africanus nucleotide sequences, EPR spectroscopy and biological activity Biochim. Biophys. Acta 1342 1997 149 163
77. 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
78. J. Maroc, R. Azerad, M.D. Kamen, and J. LeGall Menaquinone (MK-6) in the sulfate reducing obligate anaerobe, Desulfovibrio Biochim. Biophys. Acta 197 1970 87 89
79. 3 from Desulfovibrio species using continuum electrostatic methods J. Biol. Inorg. Chem. 4 1999 73 86
80. 3 from Desulfovibrio vulgaris Hildenborough at 1.9 Å resolution J. Mol. Biol. 234 1993 680 699
81. 3 from Desulfovibrio gigas crystal structure at 1.8 Å resolution and evidence for a specific calcium-binding site Prot. Sci. 5 1996 1342 1354
82. P.M. Matias, R. Coelho, I.A.C. Pereira, A.V. Coelho, A.W. Thompson, L.C. Sieker, J. LeGall, 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
83. 3 J. Biol. Inorg. Chem. 4 1999 478 494
84. 3 J. Biol. Inorg. Chem. 6 2001 63 81
85. 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 Å resolution and a view of its role in transmembrane electron transfer J. Biol. Chem. 277 2002 47907 47916
86. 3 structural basis for functional cooperativity J. Mol. Biol. 281 1998 719 739
87. 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. USA 99 2002 5632 5637
88. Y. Montet, P. Amara, A. Volbeda, X. Vernede, E.C. Hatchikian, M.J. Field, M. Frey, and J.C. Fontecilla-Camps Gas access to the active site of Ni-Fe hydrogenases probed by X-ray crystallography and molecular dynamics Nat. Struct. Biol. 4 1997 523 526
89. J. Morais, P.N. Palma, C. Frazão, J. Caldeira, J. LeGall, I. Moura, J.J.G. Moura, and M.A. Carrondo Structure of the tetraheme cytochrome from Desulfovibrio desulfuricans ATCC 27774 X-ray diffraction and electron paramagnetic resonance studies Biochemistry 34 1995 12830 12841
90. 553 complex combining TROSY experiments and soft docking calculations J. Biol. Chem. 275 2000 23204 23210
91. 553-ferredoxin complex Biochemistry 39 2000 2530 2537
92. 3 from Desulfovibrio vulgaris Hildenborough at 2 Å resolution J. Biochem. (Tokyo) 110 1991 532 540
93. A. Nakagawa, Y. Higuchi, N. Yasuoka, Y. Katsube, and T. Yagi S-class cytochromes c have a variety of folding patterns structure of cytochrome c-553 from Desulfovibrio vulgaris determined by the multi-wavelength anomalous dispersion method J. Biochem. (Tokyo) 108 1990 701 703
94. Y. Nicolet, C. Piras, P. Legrand, C.E. Hatchikian, and J.C. Fontecilla-Camps Desulfovibrio desulfuricans iron hydrogenase the structure shows unusual coordination to an active site Fe binuclear center Struct. Fold. Des. 7 1999 13 23
95. Y. Nicolet, A.L. de Lacey, X. Vernede, V.M. Fernandez, E.C. Hatchikian, and J.C. Fontecilla-Camps Crystallographic and FTIR spectroscopic evidence of changes in Fe coordination upon reduction of the active site of the Fe-only hydrogenase from Desulfovibrio desulfuricans J. Am. Chem. Soc. 123 2001 1596 1601
96. 3 Biochim. Biophys. Acta 935 1988 34 40
97. 3 from Desulfovibrio africanus J. Mol. Biol. 290 1999 881 902
98. 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
99. 3 (Hmc) isolated from Desulfovibrio vulgaris Miyazaki Biochimie 75 1993 977 983
100. H. Ogata, Y. Mizoguchi, N. Mizuno, K. Miki, S. Adachi, N. Yasuoka, T. Yagi, O. Yamauchi, S. Hirota, and Y.m. Higuchi Structural studies of the carbon monoxide complex of [NiFe] hydrogenase from Desulfovibrio vulgaris Miyazaki F suggestion for the initial activation site for dihydrogen J. Am. Chem. Soc. 124 2002 11628 11635
101. P.N. Palma, L. Krippahl, J.E. Wampler, and J.J.G. Moura BiGGER a new (soft) docking algorithm for predicting protein interactions Proteins 39 2000 372 384
102. S. Papa, F. Guerrieri, and G. Izzo Redox Bohr-effects in the cytochrome system of mitochondria FEBS Lett. 105 1979 213 216
103. I.A.C. Pereira, J. LeGall, A.V. Xavier, and M. Teixeira The membrane-bound high molecular weight cytochromes c from Desulfovibrio gigas and Desulfovibrio vulgaris Hildenborough EPR and Mössbauer studies J. Biol. Inorg. Chem. 2 1997 23 31
104. 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
105. I.A.C. Pereira, M. Teixeira, and A.V. Xavier Hemeproteins in Anaerobes Struct. Bond. 91 1998 65 89
106. I.A. Pereira, J. LeGall, A.V. Xavier, and M. Teixeira Characterization of a heme c nitrite reductase from a non-ammonifying microorganism, Desulfovibrio vulgaris Hildenborough Biochim. Biophys. Acta 1481 2000 119 130
107. 3 from Desulfovibrio africanus a novel function in a familiar heme core J. Biol. Inorg. Chem. 7 2002 815 822
108. J.W. Peters, W.N. Lanzilotta, B.J. Lemon, and L.C. Seefeldt X-ray crystal structure of the Fe-only hydrogenase (CpI) from Clostridium pasteurianum to 1.8 angstrom resolution Science 282 1998 1853 1858
109. Philippsen, A., 2002. DINO: visualizing structural biology, http://www.dino3d.org.
110. A.J. Pierik, M. Hulstein, W.R. Hagen, and S.P. Albracht A low-spin iron with CN and CO as intrinsic ligands forms the core of the active site in [Fe]-hydrogenases Eur. J. Biochem. 258 1998 572 578
111. 3 with different specificity Biochem. Biophys. Acta 1273 1996 51 61
112. R.H. Pires, A.I. Lourenço, 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
113. M.C. Pitcher, and J.H. Cummings Hydrogen sulphide a bacterial toxin in ulcerative colitis? Gut 39 1996 1 4
114. W.B. Pollock, M. Loutfi, M. Bruschi, B.J. Rapp-Giles, J.D. Wall, and G. Voordouw Cloning, sequencing, and expression of the gene encoding the high-molecular-weight cytochrome c from Desulfovibrio vulgaris Hildenborough J. Bacteriol. 173 1991 220 228
115. J.R. Postgate The Sulphate-Reducing Bacteria 1984 Cambridge University Press Cambridge
116. R. Rabus, T. Hansen, and F. Widdel Dissimilatory sulfate- and sulfur-reducing prokaryotes M.E.A. Dworkin The Prokaryotes An Evolving Electronic Resource for the Microbiological Community 2000 Springer New York http://link.springer-ny.com/link/service/books/10125/
117. C. Reis, R.O. Louro, I. Pacheco, T. Catarino, D.L. Turner, and A.V. Xavier Redox-Bohr effect in the nine haem cytochrome from Desulfovibrio desulfuricans 27774 Inorg. Chim. Acta 339 2002 248 252
118. R. Rodrigues, F.M. Valente, I.A. Pereira, S. Oliveira, and C. Rodrigues-Pousada A novel membrane-bound Ech [NiFe] hydrogenase in Desulfovibrio gigas Biochem. Biophys. Res. Commun. 306 2003 366 375
119. W.E. Roediger, J. Moore, and W. Babidge Colonic sulfide in pathogenesis and treatment of ulcerative colitis Dig. Dis. Sci. 42 1997 1571 1579
120. C.V. Romão, I.A. Pereira, A.V. Xavier, J. LeGall, and M. Teixeira Characterization of the [NiFe] hydrogenase from the sulfate reducer Desulfovibrio vulgaris Hildenborough Biochem. Biophys. Res. Commun. 240 1997 75 79
121. 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
122. M. Rousset, Y. Montet, B. Guigliarelli, N. Forget, M. Asso, P. Bertrand, J.C. Fontecilla-Camps, and E.C.m. Hatchikian [3F3-4S] to [4Fe-4S] cluster convertion in Desulfovibrio fructosovorans [NiFe] hydrogenase by site-directed mutagenesis Proc. Natl. Acad. Sci. USA 95 1998 11625 11630
123. 3 by 2D-NMR FEBS Lett. 314 1992 155 158
124. 3 J. Biol. Inorg. Chem. 2 1997 343 349
125. M.F. Sanner, A.J. Olson, and J.C. Spehner Reduced surface an efficient way to compute molecular surfaces Biopolymers 38 1996 305 320
126. 3 Eur. J. Biochem. 141 1984 283 296
127. L.M. Saraiva, P.N. da Costa, and J. LeGall Sequencing the gene encoding Desulfovibrio desulfuricans ATCC 27774 nine-heme cytochrome c Biochem. Biophys. Res. Commun. 262 1999 629 634
128. L.M. Saraiva, P.N. da Costa, C. Conte, A.V. Xavier, and J. LeGall In the facultative sulphate/nitrate reducer Desulfovibrio desulfuricans ATCC 27774, the nine-heme cytochrome c is part of a membrane-bound redox complex mainly expressed in sulphate-grown cells Biochim. Biophys. Acta 1520 2001 63 70
129. 2-metabolizing prokaryotes M.E.A. Dworkin The Prokaryotes An Evolving Electronic Resource for the Microbiological Community 2003 Springer New York http://link.springer-ny.com/ link/service/books/10125/
130. 3 from Desulfovibrio vulgaris Hildenborough at 1.67 å resolution and from Desulfovibrio desulfuricans ATCC 27774 at 1.6 Å resolution Inorg. Chim. Acta. 273 1998 213 224
131. 3 from Desulfovibrio vulgaris Hildenborough J. Biol. Inorg. Chem. 2 1997 714 727
132. 3 haem-copper oxygen reductase J. Biol. Inorg. Chem. 9 2004 124 134
133. J.L. Steger, C. Vincent, J.D. Ballard, and L.R. Krumholz Desulfovibrio sp. Genes involved in the respiration of sulfate during metabolism of hydrogen and lactate Appl. Environ. Microbiol. 68 2002 1932 1937
134. V.H. Teixeira, C.M. Soares, and A.M. Baptista Studies of the reduction and protonation behaviour of tetrahaem cytochromes using atomic detail J. Biol. Inorg. Chem. 7 2002 200 216
135. 3 Biophys. J. 86 2004 2773 2785
136. 3 in energy production system Arch. Microbiol. 125 1980 35 42
137. 3 from Desulfovibrio vulgaris Biochim. Biophys. Acta 1187 1994 232 235
138. 3 from Desulfovibrio vulgaris Eur. J. Biochem. 241 1996 723 731
139. M. Ubbink, and D.S. Bendall Complex of plastocyanin and cytochrome c characterized by NMR chemical Shift analysis Biochemistry 36 1997 6326 6335
140. M. Ubbink, M. Ejdebäck, G. Karlsson, and D.S. Bendall The structure of the complex of plastocyanin and cytochrome f, determined by paramagnetic NMR and restrained rigid-body molecular dynamics Structure 6 1998 323 335
141. M. Ubbink, J.A.R. Worrall, G.W. Canters, E.J.J. Groenen, and M. Huber Paramagnetic resonance of biological metal centers Annu. Rev. Biophys. Biomol. Struct. 31 2002 393 422
142. S. Umhau, G. Fritz, K. Diederichs, J. Breed, W. Welte, and P.M. Kroneck Three-dimensional structure of the nonaheme cytochrome c from Desulfovibrio desulfuricans Essex in the Fe(III) state at 1.89 Å resolution Biochemistry 40 2001 1308 1316
143. 3 from Desulfovibrio vulgaris Hildenborough ChemBioChem 2 2001 895 905
144. M. Valls, and V. de Lorenzo Exploiting the genetic and biochemical capacities of bacteria for the remediation of heavy metal pollution FEMS Microbiol. Rev 26 2002 327 338
145. M.F.J.M. Verhagen, A.J. Pierik, R.B.G. Wolbert, L.F. Mallée, W.G.B. Voorhorst, and W.R. Hagen Axial coordination and reduction potentials of the sixteen hemes in high-molecular-mass cytochrome c from Desulfovibrio
146. 553 from Desulfovibrio vulgaris (Hildenborough). Electrochemical properties and electron transfer with hydrogenase Eur. J. Biochem. 221 1994 821 829
147. B.L. Victor, J.B. Vicente, R. Rodrigues, S. Oliveira, C. Rodrigues-Pousada, C. Frazão, C.M. Gomes, M. Teixeira, and C.M. Soares Docking and electron transfer studies between rubredoxin and rubredoxin oxygen oxidoreductase J. Biol. Inorg. Chem. 8 2003 475 488
148. P.M. Vignais, B. Billoud, and J. Meyer Classification and phylogeny of hydrogenases FEMS Microbiol. Rev. 25 2001 455 501
149. A. Volbeda, C. Piras, M.H. Charon, 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
150. A. Volbeda, Y. Montet, E.C. Hatchikian, and J.C. Fontecilla-Camps High-resolution crystallographic analysis of Desulfovibrio fructosovorans [NiFe] hydrogenase Int. J. Hydrogen Energy 27 2002 1449 1461
151. G. Voordouw Carbon monoxide cycling by Desulfovibrio vulgaris Hildenborough J. Bacteriol. 184 2002 5903 5911
152. G. Voordouw, V. Niviere, F.G. Ferris, P.M. Fedorak, and D.W.S. Westlake Distribution of hydrogenase genes in Desulfovibrio spp. and their use in identification of species from the oil field environment Appl. Environ. Microbiol 56 1990 3748 3754
153. A.V. Xavier Energy transduction coupling mechanisms in multiredox center proteins J. Inorg. Biochem. 28 1986 239 243
154. A.V. Xavier A mechano-chemical model for energy transduction in cytochrome c oxidase the work of a Maxwell's god FEBS Lett. 532 2002 261 266
155. T. Yagi Solubilization, purification and properties of particulate hydrogenase from Desulfovibrio vulgaris J. Biochem. (Tokyo) 68 1970 649 657
156. T. Yagi, M. Honya, and N. Tamiya Purification and properties of hydrogenase of different origins Biochim. Biophys. Acta 153 1968 699 705