The prokaryotic complex iron-sulfur molybdoenzyme family

Biochimica et Biophysica Acta - Biomembranes

Volumn 1778, Issue 9, 2008, Pages 1897-1929

  Rothery, Richard A ^a   Workun, Gregory J ^a   Weiner, Joel H ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Cell envelope; Formate dehydrogenase; Iron sulfur; Molybdenum cofactor; Nitrate reductase; Structural biology

Indexed keywords

BACTERIAL ENZYME; COMPLEX IRON SULFUR MOLYBDOENZYME; CUBANE DERIVATIVE; CYSTEINE DERIVATIVE; DIMER; GUANINE DERIVATIVE; MEMBRANE PROTEIN; MOLYBDOBIS(PYRANOPTERIN GUANINE DINUCLEOTIDE); MONOMER; OXIDOREDUCTASE; PEPTIDE DERIVATIVE; PROTEIN SUBUNIT; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); TRANSLOCON; UNCLASSIFIED DRUG;

BACTERIAL OUTER MEMBRANE; BIOINFORMATICS; CELL MEMBRANE; CELL MEMBRANE TRANSPORT; ENZYME ACTIVE SITE; ENZYME ANALYSIS; ENZYME STRUCTURE; ENZYME SUBUNIT; GENE SEQUENCE; MICROBIAL DIVERSITY; MOLECULAR EVOLUTION; MOLECULAR PHYLOGENY; NONHUMAN; PRIORITY JOURNAL; PROKARYOTE; PROTEIN TRANSPORT; RESPIRATORY CHAIN; REVIEW; STRUCTURE ANALYSIS;

AMINO ACID SEQUENCE; CATALYTIC DOMAIN; EVOLUTION; IRON-SULFUR PROTEINS; MEMBRANE PROTEINS; MODELS, BIOLOGICAL; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MOLYBDENUM; OXIDATION-REDUCTION; PERIPLASM; PHYLOGENY; PROKARYOTIC CELLS; PROTEIN SUBUNITS; SEQUENCE HOMOLOGY, AMINO ACID;

BACTERIA (MICROORGANISMS); PROKARYOTA;

EID: 50049103112     PISSN: 00052736     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamem.2007.09.002     Document Type: Review

References (184)

1. Sargent F. Constructing the wonders of the bacterial world: biosynthesis of complex enzymes. Microbiology 153 (2007) 633-651
2. Unden G., and Bongaerts J. Alternative respiratory pathways of Escherichia coli: energetics and transcriptional regulation in response to electron acceptors. Biochim. Biophys. Acta 1320 (1997) 217-234
3. Gennis R., and Stewart V. Respiration. In: Neidhardt F.C. (Ed). Escherichia coli and Salmonella: cellular and molecular biology vol. 1 (1996), ASM Press, Washington, D.C. 217-261
4. Richardson D.J. Bacterial respiration: a flexible process for a changing environment. Microbiology 146 (2000) 551-571
5. Jormakka M., Byrne B., and Iwata S. Protonmotive force generation by a redox loop mechanism. FEBS Lett. 545 (2003) 25-30
6. Jormakka M., Byrne B., and Iwata S. Formate dehydrogenase-a versatile enzyme in changing environments. Curr. Opin. Struck. Biol. 13 (2003) 418-423
7. Jormakka M., Richardson D., Byrne B., and Iwata S. Architecture of NarGH reveals a structural classification of Mo-bisMGD enzymes. Structure (Camb) 12 (2004) 95-104
8. Jormakka M., Tornroth S., Byrne B., and Iwata S. Molecular basis of proton motive force generation: structure of formate dehydrogenase-N. Science 295 (2002) 1863-1868
9. Bertero M.G., Rothery R.A., Palak M., Hou C., Lim D., Blasco F., Weiner J.H., and Strynadka N.C. Insights into the respiratory electron transfer pathway from the structure of nitrate reductase A. Nat. Struct. Biol. 10 (2003) 681-687
10. Weiner J.H., Bilous P.T., Shaw G.M., Lubitz S.P., Frost L., Thomas G.H., Cole J.A., and Turner R.J. A novel and ubiquitous system for membrane targeting and secretion of cofactor-containing proteins. Cell 93 (1998) 93-101
11. Berks B.C. A common export pathway for proteins binding complex redox cofactors?. Mol. Microbiol. 22 (1996) 393-414
12. Wu L.-F., Ize B., Chanal A., Quentin Y., and Fichant G. Bacterial twin-arginine signal peptide-dependent protein translocation pathway: evolution and mechanism. J. Mol. Microbiol. Biotechnol. 2 (2000) 179-189
13. Mitchell P. Possible molecular mechanisms of the protonmotive function of cytochrome systems. J. Theor. Biol. 62 (1976) 327-367
14. Schneider F., Löwe J., Huber R., Schindelin H., Kisker C., and Knäben J. Crystal structure of dimethyl sulfoxide reductase from Rhodobacter capsulatus at 1.88 Å resolution. J. Mol. Biol. 263 (1996) 53-69
15. Schindelin H., Kisker C., Hilton J., Rajagopalan K.V., and Rees D.C. Crystal structure of DMSO reductase: redox-linked changes in molybdopterin coordination. Science 272 (1996) 1615-1621
16. Kisker C., Schindelin H., Baas D., Retey J., Meckenstock R.U., and Kroneck P.M. A structural comparison of molybdenum cofactor-containing enzymes. FEMS Microbiol. Rev. 22 (1998) 503-521
17. Krissinel E., and Henrick K. Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr., D Biol. Crystallogr. 60 (2004) 2256-2268
18. Morpeth F.F., and Boxer D.H. Kinetic analysis of respiratory nitrate reductase from Escherichia coli K12. Biochemistry 24 (1985) 40-46
19. Sabaty M., Avazeri C., Pignol D., and Vermeglio A. Characterization of the reduction of selenate and tellurite by nitrate reductases. Appl. Environ. Microbiol. 67 (2001) 5122-5126
20. Avazeri C., Turner R.J., Pommier J., Weiner J.H., Giordano G., and Vermeglio A. Tellurite reductase activity of nitrate reductase is responsible for the basal resistance of Escherichia coli to tellurite. Microbiol. 143 (1997) 1181-1189
21. Satoh T., and Kurihara F.N. Purification and properties of dimethylsulfoxide reductase containing a molybdenum cofactor from a photodenitrifier, Rhodopseudomonas sphaeroides f.s. denitrificans. J. Biochem. (Tokyo) 102 (1987) 191-197
22. Hanlon S.P., Graham D.L., Hogan P.J., Holt R.A., Reeve C.D., Shaw A.L., and McEwan A.G. Asymmetric reduction of racemic sulfoxides by dimethyl sulfoxide reductases from Rhodobacter capsulatus, Escherichia coli and Proteus species. Microbiol. 144 (1998) 2247-2253
23. Luckarift H.R., Dalton H., Sharma N.D., Boyd D.R., and Holt R.A. Isolation and characterisation of bacterial strains containing enantioselective DMSO reductase activity: application to the kinetic resolution of racemic sulfoxides. Appl. Microbiol. Biotechnol. 65 (2004) 678-685
24. Simala-Grant J.L., and Weiner J.H. Kinetic analysis and substrate specificity of Escherichia coli DMSO reductase. Microbiology 142 (1996) 3231-3239
25. Simala-Grant J.L., and Weiner J.H. Modulation of the substrate specificity of Escherichia coli dimethylsulfoxide reductase. Eur. J. Biochem. 251 (1998) 510-515
26. Berks B.C., Ferguson S.J., Moir J.W.B., and Richardson D.J. Enzymes and associated electron transport systems that catalyze the respiratory reduction of nitrogen oxides and oxyanions. Biochim. Biophys. Acta 1232 (1995) 97-123
27. Simon J. Enzymology and bioenergetics of respiratory nitrite ammonification. FEMS Microbiol. Rev. 26 (2002) 285-309
28. Welter R., Yu L., and Yu C.A. The effects of nitric oxide on electron transport complexes. Arch. Biochem. Biophys. 331 (1996) 9-14
29. Johnson J.L., and Rajagopalan K.V. Structural and metabolic relationship between the molybdenum cofactor and urothione. Proc. Natl. Acad. Sci. U. S. A. 79 (1982) 6856-6860
30. Johnson J.L., Bastian N.R., and Rajagopalan K.V. Molybdopterin guanine dinucleotide: a modified form of molybdopterin identified in the molybdenum cofactor of dimethyl sulfoxide reductase from Rhodobacter sphaeroides forma specialis denitrificans. Proc. Natl. Acad. Sci. U. S. A. 87 (1990) 3190-3194
31. Hilton J.C., and Rajagopalan K.V. Identification of the molybdenum cofactor of dimethyl sulfoxide reductase from Rhodobacter sphaeroides f. sp. denitrificans as bis(molybdopterin guanine dinucleotide)molybdenum. Arch. Biochem. Biophys. 325 (1996) 139-143
32. Arnoux P., Sabaty M., Alric J., Frangioni B., Guigliarelli B., Adriano J.M., and Pignol D. Structural and redox plasticity in the heterodimeric periplasmic nitrate reductase. Nat. Struct. Biol. 10 (2003) 928-934
33. Dias J.M., Than M.E., Humm A., Huber R., Bourenkov G.P., Bartunik H.D., Bursakov S., Calvete J., Caldeira J., Carneiro C., Moura J.J., Moura I., and Romao M.J. Crystal structure of the first dissimilatory nitrate reductase at 1.9 Å solved by MAD methods. Struct. Fold Des. 7 (1999) 65-79
34. Boyington J.C., Gladyshev V.N., Khangulov S.V., Stadtman T.C., and Sun P.D. Crystal structure of formate dehydrogenase H: catalysis involving Mo, molybdopterin, selenocyteine, and an [4Fe-4S] cluster. Science 275 (1997) 1305-1308
35. Hille R. Molybdenum enzymes containing the pyranopterin cofactor: an overview. Met. Ions Biol. Syst. 39 (2002) 187-226
36. Enemark J.H., and Garner C.D. The coordination chemistry and function of the molybdenum centres of the oxomolybdoenzymes. JBIC, J. Biol. Inorg. Chem. 2 (1997) 817-822
37. Nieter Burgmayer S.J., Pearsall D.L., Blaney S.M., Moore E.M., and Sauk-Schubert C. Redox reactions of the pyranopterin system of the molybdenum cofactor. JBIC, J. Biol. Inorg. Chem. 9 (2004) 59-66
38. Moura J.J., Brondino C.D., Trincao J., and Romao M.J. Mo and W bis-MGD enzymes: nitrate reductases and formate dehydrogenases. JBIC, J. Biol. Inorg. Chem. 9 (2004) 791-799
39. Kloer D.P., Hagel C., Heider J., and Schulz G.E. Crystal structure of ethylbenzene dehydrogenase from Aromatoleum aromaticum. Structure 14 (2006) 1377-1388
40. Trieber C.A., Rothery R.A., and Weiner J.H. Multiple pathways of electron transfer in dimethyl sulfoxide reductase of Escherichia coli. J. Biol. Chem. 269 (1994) 7103-7109
41. Trieber C.A., Rothery R.A., and Weiner J.H. Engineering a novel iron-sulfur cluster into the catalytic subunit of Escherichia coli dimethyl-sulfoxide reductase. J. Biol. Chem. 271 (1996) 4620-4626
42. Magalon A., Asso M., Guigliarelli B., Rothery R.A., Bertrand P., Giordano G., and Blasco F. Molybdenum cofactor properties and [Fe-S] cluster coordination in Escherichia coli nitrate reductase A: investigation by site-directed mutagenesis of the conserved His-50 residue in the NarG subunit. Biochemistry 37 (1998) 7363-7370
43. Rothery R.A., Bertero M.G., Cammack R., Palak M., Blasco F., Strynadka N.C., and Weiner J.H. The catalytic subunit of Escherichia coli nitrate reductase A contains a novel [4Fe-4S] cluster with a high-spin ground state. Biochemistry 43 (2004) 5324-5333
44. Augier V., Guigliarelli B., Asso M., Bertrand P., Frixon C., Giordano G., Chippaux M., and Blasco F. Site-directed mutagenesis of conserved cysteine residues within the β subunit of Escherichia coli nitrate reductase. Physiological, biochemical, and EPR characterization of the mutated enzymes. Biochemistry 32 (1993) 2013-2023
45. Augier V., Asso M., Guigliarelli B., More C., Bertrand P., Santini C., Blasco F., Chippaux M., and Giordano G. Removal of the high-potential [4Fe-4S] center of the β-subunit from Escherichia coli nitrate reductase. Physiological, biochemical, and EPR characterization of site-directed mutated enzymes. Biochemistry 32 (1993) 5099-5108
46. Guigliarelli B., Asso M., More C., Augier V., Blasco F., Pommier J., Giordano G., and Bertrand P. EPR and redox characterization of the iron-sulfur centres in nitrate reductases A and Z from Escherichia coli. Evidence of a high and low potential class and their relevance in the electron-transfer mechanism. Eur. J. Biochem. 207 (1992) 61-68
47. Guigliarelli B., Guillasssier J., More C., Sétif P., Bottin H., and Bertrand P. Structural organization of the iron-sulfur centers in Synechocystis 6803 photosystem I. EPR study of oriented thylakoid membranes and analysis of the magnetic interactions. J. Biol. Chem. 268 (1993) 900-908
48. Guigliarelli B., Magalon A., Asso M., Bertrand P., Frixon C., Giordano G., and Blasco F. Complete coordination of the four Fe-S centres of the β subunit from Escherichia coli nitrate reductase. Physiological, biochemical and EPR characterization of site-directed mutants lacking the highest or lowest potential [4Fe-4S] clusters. Biochemistry 35 (1996) 4828-4836
49. nr of Escherichia coli nitrate reductase A (NarGHI). J. Biol. Chem. 272 (1997) 25652-25658
50. Magalon A., Rothery R.A., Giordano G., Blasco F., and Weiner J.H. Characterization by electron paramagnetic resonance of the role of the Escherichia coli nitrate reductase (NarGHI) iron-sulfur clusters in electron transfer to nitrate and identification of a semiquinone radical intermediate. J. Bacteriol. 179 (1997) 5037-5045
51. nr) of Escherichia coli nitrate reductase A. J. Biol. Chem. 273 (1998) 10851-10856
52. Rothery R.A., Magalon A., Giordano G., Guigliarelli B., Blasco F., and Weiner J.H. The molybdenum cofactor of Escherichia coli nitrate reductase A (NarGHI): effect of a mobAB mutation and interactions with [Fe-S] clusters. J. Biol. Chem. 273 (1998) 7462-7469
53. Rothery R.A., Blasco F., Magalon A., Asso M., and Weiner J.H. The hemes of Escherichia coli nitrate reductase A (NarGHI): potentiometric effects of inhibitor binding to NarI. Biochemistry 38 (1999) 12747-12757
54. L to the [3Fe-4S] cluster of Escherichia coli nitrate reductase A (NarGHI). Biochemistry 40 (2001) 5260-5268
55. Lanciano P., Vergnes A., Grimaldi S., Guigliarelli B., and Magalon A. Biogenesis of a respiratory complex is orchestrated by a single accessory protein. J. Biol. Chem. 282 (2007) 17468-17474
56. D. Biochemistry 46 (2007) 5323-5329
57. Cammack R., and Weiner J.H. Electron paramagnetic resonance spectroscopic characterization of dimethyl sulfoxide reductase of Escherichia coli. Biochemistry 29 (1990) 8410-8416
58. Cheng V.W., Rothery R.A., Bertero M.G., Strynadka N.C., and Weiner J.H. Investigation of the environment surrounding iron-sulfur cluster 4 of Escherichia coli dimethylsulfoxide reductase. Biochemistry 44 (2005) 8068-8077
59. Rothery R.A., and Weiner J.H. Alteration of the iron-sulfur composition of Escherichia coli dimethyl sulfoxide reductase by site-directed mutagenesis. Biochemistry 30 (1991) 8296-8305
60. Rothery R.A., and Weiner J.H. Topological characterization of Escherichia coli DMSO reductase by electron paramagnetic resonance spectroscopy of an engineered [3Fe-4S] cluster. Biochemistry 32 (1993) 5855-5861
61. Rothery R.A., and Weiner J.H. Interaction of an engineered [3Fe-4S] cluster with a menaquinol binding site of Escherichia coli DMSO reductase. Biochemistry 35 (1996) 3247-3257
62. Rothery R.A., Trieber C.A., and Weiner J.H. Interactions between the molybdenum cofactor and iron-sulfur clusters of Escherichia coli dimethylsulfoxide reductase. J. Biol. Chem. 274 (1999) 13002-13009
63. Trieber C.A., Rothery R.A., and Weiner J.H. Consequences of removal of a molybdenum ligand (DmsA-Ser-176) of Escherichia coli dimethyl sulfoxide reductase. J. Biol. Chem. 271 (1996) 27339-27345
64. Manadori A., Cecchini G., Shröder I., Gunsalus R.P., Werth M.T., and Johnson M.K. [3Fe-4S] to [4Fe-4S] cluster conversion in Escherichia coli fumarate reductase by site-directed mutagenesis. Biochemistry 31 (1992) 2703-2712
65. Breton J., Berks B.C., Reilly A., Thomson A.J., Ferguson S.J., and Richardson D.J. Characterization of the paramagnetic iron-sontaining redox centres of Thiosphaera pantotropha periplasmic nitrate reductase. FEBS Lett. 345 (1994) 76-80
66. Gladyshev V.N., Boyington J.C., Khangulov S.V., Grahame D.A., Stadtman T.C., and Sun P.C. Characterization of crystalline formate dehydrogenase H from Escherichia coli. Stabilization, EPR spectroscopy, and preliminary crystollographic analysis. J. Biol. Chem. 271 (1996) 8095-8100
67. McDevitt C.A., Hugenholtz P., Hanson G.R., and McEwan A.G. Molecular analysis of dimethyl sulphide dehydrogenase from Rhodovulum sulfidophilum: its place in the dimethyl sulphoxide reductase family of microbial molybdopterin-containing enzymes. Mol. Microbiol. 44 (2002) 1575-1587
68. McDevitt C.A., Hanson G.R., Noble C.J., Cheesman M.R., and McEwan A.G. Characterization of the redox centers in dimethyl sulfide dehydrogenase from Rhodovulum sulfidophilum. Biochemistry 41 (2002) 15234-15244
69. Moser C.C., Farid T.A., Chobot S.E., and Dutton P.L. Electron tunneling chains of mitochondria. Biochim. Biophys. Acta 1757 (2006) 1096-1109
70. Page C.C., Moser C.C., Chen X., and Dutton P.L. Natural engineering principles of electron tunneling in biological oxidation-reduction. Nature 402 (1999) 47-52
71. Page C.C., Moser C.C., and Dutton P.L. Mechanism for electron transfer within and between proteins. Curr. Opin. Chem. Biol. 7 (2003) 551-556
72. Daizadeh I., Medvedev D.M., and Stuchebrukhov A.A. Electron transfer in ferredoxin: are tunneling pathways evolutionarily conserved?. Mol. Biol. Evol. 19 (2002) 406-415
73. Hettmann T., Siddiqui R.A., von Langen J., Frey C., Romao M.J., and Diekmann S. Mutagenesis study on the role of a lysine residue highly conserved in formate dehydrogenases and periplasmic nitrate reductases. Biochem. Biophys. Res. Commun. 310 (2003) 40-47
74. Turner R.J., Papish A.L., and Sargent F. Sequence analysis of bacterial redox enzyme maturation proteins (REMPs). Can. J. Microbiol. 50 (2004) 225-238
75. Chan C.S., Howell J.M., Workentine M.L., and Turner R.J. Twin-arginine translocase may have a role in the chaperone function of NarJ from Escherichia coli. Biochem. Biophys. Res. Commun. 343 (2006) 244-251
76. Krafft T., Bokranz M., Klimmeck O., Schröder I., Fahrenholz F., Kojro E., and Kröger A. Cloning and nucleotide sequence of the psrA gene of Wolinella succinogenes polysulphide reductase. Eur. J. Biochem. 206 (1992) 5456-5463
77. Blasco F., Iobbi C., Giordano G., Chippaux M., and Bonnefoy V. Nitrate reductase of Escherichia coli: completion of the nucleotide sequence of the nar operon and reassessment of the role of the alpha and beta subunits in iron binding and electron transfer. Molec. Gen. Genet. 218 (1989) 249-256
78. Weiner J.H., Rothery R.A., Sambasivarao D., and Trieber C.A. Molecular analysis of dimethylsulfoxide reductase: a complex iron-sulfur molybdoenzyme of Escherichia coli. Biochim. Biophys. Acta 1102 (1992) 1-18
79. Blasco F., Guigliarelli B., Magalon A., Asso M., Giordano G., and Rothery R.A. The coordination and function of the redox centres of the membrane-bound nitrate reductases. Cell. Mol. Life Sci. 58 (2001) 179-193
80. Fukuyama K., Nagahara Y., Tsukihara T., Katsube Y., Hase T., and Matsubara H. Tertiary structure of Bacillus thermoproteolyticus [4Fe-4S] ferredoxin. Evolutionary implications for bacterial ferredoxins. J. Mol. Biol. 199 (1988) 183-193
81. George D.G., Hunt L.T., Yeh L.S., and Barker W.C. New perspectives on bacterial ferredoxin evolution. J. Mol. Evol. 22 (1985) 20-31
82. Cammack R., Patil D.S., and Weiner J.H. Evidence that centre 2 in Escherichia coli fumarate reductase is a [4Fe-4S] cluster. Biochim. Biophys. Acta 870 (1986) 545-551
83. Condon C., Cammack R., Patil D.S., and Owen P. The succinate dehydrogenase of Escherichia coli. Immunochemical resolution and biophysical characterization of a 4-subunit enzyme complex. J. Biol. Chem. 260 (1985) 9427-9434
84. Cheng V.W., Ma E., Zhao Z., Rothery R.A., and Weiner J.H. The iron-sulfur clusters in Escherichia coli succinate dehydrogenase direct electron flow. J. Biol. Chem. (2006) Electronic publication ahead of print
85. Hudson J.M., Heffron K., Kotlyar V., Sher Y., Maklashina E., Cecchini G., and Armstrong F.A. Electron transfer and catalytic control by the iron-sulfur clusters in a respiratory enzyme, E. coli fumarate reductase. J. Am. Chem. Soc. 127 (2005) 6977-6989
86. Ohnishi T., Moser C.C., Page C.C., Dutton P.L., and Yano T. Simple redox-linked proton-transfer design: new insights from structures of quinol-fumarate reductase. Structure 8 (2000) R23-R32
87. Berg B.L., Li J., Heider J., and Stewart V. Nitrate-inducible formate dehydrogenase in Escherichia coli K-12: I. Nucleotide sequence of the fdnGHI operon and evidence that opal (UGA) encodes selenocysteine. J. Biol. Chem. 266 (1991) 22380-22385
88. Hederstedt L. Succinate:quinone oxidoreductase in the bacteria Paracoccus denitrificans and Bacillus subtilis. Biochim. Biophys. Acta 1553 (2002) 74-83
89. Huang L.S., Sun G., Cobessi D., Wang A.C., Shen J.T., Tung E.Y., Anderson V.E., and Berry E.A. 3-Nitropropionic acid is a suicide inhibitor of mitochondrial respiration that, upon oxidation by complex II, forms a covalent adduct with a catalytic base arginine in the active site of the enzyme. J. Biol. Chem. 281 (2006) 5965-5972
90. Sun F., Huo X., Zhai Y., Wang A., Xu J., Su D., Bartlam M., and Rao Z. Crystal structure of mitochondrial respiratory membrane protein complex. Cell 121 (2005) 1043-1057
91. Yankovskaya V., Horsefield R., Törnroth S., Luna-Chavez C., Miyoshi H., Léger C., Byrne B., Cecchini G., and Iwata S. Architecture of succinate dehydrogenase and reactive oxygen species generation. Science 299 (2003) 700-704
92. Altschul S.F., Madden T.L., Schäffer A.A., Zhang J., Zhang Z., Miller W., and Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25 (1997) 3389-3402
93. Bertero M.G., Rothery R.A., Boroumand N., Palak M., Blasco F., Ginet N., Weiner J.H., and Strynadka N.C. Structural and biochemical characterization of a quinol binding site of Escherichia coli nitrate reductase A. J. Biol. Chem. 280 (2005) 14836-14843
94. Rothery R.A., Blasco F., Magalon A., and Weiner J.H. The diheme cytochrome b subunit (NarI) of Escherichia coli nitrate reductase A (NarGHI): structure, function, and interaction with quinols. J. Mol. Microbiol. Biotechnol. 3 (2001) 273-283
95. Thompson J.D., Higgins D.G., and Gibson T.J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22 (1994) 4673-4680
96. Mander G.J., Duin E.C., Linder D., Stetter K.O., and Hedderich R. 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
97. Hedderich R., Klimmek O., Kröger A., Dirmeier R., Keller M., and Stetter K.O. Anaerobic respiration with elemental sulfur and with disulfides. FEMS Microbiol. Rev. 22 (1999) 353-381
98. Krogh A., Larsson B., von Heijne G., and Sonnhammer E.L. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 305 (2001) 567-580
99. Moller S., Croning M.D., and Apweiler R. Evaluation of methods for the prediction of membrane spanning regions. Bioinformatics 17 (2001) 646-653
100. Bogsch E.G., Sargent F., Stanley N.R., Berks B.C., Robinson C., and Palmer T. An essential component of a novel bacterial protein export system with homologues in plastids and mitochondria. J. Biol. Chem. 273 (1998) 18003-18006
101. 2. Mol. Microbiol. 30 (1998) 639-646
102. Groβ R., Pisa R., Sanger M., Lancaster C.R., and Simon J. Characterization of the menaquinone reduction site in the diheme cytochrome b membrane anchor of Wolinella succinogenes NiFe-hydrogenase. J. Biol. Chem. 279 (2004) 274-281
103. Volbeda A., Charon M.-H., Piras C., Hatchikian E.C., Frey M., and Fontecilla-Camps J.C. Crystal structure of the nickel-iron hydrogenase from Desulfovibrio gigas. Nature 273 (1995) 580-587
104. Heinzinger N.K., Fujimoto S.Y., Clark M.A., Moreno M.S., and Barrett E.L. Sequence analysis of the phs operon in Salmonella typhymurium and the contribution of thiosulfate reduction to anaerobic metabolism. J. Bacteriol. 177 (1995) 2813-2820
105. Weiner J.H., Shaw G., Turner R.J., and Trieber C.A. The topology of the anchor subunit of dimethyl sulfoxide reductase of Escherichia coli. J. Biol. Chem. 268 (1993) 3238-3244
106. Sambasivarao D., Scraba D.G., Trieber C.A., and Weiner J.H. Organization of dimethyl sulfoxide reductase in the plasma membrane of Escherichia coli. J. Bacteriol. 172 (1990) 5938-5948
107. Richardson D.J., and Watmough N.J. Inorganic nitrogen metabolism in bacteria. Curr. Opin. Chem. Biol. 3 (1999) 207-219
108. Clarke T.A., Dennison V., Seward H.E., Burlat B., Cole J.A., Hemmings A.M., and Richardson D.J. Purification and spectropotentiometric characterization of Escherichia coli NrfB, a decaheme homodimer that transfers electrons to the decaheme periplasmic nitrite reductase complex. J. Biol. Chem. 279 (2004) 41333-41339
109. Stanley N.R., Sargent F., Buchanan G., Shi J., Stewart V., Palmer T., and Berks B.C. Behaviour of topological marker proteins targeted to the Tat protein transport pathway. Mol. Microbiol. 43 (2002) 1005-1021
110. Sambasivarao D., Dawson H.A., Zhang G., Shaw G., Hu J., and Weiner J.H. Investigation of Escherichia coli dimethyl sulfoxide reductase assembly and processing in strains defective for the sec-independent protein translocation system membrane targeting and translocation. J. Biol. Chem. 276 (2001) 20167-20174
111. Rothery R.A., Kalra N., Turner R.J., and Weiner J.H. Sequence similarity as a predictor of the transmembrane topology of membrane-intrinsic subunits of bacterial respiratory chain enzymes. J. Mol. Microbiol. Biotechnol. 4 (2002) 133-150
112. Zhao Z., and Weiner J.H. Interaction of HOQNO with dimethyl sulfoxide reductase of Escherichia coli. J. Biol. Chem. 273 (1998) 20758-20763
113. Geijer P., and Weiner J.H. Glutamate 87 is important for menaquinol binding in DmsC of the DMSO reductase (DmsABC) from Escherichia coli. Biochim. Biophys. Acta 1660 (2004) 66-74
114. Hinsley A.P., and Berks B.C. Specificity of respiratory pathways involved in the reduction of sulfur compounds by Salmonella enterica. Microbiology 148 (2002) 3631-3638
115. Baymann F., Lebrun E., Brugna M., Schoepp-Cothenet B., Giudici-Orticoni M.T., and Nitschke W. 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
116. Méjean V., Iobbi-Nivol C., Lepelletier M., Chippaux M., and Pascal M. TMAO anaerobic respiration in Escherichia coli: involvement of the tor operon. Mol. Microbiol. 11 (1994) 1169-1179
117. Czjek M., Dos Santos J., Pommier J., Giordano G., Méjean V., and Haser R. Crystal structure of oxidized trimethylamine-N-oxide reductase from Shewanella massilia at 2.5 Å resolution. J. Mol. Biol. 284 (1998) 435-447
118. Brige A., Leys D., Meyer T.E., Cusanovich M.A., and Van Beeumen J.J. The 1.25 Å resolution structure of the diheme NapB subunit of soluble nitrate reductase reveals a novel cytochrome c fold with a stacked heme arrangement. Biochemistry 41 (2002) 4827-4836
119. Ellis P.J., Conrads T., Hille R., and Kuhn P. Crystal structure of the 100 kDa arsenite oxidase from Alcaligenes faecalis in two crystal forms at 1.64 Å and 2.03 Å. Structure 9 (2001) 125-132
120. Raaijmakers H., Macieira S., Dias J.M., Teixeira S., Bursakov S., Huber R., Moura J.J., Moura I., and Romao M.J. Gene sequence and the 1.8 Å crystal structure of the tungsten-containing formate dehydrogenase from Desulfovibrio gigas. Structure 10 (2002) 1261-1272
121. Pollock W.B., Loutfi M., Bruschi M., Rapp-Giles B.J., Wall J.D., and Voordouw G. Cloning, sequencing, and expression of the gene encoding the high-molecular-weight cytochrome c from Desulfovibrio vulgaris Hildenborough. J. Bacteriol. 173 (1991) 220-228
122. Rossi M., Pollock W.B.R., Reij M.W., Keon R.G., Fu R., and Voordouw G. The hmc operon of Desulfovibrio vulgaris subsp. vulgaris Hildenborough encodes a potential transmembrane redox protein complex. J. Bacteriol. 175 (1993) 4699-4711
123. Pereira I.A., Romao M.J., Xavier A.V., LeGall J., and Tiexeira M. Electron transfer between hydrogenases and mono- and multiheme cytochromes in Desulfovibrio sp. JBIC, J. Biol. Inorg. Chem. 3 (1998) 494-498
124. Sazanov L.A., and Hinchliffe P. Structure of the hydrophilic domain of respiratory complex I from Thermus thermophilus. Science 311 (2006) 1430-1436
125. Finel M. Organization and evolution of structural elements within complex I. Biochim. Biophys. Acta 1364 (1998) 112-121
126. Odom J.M., and Peck Jr. H.D. Localization of dehydrogenases, reductases, and electron transfer components in the sulfate-reducing bacterium Desulfovibrio gigas. J. Bacteriol. 147 (1981) 161-169
127. Costa A., Tiexeira M., LeGall J., Moura J.J., and Moura I. Formate dehydrogenase from Desulfovibrio desulfuricans ATCC 27774: isolation and spectroscopic characterization of the active sites (heme, iron-sulfur centers and molybdenum). JBIC, J. Biol. Inorg. Chem. 2 (1997) 198-208
128. Sebban C., Blanchard L., Bruschi M., and Guerlesquin F. Purification and characterization of the formate dehydrogenase from Desulfovibrio vulgaris Hildenborough. FEMS Microbiol. Lett. 133 (1995) 143-149
129. 3 from Desulfovibrio gigas: crystal structure at 1.8 Å resolution and evidence for a specific calcium-binding site. Protein Sci. 5 (1996) 1342-1354
130. Boll M., Schink B., Messerschmidt A., and Kroneck P.M. Novel bacterial molybdenum and tungsten enzymes: three-dimensional structure, spectroscopy, and reaction mechanism. Biol. Chem. 386 (2005) 999-1006
131. Reichenbecher W., and Schink B. Towards the reaction mechanism of pyrogallol-phloroglucinol transhydroxylase of Pelobacter acidigallici. Biochim. Biophys. Acta 1430 (1999) 245-253
132. Messerschmidt A., Niessen H., Abt D., Einsle O., Schink B., and Kroneck P.M. Crystal structure of pyrogallol-phloroglucinol transhydroxylase, an Mo enzyme capable of intermolecular hydroxyl transfer between phenols. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 11571-11576
133. Leahy D.J., Hendrickson W.A., Aukhil I., and Erickson H.P. Structure of a fibronectin type III domain from tenascin phased by MAD analysis of the selenomethionyl protein. Science 258 (1992) 987-991
134. Stewart V., Lu Y., and Darwin A.J. Periplasmic nitrate reductase (NapABC enzyme) supports anaerobic respiration by Escherichia coli K-12. J. Bacteriol. 184 (2002) 1314-1323
135. Potter L.C., Millington P., Griffifths L., Thomas G.H., and Cole J.A. Competition between Escherichia coli strains expressing a periplasic or a membrane-bound nitrate reductase: does Nap confer a selective advantage during nitrate-limited growth?. Biochem. J. 344 (1999) 77-84
136. Philippot L., and Højberg O. Dissimilatory nitrate reductases in bacteria. Biochim. Biophys. Acta 1446 (1999) 1-23
137. Moreno-Vivián C., Cabello P., Martínez-Luque M., Blasco R., and Castillo F. Prokaryotic nitrate reduction: molecular properties and functional distinction among bacterial nitrate reductases. J. Bacteriol. 181 (1999) 6573-6584
138. Pierson D.E., and Campbell A. Cloning and nucleotide sequence of bisC, the structural gene for biotin sulfoxide reductase in Escherichia coli. J. Bacteriol. 172 (1990) 2194-2198
139. Pollock V.V., and Barber M.J. Molecular cloning and expression of biotin sulfoxide reductase from Rhodobacter sphaeroides forma sp. denitrificans. Arch. Biochem. Biophys. 318 (1995) 322-332
140. Stolz J.F., Basu P., Santini J.M., and Oremland R.S. Arsenic and selenium in microbial metabolism. Annu. Rev. Microbiol. 60 (2006) 107-130
141. Hille R. The mononuclear molybdenum enzymes. Chem. Rev. 96 (1996) 2757-2816
142. Peters J.W., Lanzilotta W.N., Lemon B.J., and Seefeldt L.C. X-ray crystal structure of the Fe-only hydrogenase (CpI) from Clostridium pasteurianum to 1.8 Angstrom resolution. Science 282 (1998) 1853-1858
143. +-reducing hydrogenase from Ralstonia eutropha. Biochemistry 45 (2006) 11658-11665
144. Hinchliffe P., and Sazanov L.A. Organization of iron-sulfur clusters in respiratory complex I. Science 309 (2005) 771-774
145. Nakamaru-Ogiso E., Yano T., Yagi T., and Ohnishi T. Characterization of the iron-sulfur cluster N7 (N1c) in the subunit NuoG of the proton-translocating NADH-quinone oxidoreductase from Escherichia coli. J. Biol. Chem. 280 (2005) 301-307
146. Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., and Higgins D.G. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25 (1997) 4876-4882
147. Jeanmougin F., Thompson J.D., Gouy M., Higgins D.G., and Gibson T.J. Multiple sequence alignment with Clustal X. Trends Biochem. Sci. 23 (1998) 403-405
148. Fearnley I.M., and Walker J.E. Conservation of sequences of subunits of mitochondrial complex I and their relationships with other proteins. Biochim. Biophys. Acta 1140 (1992) 105-134
149. Einsle O., Messerschmidt A., Huber R., Kroneck P.M., and Neese F. Mechanism of the six-electron reduction of nitrite to ammonia by cytochrome c nitrite reductase. J. Am. Chem. Soc. 124 (2002) 11737-11745
150. Eaves D.J., Grove J., Staudenmann W., James P., Poole R.K., White S.A., Griffiths I., and Cole J.A. Involvement of products of the nrfEFG genes in the covalent attachment of haem c to a novel cysteine-lysine motif in the cytochrome c552 nitrite reductase from Escherichia coli. Mol. Microbiol. 28 (1998) 205-216
151. Einsle O., Stach P., Messerschmidt A., Simon J., Kroger A., Huber R., and Kroneck P.M. Cytochrome c nitrite reductase from Wolinella succinogenes. Structure at 1.6 Å resolution, inhibitor binding, and heme-packing motifs. J. Biol. Chem. 275 (2000) 39608-39616
152. Rousset M., Montet Y., Guigliarelli B., Forget N., Asso M., Bertrand P., Fontecilla-Camps J.C., and Hatchikian E.C. [3Fe-4S] to [4Fe-4S] cluster conversion in Desulfovibrio fructosovorans [Ni-Fe] hydrogenase by site-directed mutagenesis. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 11625-11630
153. Groβ R., Simon J., and Kröger A. The role of the twin-arginine motif in the signal peptide encoded by the hydA gene of the hydrogenase from Wolinella succinogenes. Arch. Microbiol. 172 (1999) 227-232
154. 2 oxidation capability. J. Bacteriol. 182 (2000) 3429-3436
155. Matias P.M., Coelho A.V., Valente F.M., Placido D., LeGall J., Xavier A.V., Pereira I.A., and Carrondo M.A. 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
156. Cecchini G., Schröder I., Gunsalus R.P., and Maklashina E. Succinate dehydrogenase and fumarate reductase from Escherichia coli. Biochim. Biophys. Acta 1553 (2002) 140-157
157. Hederstedt L., and Ohnishi T. Progress in succinate:quinone oxidoreductase research. In: Ernster L. (Ed). Molecular Mechanisms in Bioenergetics vol. 23 (1992), Elsevier Science Publishing Co. Inc, New York 163-197
158. Villemur R., Lanthier M., Beaudet R., and Lepine F. The Desulfitobacterium genus. FEMS Microbiol. Rev. 30 (2006) 706-733
159. Madsen T., and Licht D. Isolation and characterization of an anaerobic chlorophenol-transforming bacterium. Appl. Environ. Microbiol. 58 (1992) 2874-2878
160. Lee T., Tokunaga T., Suyama A., and Furukawa K. Efficient dechlorination of tetrachloroethylene in soil slurry by combined use of an anaerobic Desulfitobacterium sp. strain Y-51 and zero-valent iron. J. Biosci. Bioeng. 92 (2001) 453-458
161. Suyama A., Iwakiri R., Kai K., Tokunaga T., Sera N., and Furukawa K. Isolation and characterization of Desulfitobacterium sp. strain Y51 capable of efficient dehalogenation of tetrachloroethene and polychloroethanes. Biosci. Biotechnol. Biochem. 65 (2001) 1474-1481
162. Lanthier M., Juteau P., Lepine F., Beaudet R., and Villemur R. Desulfitobacterium hafniense is present in a high proportion within the biofilms of a high-performance pentachlorophenol-degrading, methanogenic fixed-film reactor. Appl. Environ. Microbiol. 71 (2005) 1058-1065
163. Ueda K., Ohno M., Yamamoto K., Nara H., Mori Y., Shimada M., Hayashi M., Oida H., Terashima Y., Nagata M., and Beppu T. Distribution and diversity of symbiotic thermophiles, Symbiobacterium thermophilum and related bacteria, in natural environments. Appl. Environ. Microbiol. 67 (2001) 3779-3784
164. Ohno M., Shiratori H., Park M.J., Saitoh Y., Kumon Y., Yamashita N., Hirata A., Nishida H., Ueda K., and Beppu T. Symbiobacterium thermophilum gen. nov., sp. nov., a symbiotic thermophile that depends on co-culture with a Bacillus strain for growth. Int. J. Syst. Evol. Microbiol. 50 (2000) 1829-1832
165. Vignais P.M., Billoud B., and Meyer J. Classification and phylogeny of hydrogenases. FEMS Microbiol. Rev. 25 (2001) 455-501
166. Vignais P.M., and Colbeau A. Molecular biology of microbial hydrogenases. Curr. Issues Mol. Biol. 6 (2004) 159-188
167. +-linked formate dehydrogenase of Ralstonia eutropha. J. Biol. Chem. 273 (1998) 26349-26360
168. Friedrich T., and Scheide D. The respiratory complex I of bacteria, archaea and eukarya and its module common with membrane-bound multisubunit hydrogenases. FEBS Lett. 479 (2000) 1-5
169. Richardson D.J., Berks B.C., Russell D.A., Spiro S., and Taylor C.J. Functional, biochemical and genetic diversity of prokaryotic nitrate reductases. Cell. Mol. Life Sci. 58 (2001) 165-178
170. Lin J.T., Goldman B.S., and Stewart V. Structures of genes nasA and nasB, encoding assimilatory nitrate and nitrite reductases in Klebsiella pneumoniae M5al. J. Bacteriol. 175 (1993) 2370-2378
171. Hensel M., Hinsley A.P., Nikolaus T., Sawers G., and Berks B.C. The genetic basis of tetrathionate respiration in Salmonella typhimurium. Mol. Microbiol. 32 (1999) 275-287
172. Sirko A., Zatyka M., Sadowy E., and Hulanicka D. Sulfate and thiosulfate transport in Escherichia coli K-12: evidence for a functional overlapping of sulfate- and thiosulfate-binding proteins. J. Bacteriol. 177 (1995) 4134-4136
173. Colyer T.E., and Kredich N.M. In vitro characterization of constitutive CysB proteins from Salmonella typhimurium. Mol. Microbiol. 21 (1996) 247-256
174. Lira-Ruan V., Sarath G., Klucas R.V., and Arredondo-Peter R. In silico analysis of a flavohemoglobin from Sinorhizobium meliloti strain 1021. Microbiol. Res. 158 (2003) 215-227
175. Kerby R.L., Hong S.S., Ensign S.A., Coppoc L.J., Ludden P.W., and Roberta G.P. Genetic and physiological characterization of the Rhodospirillum rubrum carbon monoxide dehydrogenase system. J. Bacteriol. 174 (1992) 5284-5294
176. Rice P., Longden I., and Bleasby A. EMBOSS: The European Molecular Biology Open Software Suite. Trends Genet. 16 (2000) 276-277
177. Bruschi M., and Guerlesquin F. Structure, function, and evolution of bacterial ferredoxins. FEMS Microbiol. Rev. 54 (1988) 155-176
178. Beinert H. Recent developments in the field of iron-sulfur proteins. FASEB J. 4 (1990) 2483-2491
179. Darimont B., and Sterner R. Sequence, assembly and evolution of a primordial ferredoxin from Thermotoga maritima. EMBO J. 13 (1994) 1772-1781
180. Macedo-Ribeiro S., Martins B.M., Pereira P.J., Buse G., Huber R., and Soulimane T. New insights into the thermostability of bacterial ferredoxins: high-resolution crystal structure of the seven-iron ferredoxin from Thermus thermophilus. JBIC, J. Biol. Inorg. Chem. 6 (2001) 663-674
181. Sery A., Housset D., Serre L., Bonicel J., Hatchikian C., Frey M., and Roth M. Crystal structure of the ferredoxin I from Desulfovibrio africanus at 2.3 Å resolution. Biochemistry 33 (1994) 15408-15417
182. Nakajima Y., Fujiwara T., and Fukumori Y. Purification and characterization of a [3Fe-4S][4Fe-4S] type ferredoxin from hyperthermophilic archaeon, Pyrobaculum islandicum. J. Biochem. (Tokyo) 123 (1998) 521-527
183. Duee E.D., Fanchon E., Vicat J., Sieker L.C., Meyer J., and Moulis J.M. Refined crystal structure of the 2[4Fe-4S] ferredoxin from Clostridium acidurici at 1.84 Å resolution. J. Mol. Biol. 243 (1994) 683-695
184. Chan M.K., Mukund S., Kletzin A., Adams M.W., and Rees D.C. Structure of a hyperthermophilic tungstopterin enzyme, aldehyde ferredoxin oxidoreductase. Science 267 (1995) 1463-1469