Biochemistry, evolution and physiological function of the Rnf complex, a novel ion-motive electron transport complex in prokaryotes

Cellular and Molecular Life Sciences

Volumn 68, Issue 4, 2011, Pages 613-634

  Biegel, Eva ^a   Schmidt, Silke ^a   González, José M ^b   Müller, Volker ^a  

^a GOETHE UNIVERSITY   (Germany)

^b UNIVERSIDAD DE LA LAGUNA   (Spain)

Author keywords

Acetobacterium woodii; Electron transport; Energy conservation; Ferredoxin; Rnf

Indexed keywords

ADENOSINE TRIPHOSPHATE; BACTERIAL ENZYME; CAFFEIC ACID; ECH HYDROGENASE; FERREDOXIN; NICOTINAMIDE ADENINE DINUCLEOTIDE; NQR PROTEIN; PYRIDINE NUCLEOTIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); RNF PROTEIN; RNFA PROTEIN; RNFB PROTEIN; RNFC PROTEIN; RNFD PROTEIN; RNFG PROTEIN; UNCLASSIFIED DRUG;

ACETOBACTERIUM; ACETOBACTERIUM WOODII; AZOTOBACTER VINELANDII; BACTERIAL GENOME; BACTERIAL METABOLISM; BACTERIUM; CELLULAR DISTRIBUTION; CLOSTRIDIA; COMPLEX FORMATION; DESULFOBACTER; DESULFOBACTERIUM AUTOTROPHICUM; ELECTRON TRANSPORT; ENERGY METABOLISM; ESCHERICHIA COLI; MEMBRANE VESICLE; METHANOSARCINA ACETIVORANS; MICROBIAL RESPIRATION; NITROGEN FIXATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PSEUDOMONAS STUTZERI; RESPIRATORY CHAIN; REVIEW; RHODOBACTER CAPSULATUS; SEQUENCE HOMOLOGY; SODIUM CURRENT; SODIUM TRANSPORT; STOICHIOMETRY; SYNTROPHUS ACIDITROPHICUS; VIBRIO CHOLERAE;

ACETOBACTERIUM; BACTERIA; ELECTRON TRANSPORT; ENERGY METABOLISM; EVOLUTION, MOLECULAR; GENES, BACTERIAL; OXIDOREDUCTASES; PHYLOGENY; PROTEIN SUBUNITS;

ACETOBACTERIUM WOODII; PROKARYOTA;

EID: 79951579402     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-010-0555-8     Document Type: Review

References (133)

1. HL Drake S Daniel K Küsel C Matthies C Kuhner S Braus-Strohmeyer 1997 Acetogenic bacteria: what are the in situ consequences of their diverse metabolic diversities? Biofactors 1 13 24 (Pubitemid 27287120)
2. Müller V, Imkamp F, Rauwolf A, Küsel K, Drake HL (2004) Molecular and cellular biology of acetogenic bacteria. In: Nakano MM, Zuber P (eds) Strict and facultative anaerobes. Medical and environmental aspects. Horizon Biosciences, Norfolk, pp 251-281
3. SW Ragsdale 2008 Enzymology of the Wood-Ljungdahl pathway of acetogenesis Ann N Y Acad Sci 1125 129 136 1:CAS:528:DC%2BD1cXlsV2rs7g%3D 18378591 (Pubitemid 351451161)
4. G Diekert G Wohlfarth 1994 Metabolism of homoacetogens Antonie van Leeuwenhoek Int J Gen M 66 209 221 1:CAS:528:DyaK2MXjs1yhu78%3D
5. 2 fixation Biochim Biophys Acta 1784 1873 1898 1:CAS:528: DC%2BD1cXhtlaqtb7O 18801467
6. B Eichler B Schink 1984 Oxidation of primary aliphatic alcolhols by Acetobacterium carbinolicum sp. nov., a homoacetogenic anaerobe Arch Microbiol 140 147 152 1:CAS:528:DyaL2MXnsFChtg%3D%3D (Pubitemid 15181733)
7. R Bache N Pfennig 1981 Selective isolation of Acetobacterium woodii on methoxylated aromatic acids and determination of growth yields Arch Microbiol 130 255 261 1:CAS:528:DyaL38XkvVOmsQ%3D%3D
8. V Müller 2003 Energy conservation in acetogenic bacteria Appl Environ Microbiol 69 6345 6353 14602585 (Pubitemid 37420162)
9. + as the coupling ion during hydrogen-dependent caffeate reduction by Acetobacterium woodii J Bacteriol 184 1947 1951 1:CAS:528:DC%2BD38Xit1Gktbg%3D 11889102 (Pubitemid 34275538)
10. R Heise V Müller G Gottschalk 1992 Presence of a sodium-translocating ATPase in membrane vesicles of the homoacetogenic bacterium Acetobacterium woodii Eur J Biochem 206 553 557 1:CAS:528:DyaK38Xks1Khtrw%3D 1534543
11. O-type enzyme Eur J Biochem 223 275 283 1:CAS:528:DyaK2cXlt1yntr4%3D 8033902 (Pubitemid 24221672)
12. O ATP synthase FEBS J 275 1999 2007 1:CAS:528: DC%2BD1cXlslCrtLs%3D 18355313 (Pubitemid 351569542)
13. O-ATPase from Acetobacterium woodii contains F-type and V-type rotor subunits and is capable of ATP synthesis FEBS J 274 3421 3428 1:CAS:528:DC%2BD2sXns1Oktro%3D 17555523 (Pubitemid 47024975)
14. V Müller S Bowien 1995 Differential effects of sodium ions on motility in the homoacetogenic bacteria Acetobacterium woodii and Sporomusa sphaeroides Arch Microbiol 164 363 369
15. + bioenergetics in Acetobacterium woodii Biochim Biophys Acta 1787 691 696 1:CAS:528:DC%2BD1MXntVSitrg%3D 19167341
16. C Seifritz SL Daniel A Gössner HL Drake 1993 Nitrate as a preferred electron sink for the acetogen Clostridium thermoaceticum J Bacteriol 175 8008 8013 1:CAS:528:DyaK2cXkvFyntw%3D%3D 8253688 (Pubitemid 24004410)
17. JM Fröstl C Seifritz HL Drake 1996 Effect of nitrate on the autotrophic metabolism of the acetogens Clostridium thermoautotrophicum and Clostridium thermoaceticum J Bacteriol 178 4597 4603 8755890 (Pubitemid 26262248)
18. A Tschech N Pfennig 1984 Growth yield increase linked to caffeate reduction in Acetobacterium woodii Arch Microbiol 137 163 167 1:CAS:528:DyaL2cXhtlGltro%3D (Pubitemid 14157100)
19. +-oxidoreductase (Rnf) in Acetobacterium woodii: a novel potential coupling site in acetogens Ann N Y Acad Sci 1125 137 146 18378592 (Pubitemid 351451157)
20. U Blum TR Wentworth K Klein AD Worsham LD King TM Gerig S-W Lyu 1991 Phenolic acid content of soils from wheat-no till, wheat-conventional till, and fallow-conventional till soybean cropping systems J Chem Ecol 17 1045 1068 1:CAS:528:DyaK3MXkslSnsLY%3D
21. 2 in Acetobacterium woodii NZva16 Arch Microbiol 150 447 451 1:CAS:528:DyaL1cXlvVOjsLc%3D
22. F Imkamp E Biegel E Jayamani W Buckel V Müller 2007 Dissection of the caffeate respiratory chain in the acetogen Acetobacterium woodii: indications for a Rnf-type NADH dehydrogenase as coupling site J Bacteriol 189 8145 8153 1:CAS:528:DC%2BD2sXhtlyht7rI 17873051 (Pubitemid 350178926)
23. SW Ragsdale LG Ljungdahl 1984 Hydrogenase from Acetobacterium woodii Arch Microbiol 139 361 365 1:CAS:528:DyaL2cXlvVKktLo%3D 6393895
24. + oxidoreductase. Proc Natl Acad Sci USA 107:18138-18142
25. E Biegel S Schmidt V Müller 2009 Genetic, immunological and biochemical evidence of a Rnf complex in the acetogen Acetobacterium woodii Environ Microbiol 11 1438 1443 1:CAS:528:DC%2BD1MXotlSiu7w%3D 19222539
26. M Schmehl A Jahn A Meyer zu Vilsendorf S Hennecke B Masepohl M Schuppler M Marxer J Oelze W Klipp 1993 Identification of a new class of nitrogen fixation genes in Rhodobacter capsulatus: a putative membrane complex involved in electron transport to nitrogenase Mol Gen Genet 241 602 615 1:CAS:528: DyaK2cXltVSrurY%3D 8264535 (Pubitemid 24003880)
27. Y Jouanneau HS Jeong N Hugo C Meyer JC Willison 1998 Overexpression in Escherichia coli of the rnf genes from Rhodobacter capsulatus: characterization of two membrane-bound iron-sulfur proteins Eur J Biochem 251 54 64 1:CAS:528:DyaK1cXnvV2mtQ%3D%3D 9492268 (Pubitemid 28080898)
28. MS Koo JH Lee SY Rah WS Yeo JW Lee KL Lee YS Koh SO Kang JH Roe 2003 A reducing system of the superoxide sensor SoxR in Escherichia coli EMBO J 22 2614 2622 1:CAS:528:DC%2BD3sXkt1Wrtrs%3D 12773378
29. Y Yan J Yang Y Dou M Chen S Ping J Peng W Lu W Zhang Z Yao H Li W Liu S He L Geng X Zhang F Yang H Yu Y Zhan D Li Z Lin Y Wang C Elmerich M Lin Q Jin 2008 Nitrogen fixation island and rhizosphere competence traits in the genome of root-associated Pseudomonas stutzeri A1501 Proc Natl Acad Sci USA 105 7564 7569 1:CAS:528:DC%2BD1cXmvFKksbk%3D 18495935 (Pubitemid 351830058)
30. L Curatti CS Brown PW Ludden LM Rubio 2005 Genes required for rapid expression of nitrogenase activity in Azotobacter vinelandii Proc Natl Acad Sci USA 102 6291 6296 1:CAS:528:DC%2BD2MXktlygsb0%3D 15845763 (Pubitemid 40617436)
31. CM Gifford SS Wallace 2000 The genes encoding endonuclease VIII and endonuclease III in Escherichia coli are transcribed as the terminal genes in operons Nucleic Acids Res 28 762 769 1:CAS:528:DC%2BD3cXhtVSnt74%3D 10637328 (Pubitemid 30068260)
32. H Brüggemann S Bäumer WF Fricke A Wiezer H Liesegang I Decker C Herzberg R Martinez-Arias R Merkl A Henne G Gottschalk 2003 The genome sequence of Clostridium tetani, the causative agent of tetanus disease Proc Natl Acad Sci USA 100 1316 1321 12552129 (Pubitemid 36183999)
33. H Seedorf WF Fricke B Veith H Brüggemann H Liesegang A Strittmatter M Miethke W Buckel J Hinderberger F Li C Hagemeier RK Thauer G Gottschalk 2008 The genome of Clostridium kluyveri, a strict anaerobe with unique metabolic features Proc Natl Acad Sci USA 105 2128 2133 1:CAS:528:DC%2BD1cXitl2ls70%3D 18218779 (Pubitemid 351439476)
34. Q Li L Li T Rejtar DJ Lessner BL Karger JG Ferry 2006 Electron transport in the pathway of acetate conversion to methane in the marine archaeon Methanosarcina acetivorans J Bacteriol 188 702 710 1:CAS:528: DC%2BD28Xms1OhsQ%3D%3D 16385060 (Pubitemid 43100558)
35. HS Jeong Y Jouanneau 2000 Enhanced nitrogenase activity in strains of Rhodobacter capsulatus that overexpress the rnf genes J Bacteriol 182 1208 1214 1:CAS:528:DC%2BD3cXhtF2ltLo%3D 10671439 (Pubitemid 30104395)
36. H Kumagai T Fujiwara H Matsubara K Saeki 1997 Membrane localization, topology, and mutual stabilization of the rnfABC gene products in Rhodobacter capsulatus and implications for a new family of energy-coupling NADH oxidoreductases Biochemistry 36 5509 5521 1:CAS:528:DyaK2sXisFCjsbY%3D 9154934 (Pubitemid 27200048)
37. CD Boiangiu E Jayamani D Brügel G Herrmann J Kim L Forzi R Hedderich I Vgenopoulou AJ Pierik J Steuber W Buckel 2005 Sodium ion pumps and hydrogen production in glutamate fermenting anaerobic bacteria J Mol Microbiol Biotechnol 10 105 119 1:CAS:528:DC%2BD28XjvFSmt70%3D 16645308 (Pubitemid 43800686)
38. J Kim M Hetzel CD Boiangiu W Buckel 2004 Dehydration of (R)-2-hydroxyacyl-CoA to enoyl-CoA in the fermentation of alpha-amino acids by anaerobic bacteria FEMS Microbiol Rev 28 455 468 1:CAS:528:DC%2BD2cXnslGhsLk%3D 15374661 (Pubitemid 39209466)
39. +-translocating NADH-quinone reductase from Vibrio alginolyticus FEBS Lett 474 165 168 1:CAS:528:DC%2BD3cXjs1Chtrc%3D 10838078 (Pubitemid 30330827)
40. T Yagi 1993 The bacterial energy-transducing NADH-quinone oxidoreductases Biochim Biophys Acta 1141 1 17 1:CAS:528:DyaK3sXhsVait7s%3D 8435434 (Pubitemid 23051546)
41. T Yagi T Yano A Matsuno-Yagi 1993 Characteristics of the energy-transducing NADH-quinone oxidoreductase of Paracoccus denitrificans as revealed by biochemical, biophysical, and molecular biological approaches J Bioenerg Biomembr 25 339 345 1:CAS:528:DyaK3sXmsVCisrY%3D 8226715
42. JE Walker 1992 The NADH: ubiquinone oxidoreductase (Complex-I) of respiratory chains Q Rev Biophys 25 253 324 1:CAS:528:DyaK3sXps1KktQ%3D%3D 1470679 (Pubitemid 23014370)
43. IM Fearnley JE Walker 1992 Conservation of sequences of subunits of mitochondrial complex I and their relationships with other proteins Biochim Biophys Acta 1140 105 134 1:CAS:528:DyaK3sXhtF2gtL4%3D 1445936
44. A Tran-Betcke U Warnecke C Böcker C Zaborosch B Friedrich 1990 Cloning and nucleotide sequences of the genes for the subunits of NAD-reducing hydrogenase of Alcaligenes eutrophus H16 J Bacteriol 172 2920 2929 1:CAS:528:DyaK3cXlt1OhtLc%3D 2188945 (Pubitemid 20179737)
45. O Schmitz G Boison R Hilscher B Hundeshagen W Zimmer F Lottspeich H Bothe 1995 Molecular biological analysis of a bidirectional hydrogenase from cyanobacteria Eur J Biochem 233 266 276 1:CAS:528:DyaK2MXptVCgs74%3D 7588754
46. S Malki I Saimmaime G De Luca M Rousset Z Dermoun JP Belaich 1995 Characterization of an operon encoding an NADP-reducing hydrogenase in Desulfovibrio fructosovorans J Bacteriol 177 2628 2636 1:STN:280: DyaK2M3ntVGktQ%3D%3D 7751270
47. J Backiel O Juarez DV Zagorevski Z Wang MJ Nilges B Barquera 2008 Covalent binding of flavins to RnfG and RnfD in the Rnf complex from Vibrio cholerae Biochemistry 47 11273 11284 1:CAS:528:DC%2BD1cXhtF2isrzM 18831535
48. +-pumping NADH: quinone oxidoreductase from Vibrio cholerae by PhoA-green fluorescent protein fusion analysis J Bacteriol 188 8343 8351 1:CAS:528:DC%2BD28XhtlejtrfN 17041063 (Pubitemid 44894033)
49. A Sääf M Johansson E Wallin G von Heijne 1999 Divergent evolution of membrane protein topology: the Escherichia coli RnfA and RnfE homologues Proc Natl Acad Sci USA 96 8540 8544 10411911 (Pubitemid 29354827)
50. E Otaka T Ooi 1987 Examination of protein sequence homologies: IV. Twenty-seven bacterial ferredoxins J Mol Evol 26 257 267 1:CAS:528: DyaL1cXht1Kqu7o%3D 3129571
51. I Quinkal V Davasse J Gaillard JM Moulis 1994 On the role of conserved proline residues in the structure and function of Clostridium pasteurianum 2[4Fe-4S] ferredoxin Protein Eng 7 681 687 1:CAS:528:DyaK2cXltVagsbk%3D 8073038 (Pubitemid 24150077)
52. S Kerscher S Dröse V Zickermann U Brandt 2008 The three families of respiratory NADH dehydrogenases Results Probl Cell Differ 45 185 222 1:CAS:528:DC%2BD1cXhtFSrt7zK 17514372
53. +-pumping NADH:quinone oxidoreductase from Vibrio cholerae involved in sodium translocation Biochemistry 48 9516 9524 1:CAS:528:DC%2BD1MXhtFemu7jL 19694431
54. +- dependent F-ATP synthases J Mol Biol 391 498 507 1:CAS:528:DC%2BD1MXptVeitro%3D 19500592
55. +-ATPase from Ilyobacter tartaricus Science 308 659 662 1:CAS:528:DC%2BD2MXjsFyktbY%3D 15860619 (Pubitemid 40594380)
56. O-ATPase operon from Acetobacterium woodii. Operon structure and presence of multiple copies of atpE which encode proteolipids of 8- and 18-kDa J Biol Chem 274 33999 34004 1:CAS:528:DyaK1MXnslOlurc%3D 10567365 (Pubitemid 129511731)
57. + specificity as revealed by sequence comparisons FEBS Lett 404 269 271 1:CAS:528:DyaK2sXhsFKkt7s%3D 9119076 (Pubitemid 27113465)
58. + binding FEBS Lett 453 35 40 1:CAS:528:DyaK1MXkt1CqtbY%3D 10403370 (Pubitemid 29335468)
59. Altendorf K, Siebers A, Epstein W (1992) The Kdp ATPase of Escherichia coli. In: Scarpa A, Carafoli E, Papa S (eds) Ion: motive ATPases: structure, function, and regulation, vol 671. Annals of the New York Academy of Sciences, New York, NY, USA, pp 228-243 (Pubitemid 23087655)
60. O complex Annu Rev Microbiol 50 791 824 1:CAS:528:DyaK28XmtFGht7w%3D 8905099 (Pubitemid 26337482)
61. 0-ATP synthases: glimpses of interacting parts in a dynamic molecular machine J Exp Biol 200 217 224 1:CAS:528:DyaK2sXhslOnsL4%3D 9050229 (Pubitemid 27126452)
62. RK Thauer K Jungermann K Decker 1977 Energy conservation in chemotrophic anaerobic bacteria Bact Rev 41 100 180 1:CAS:528:DyaE2sXktVajtLs%3D 860983 (Pubitemid 8082287)
63. Anthony C (1988) Quinoproteins and energy transduction. In: Anthony C (ed) Bacterial energy transduction. Academic, New York, pp 293-316
64. AB Hooper T Vannelli DJ Bergmann DM Arciero 1997 Enzymology of the oxidation of ammonia to nitrite by bacteria Antonie Van Leeuwenhoek 71 59 67 1:CAS:528:DyaK2sXhvVejurY%3D 9049018 (Pubitemid 27075764)
65. L Poughon CG Dussap JB Gros 2001 Energy model and metabolic flux analysis for autotrophic nitrifiers Biotechnol Bioeng 72 416 433 1:CAS:528: DC%2BD3MXhtVOht7o%3D 11180062
66. MI Aleem 1966 Generation of reducing power in chemosynthesis. II. Energy-linked reduction of pyridine nucleotides in the chemoautotroph, Nitrosomonas europaea Biochim Biophys Acta 113 216 224 1:CAS:528: DyaF28XmtV2gsw%3D%3D 4380274
67. DJ Arp LY Stein 2003 Metabolism of inorganic N compounds by ammonia-oxidizing bacteria Crit Rev Biochem Mol Biol 38 471 495 1:CAS:528:DC%2BD2cXhsVelsbg%3D 14695127 (Pubitemid 38091406)
68. Wood PM (1986) Nitrification as a bacterial energy source. In: Prosser JI (ed) Nitrification. IRL, Oxford, pp 39-62
69. RV Eck MO Dayhoff 1966 Evolution of the structure of ferredoxin based on living relics of primitive amino acid sequences Science 152 363 366 1:CAS:528:DyaF28XktFegtbo%3D 17775169
70. HP Blaschkowski G Neuer M Ludwig-Festl J Knappe 1982 Routes of flavodoxin and ferredoxin reduction in Escherichia coli. CoA-acylating pyruvate: flavodoxin and NADPH: flavodoxin oxidoreductases participating in the activation of pyruvate formate-lyase Eur J Biochem 123 563 569 1:CAS:528: DyaL38XhvFKgtrs%3D 7042345 (Pubitemid 12119181)
71. C Furdui SW Ragsdale 2000 The role of pyruvate ferredoxin oxidoreductase in pyruvate synthesis during autotrophic growth by the Wood-Ljungdahl pathway J Biol Chem 275 28494 28499 1:CAS:528:DC%2BD3cXms1Cru7s%3D 10878009
72. T Shanmugasundaram HG Wood 1992 Interaction of ferredoxin with carbon monoxide dehydrogenase from Clostridium thermoaceticum J Biol Chem 267 897 900 1:CAS:528:DyaK38XnvFajug%3D%3D 1730678
73. 2 reduction to formate in Clostridium pasteurianum Biochem Biophys Res Commun 41 682 689 1:CAS:528:DyaE3MXivFWmsQ%3D%3D 4394648
74. 2 via a new ferredoxin dependent monocarboxylic acid cycle FEBS Lett 8 304 307 1:CAS:528:DyaE3cXksFahsbw%3D 11947600
75. 2 storage Annu Rev Biochem 79 507 536 1:CAS:528:DC%2BC3cXpslShtrc%3D 20235826
76. R Hedderich 2004 Energy-converting [NiFe] hydrogenases from archaea and extremophiles: ancestors of complex I J Bioenerg Biomembr 36 65 75 1:CAS:528:DC%2BD2cXitVOit7Y%3D 15168611 (Pubitemid 38500761)
77. 2 with the phosphorylation of ADP in acetate-grown Methanosarcina barkeri Eur J Biochem 159 393 398 1:CAS:528:DyaL28XltlSnur0%3D 3093229
78. 2 in Methanosarcina barkeri Eur J Biochem 179 469 472 1:CAS:528:DyaL1MXhsFWjsbc%3D 2537211
79. Welte C, Krätzer C, Deppenmeier U (2010) Involvement of Ech hydrogenase in energy conservation of Methanosarcina mazei. FEBS J 277:3396-3403
80. RK Thauer AK Kaster H Seedorf W Buckel R Hedderich 2008 Methanogenic archaea: ecologically relevant differences in energy conservation Nat Rev Microbiol 6 579 591 1:CAS:528:DC%2BD1cXosFSktLs%3D 18587410
81. U Deppenmeier 2002 The unique biochemistry of methanogenesis Prog Nucleic Acid Res Mol Biol 71 223 283 1:CAS:528:DC%2BD38XnvFKnuro%3D 12102556
82. U Deppenmeier V Müller 2008 Life close to the thermodynamic limit: how methanogenic archaea conserve energy Results Probl Cell Differ 45 123 152 1:CAS:528:DC%2BD1cXhtFSrt7zI 17713742
83. R Sapra K Bagramyan MWW Adams 2003 A simple energy-conserving system: proton reduction coupled to proton translocation Proc Natl Acad Sci USA 100 7545 7550 1:CAS:528:DC%2BD3sXlt1Wrurw%3D 12792025 (Pubitemid 36760006)
84. O ATP synthase from the hyperthermophilic archaeon Pyrococcus furiosus FEBS J 274 3928 3938 1:CAS:528:DC%2BD2sXptFCnurw%3D 17614964 (Pubitemid 47087680)
85. T Friedrich D Scheide 2000 The respiratory complex I of bacteria, archaea and eukarya and its module common with membrane-bound multisubunit hydrogenases FEBS Lett 479 1 5 1:CAS:528:DC%2BD3cXlsFCit7w%3D 10940377 (Pubitemid 30625247)
86. T Friedrich H Weiss 1997 Modular evolution of the respiratory NADH:ubiquinone oxidoreductase and the origin of its modules J Theor Biol 187 529 540 1:CAS:528:DyaK2sXmtVGlsL4%3D 9299297
87. PM Vignais A Colbeau 2004 Molecular biology of microbial hydrogenases Curr Issues Mol Biol 6 159 188 1:CAS:528:DC%2BD2cXkt1ShtL0%3D 15119826 (Pubitemid 38541487)
88. U Brandt S Kerscher S Dröse K Zwicker V Zickermann 2003 Proton pumping by NADH:ubiquinone oxidoreductase. A redox driven conformational change mechanism? FEBS Lett 545 9 17 1:CAS:528:DC%2BD3sXkt1ymt7o%3D 12788486 (Pubitemid 36629630)
89. + is translocated at NADH:quinone oxidoreductase segment in the respiratory chain of Vibrio alginolyticus J Biol Chem 259 7785 7790 1:CAS:528:DyaL2cXks1Oqs7o%3D 6736026 (Pubitemid 14081195)
90. +-motive respiratory chain of marine bacteria Microbiol Sci 2 65 71 1:CAS:528:DyaL28XkvFChtbg%3D 2856376 (Pubitemid 16253949)
91. +-translocating NADH:quinone oxidoreductase from Vibrio cholerae Biochemistry 41 3781 3789 1:CAS:528:DC%2BD38XhsVCiurw%3D 11888296 (Pubitemid 34224692)
92. +-motive NADH oxidase in inverted membrane vesicles of Vibrio alginolyticus FEBS Lett 183 95 98 1:CAS:528:DyaL2MXhvF2ksbw%3D 2579856 (Pubitemid 15090136)
93. +-translocation by bacterial NADH:quinone oxidoreductases: an extension to the complex-I family of primary redox pumps Biochim Biophys Acta 1505 45 56 1:CAS:528:DC%2BD3MXhvVagsbk%3D 11248188 (Pubitemid 32204458)
94. +-translocating NADH-quinone reductase from the marine Vibrio alginolyticus Biochim Biophys Acta 1505 37 44 1:CAS:528:DC%2BD3MXhvVagsbg%3D 11248187 (Pubitemid 32204457)
95. +-translocating NADH-quinone reductase from Vibrio alginolyticus FEBS Lett 488 5 8 1:CAS:528:DC%2BD3MXksVejtQ%3D%3D 11163785 (Pubitemid 32332796)
96. +-pumping NADH-quinone oxidoreductase from Vibrio cholerae Proc Natl Acad Sci USA 99 10322 10324 1:CAS:528:DC%2BD38Xmt1Citbc%3D 12122213
97. + pump Biochemistry 35 6233 6242 1:CAS:528:DyaK28Xis1ars78%3D 8639563 (Pubitemid 26164051)
98. +-translocating NADH:ubiquinone oxidoreductase from Vibrio harveyi Biochemistry 38 16246 16252 1:CAS:528:DyaK1MXntFGmsb4%3D 10587447 (Pubitemid 129520545)
99. U Brandt 2006 Energy converting NADH:quinone oxidoreductase (complex I) Annu Rev Biochem 75 69 92 1:CAS:528:DC%2BD28XosVKhsr0%3D 16756485 (Pubitemid 44118026)
100. +-translocating NADH:quinone oxidoreductase from Vibrio cholerae: functional role of the NqrF subunit J Biol Chem 279 21349 21355 15010474 (Pubitemid 38656543)
101. CC Häse B Barquera 2001 Role of sodium bioenergetics in Vibrio cholerae Biochim Biophys Acta 1505 169 178 11248198 (Pubitemid 32204468)
102. CC Häse JJ Mekalanos 1999 Effects of changes in membrane sodium flux on virulence gene expression in Vibrio cholerae Proc Natl Acad Sci USA 96 3183 3187 10077658 (Pubitemid 29148865)
103. O-ATPase with a mixed oligomer of 8 and 16 kDa proteolipids Biochim Biophys Acta 1505 108 120 11248193 (Pubitemid 32204463)
104. Müller V, Gottschalk G (1994) The sodium ion cycle in acetogenic and methanogenic bacteria: generation and utilization of a primary electrochemical sodium ion gradient. In: Drake HL (ed) Acetogenesis. Chapman & Hall, New York, pp 127-156
105. M Köpke C Held S Hujer H Liesegang A Wiezer A Wollherr A Ehrenreich W Liebl G Gottschalk P Dürre 2010 Clostridium ljungdahlii represents a microbial production platform based on syngas Proc Natl Acad Sci USA 107 13087 13092 20616070
106. S Stolpe T Friedrich 2004 The Escherichia coli NADH:ubiquinone oxidoreductase (complex I) is a primary proton pump but may be capable of secondary sodium antiport J Biol Chem 279 18377 18383 1:CAS:528: DC%2BD2cXjsVKntbc%3D 14970214 (Pubitemid 38623253)
107. +-translocation by the NADH:ubiquinone oxidoreductase (complex I) from Klebsiella pneumoniae Mol Microbiol 33 590 598 1:CAS:528:DyaK1MXlslSjurw%3D 10417649 (Pubitemid 29387183)
108. AC Gemperli P Dimroth J Steuber 2003 Sodium ion cycling mediates energy coupling between complex I and ATP synthase Proc Natl Acad Sci USA 100 839 844 1:CAS:528:DC%2BD3sXhtF2gsrs%3D 12538874 (Pubitemid 36183917)
109. BJ Efiok DA Webster 1990 A cytochrome that can pump sodium ion Biochem Biophys Res Commun 173 370 375 1:CAS:528:DyaK3MXjsl2jtA%3D%3D 2256929
110. PC Hallenbeck PM Vignais 1981 The effect of electron transport inhibitors on nitrogenase activity in the photosynthetic bacterium, Rhodopseudomonas capsulata FEMS Microbiol Lett 12 15 18 1:CAS:528:DyaL3MXlvVWmur8%3D (Pubitemid 12226343)
111. GW Schmidt KS Matlin NH Chua 1977 A rapid procedure for selective enrichment of photosynthetic electron transport mutants Proc Natl Acad Sci USA 74 610 614 1:CAS:528:DyaE2sXhtFOku7k%3D 265526 (Pubitemid 8038773)
112. K Saeki H Kumagai 1998 The rnf gene products in Rhodobacter capsulatus play an essential role in nitrogen fixation during anaerobic DMSO-dependent growth in the dark Arch Microbiol 169 464 467 1:CAS:528:DyaK1cXjsFSnt78%3D 9560429 (Pubitemid 28204290)
113. N Desnoues M Lin X Guo L Ma R Carreño-Lopez C Elmerich 2003 Nitrogen fixation genetics and regulation in a Pseudomonas stutzeri strain associated with rice Microbiology 149 2251 2262 1:CAS:528:DC%2BD3sXmslaqtrg%3D 12904565 (Pubitemid 37038431)
114. RP Cunningham H Asahara JF Bank CP Scholes JC Salerno K Surerus E Munck J McCracken J Peisach MH Emptage 1989 Endonuclease III is an iron-sulfur protein Biochemistry 28 4450 4455 1:CAS:528:DyaL1MXitVyntr4%3D 2548577 (Pubitemid 19141656)
115. SM Faruque GB Nair 2002 Molecular ecology of toxigenic Vibrio cholerae Microbiol Immunol 46 59 66 1:CAS:528:DC%2BD38Xitl2rtrw%3D 11939579 (Pubitemid 34194963)
116. H Brüggemann G Gottschalk 2004 Insights in metabolism and toxin production from the complete genome sequence of Clostridium tetani Anaerobe 10 53 68 16701501 (Pubitemid 38519805)
117. F Li J Hinderberger H Seedorf J Zhang W Buckel RK Thauer 2008 Coupled ferredoxin and crotonyl coenzyme A (CoA) reduction with NADH catalyzed by the butyryl-CoA dehydrogenase/Etf complex from Clostridium kluyveri J Bacteriol 190 843 850 1:CAS:528:DC%2BD1cXhsFShu7Y%3D 17993531 (Pubitemid 351170927)
118. G Herrmann E Jayamani G Mai W Buckel 2008 Energy conservation via electron-transferring flavoprotein in anaerobic bacteria J Bacteriol 190 784 791 1:CAS:528:DC%2BD1cXhsFShu78%3D 18039764 (Pubitemid 351170920)
119. U Brandt 1996 Bifurcated ubihydroquinone oxidation in the cytochrome bc1 complex by proton-gated charge transfer FEBS Lett 387 1 6 1:CAS:528: DyaK28XjtlSktbs%3D 8654557 (Pubitemid 26170729)
120. Schut GJ, Adams MW (2009) The iron hydrogenase of Thermotoga maritima utilizes ferredoxin and NADH synergistically: a new perspective on anaerobic hydrogen production. J Bacteriol 191:4451-4457
121. MJ McInerney L Rohlin H Mouttaki U Kim RS Krupp L Rios-Hernandez J Sieber CG Struchtemeyer A Bhattacharyya JW Campbell RP Gunsalus 2007 The genome of Syntrophus aciditrophicus: life at the thermodynamic limit of microbial growth Proc Natl Acad Sci USA 104 7600 7605 17442750 (Pubitemid 47185952)
122. W Badziong RK Thauer JG Zeikus 1978 Isolation and characterization of Desulfovibrio growing on hydrogen plus sulfate as the sole energy source Arch Microbiol 116 41 49 1:CAS:528:DyaE1cXhtFOlsr0%3D 623496 (Pubitemid 8310599)
123. W Badziong RK Thauer 1978 Growth yields and growth rates of Desulfovibrio vulgaris (Marburg) growing on hydrogen plus sulfate and hydrogen plus thiosulfate as the sole energy sources Arch Microbiol 117 209 214 1:CAS:528:DyaE1cXltVentr4%3D 28099 (Pubitemid 8354231)
124. AW Strittmatter H Liesegang R Rabus I Decker J Amann S Andres A Henne WF Fricke R Martinez-Arias D Bartels A Goesmann L Krause A Pühler HP Klenk M Richter M Schüler FO Glöckner A Meyerdierks G Gottschalk R Amann 2009 Genome sequence of Desulfobacterium autotrophicum HRM2, a marine sulfate reducer oxidizing organic carbon completely to carbon dioxide Environ Microbiol 11 1038 1055 1:CAS:528:DC%2BD1MXmsVeqtrs%3D 19187283
125. JG Ferry 1992 Biochemistry of methanogenesis Crit Rev Biochem Mol Biol 27 473 503 1:CAS:528:DyaK3sXht1Smsr4%3D 1473352
126. Rother M (2010) Methanogenesis. In: Timmis KN (ed) Handbook of hydrocarbon and lipid microbiology. Springer, Berlin, pp 483-499
127. 2 by Methanosarcina barkeri Eur J Biochem 178 519 525 2850182
128. +-translocating methyltransferase complex from methanogenic archaea Biochim Biophys Acta 1505 28 36 1:CAS:528:DC%2BD3MXhvVagsbs%3D 11248186 (Pubitemid 32204456)
129. U Deppenmeier 2002 Redox-driven proton translocation in methanogenic archaea Cell Mol Life Sci 59 1 21
130. L Rohlin RP Gunsalus 2010 Carbon-dependent control of electron transfer and central carbon pathway genes for methane biosynthesis in the Archaean, Methanosarcina acetivorans strain C2A BMC Microbiol 10 62 20178638
131. PD Franzmann N Springer W Ludwig E Conway de Macario M Rohde 1992 A methanogenic archaeon from Ace lake, antarctica: Methanococcoides burtonii sp. nov Syst Appl Microbiol 15 573 581 (Pubitemid 23036071)
132. T Hirokawa S Boon-Chieng S Mitaku 1998 SOSUI: classification and secondary structure prediction system for membrane proteins Bioinformatics 14 378 379 1:CAS:528:DyaK1cXks12gt70%3D 9632836 (Pubitemid 28393805)
133. MA Larkin G Blackshields NP Brown R Chenna PA McGettigan H McWilliam F Valentin IM Wallace A Wilm R Lopez JD Thompson TJ Gibson DG Higgins 2007 Clustal W and Clustal X version 2.0 Bioinformatics 23 2947 2948 1:CAS:528: DC%2BD2sXhtlaqsL%2FM 17846036 (Pubitemid 350162903)