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

• Drake HL, Daniel S, Küsel K, Matthies C, Kuhner C, Braus-Strohmeyer S (1997) Acetogenic bacteria: what are the in situ consequences of their diverse metabolic diversities? Biofactors 1:13–24
  Google Scholar
• 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
  Google Scholar
• Ragsdale SW (2008) Enzymology of the Wood–Ljungdahl pathway of acetogenesis. Ann N Y Acad Sci 1125:129–136
  CAS PubMed Google Scholar
• Diekert G, Wohlfarth G (1994) Metabolism of homoacetogens. Antonie van Leeuwenhoek Int J Gen M 66:209–221
  CAS Google Scholar
• Ragsdale SW, Pierce E (2008) Acetogenesis and the Wood–Ljungdahl pathway of CO2 fixation. Biochim Biophys Acta 1784:1873–1898
  CAS PubMed Google Scholar
• Eichler B, Schink B (1984) Oxidation of primary aliphatic alcolhols by Acetobacterium carbinolicum sp. nov., a homoacetogenic anaerobe. Arch Microbiol 140:147–152
  CAS Google Scholar
• Bache R, Pfennig N (1981) Selective isolation of Acetobacterium woodii on methoxylated aromatic acids and determination of growth yields. Arch Microbiol 130:255–261
  CAS Google Scholar
• Müller V (2003) Energy conservation in acetogenic bacteria. Appl Environ Microbiol 69:6345–6353
  PubMed Google Scholar
• Imkamp F, Müller V (2002) Chemiosmotic energy conservation with Na+ as the coupling ion during hydrogen-dependent caffeate reduction by Acetobacterium woodii. J Bacteriol 184:1947–1951
  CAS PubMed Google Scholar
• Heise R, Müller V, Gottschalk G (1992) Presence of a sodium-translocating ATPase in membrane vesicles of the homoacetogenic bacterium Acetobacterium woodii. Eur J Biochem 206:553–557
  CAS PubMed Google Scholar
• Reidlinger J, Müller V (1994) Purification of ATP synthase from Acetobacterium woodii and identification as a Na+-translocating F1FO-type enzyme. Eur J Biochem 223:275–283
  CAS PubMed Google Scholar
• Fritz M, Klyszejko AL, Morgner N, Vonck J, Brutschy B, Müller DJ, Meier T, Müller V (2008) An intermediate step in the evolution of ATPases: a hybrid F1FO rotor in a bacterial Na+ F1FO ATP synthase. FEBS J 275:1999–2007
  CAS PubMed Google Scholar
• Fritz M, Müller V (2007) An intermediate step in the evolution of ATPases: the F1FO-ATPase from Acetobacterium woodii contains F-type and V-type rotor subunits and is capable of ATP synthesis. FEBS J 274:3421–3428
  CAS PubMed Google Scholar
• Müller V, Bowien S (1995) Differential effects of sodium ions on motility in the homoacetogenic bacteria Acetobacterium woodii and Sporomusa sphaeroides. Arch Microbiol 164:363–369
  Google Scholar
• Schmidt S, Biegel E, Müller V (2009) The ins and outs of Na+ bioenergetics in Acetobacterium woodii. Biochim Biophys Acta 1787:691–696
  CAS PubMed Google Scholar
• Seifritz C, Daniel SL, Gössner A, Drake HL (1993) Nitrate as a preferred electron sink for the acetogen Clostridium thermoaceticum. J Bacteriol 175:8008–8013
  CAS PubMed Google Scholar
• Fröstl JM, Seifritz C, Drake HL (1996) Effect of nitrate on the autotrophic metabolism of the acetogens Clostridium thermoautotrophicum and Clostridium thermoaceticum. J Bacteriol 178:4597–4603
  PubMed Google Scholar
• Tschech A, Pfennig N (1984) Growth yield increase linked to caffeate reduction in Acetobacterium woodii. Arch Microbiol 137:163–167
  CAS Google Scholar
• Müller V, Imkamp F, Biegel E, Schmidt S, Dilling S (2008) Discovery of a ferredoxin:NAD+-oxidoreductase (Rnf) in Acetobacterium woodii: a novel potential coupling site in acetogens. Ann N Y Acad Sci 1125:137–146
  PubMed Google Scholar
• Blum U, Wentworth TR, Klein K, Worsham AD, King LD, Gerig TM, Lyu S-W (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
  CAS Google Scholar
• Hansen B, Bokranz M, Schönheit P, Kröger A (1988) ATP formation coupled to caffeate reduction by H2 in Acetobacterium woodii NZva16. Arch Microbiol 150:447–451
  CAS Google Scholar
• Imkamp F, Biegel E, Jayamani E, Buckel W, Müller V (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
  CAS PubMed Google Scholar
• Ragsdale SW, Ljungdahl LG (1984) Hydrogenase from Acetobacterium woodii. Arch Microbiol 139:361–365
  CAS PubMed Google Scholar
• Biegel E, Müller V (2010) A bacterial Na+-translocating ferredoxin:NAD+ oxidoreductase. Proc Natl Acad Sci USA 107:18138–18142
  Google Scholar
• Biegel E, Schmidt S, Müller V (2009) Genetic, immunological and biochemical evidence of a Rnf complex in the acetogen Acetobacterium woodii. Environ Microbiol 11:1438–1443
  CAS PubMed Google Scholar
• Schmehl M, Jahn A, Meyer zu Vilsendorf A, Hennecke S, Masepohl B, Schuppler M, Marxer M, Oelze J, Klipp W (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
  CAS PubMed Google Scholar
• Jouanneau Y, Jeong HS, Hugo N, Meyer C, Willison JC (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
  CAS PubMed Google Scholar
• Koo MS, Lee JH, Rah SY, Yeo WS, Lee JW, Lee KL, Koh YS, Kang SO, Roe JH (2003) A reducing system of the superoxide sensor SoxR in Escherichia coli. EMBO J 22:2614–2622
  CAS PubMed Google Scholar
• Yan Y, Yang J, Dou Y, Chen M, Ping S, Peng J, Lu W, Zhang W, Yao Z, Li H, Liu W, He S, Geng L, Zhang X, Yang F, Yu H, Zhan Y, Li D, Lin Z, Wang Y, Elmerich C, Lin M, Jin Q (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
  CAS PubMed Google Scholar
• Curatti L, Brown CS, Ludden PW, Rubio LM (2005) Genes required for rapid expression of nitrogenase activity in Azotobacter vinelandii. Proc Natl Acad Sci USA 102:6291–6296
  CAS PubMed Google Scholar
• Gifford CM, Wallace SS (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
  CAS PubMed Google Scholar
• Brüggemann H, Bäumer S, Fricke WF, Wiezer A, Liesegang H, Decker I, Herzberg C, Martinez-Arias R, Merkl R, Henne A, Gottschalk G (2003) The genome sequence of Clostridium tetani, the causative agent of tetanus disease. Proc Natl Acad Sci USA 100:1316–1321
  PubMed Google Scholar
• Seedorf H, Fricke WF, Veith B, Brüggemann H, Liesegang H, Strittmatter A, Miethke M, Buckel W, Hinderberger J, Li F, Hagemeier C, Thauer RK, Gottschalk G (2008) The genome of Clostridium kluyveri, a strict anaerobe with unique metabolic features. Proc Natl Acad Sci USA 105:2128–2133
  CAS PubMed Google Scholar
• Li Q, Li L, Rejtar T, Lessner DJ, Karger BL, Ferry JG (2006) Electron transport in the pathway of acetate conversion to methane in the marine archaeon Methanosarcina acetivorans. J Bacteriol 188:702–710
  CAS PubMed Google Scholar
• Jeong HS, Jouanneau Y (2000) Enhanced nitrogenase activity in strains of Rhodobacter capsulatus that overexpress the rnf genes. J Bacteriol 182:1208–1214
  CAS PubMed Google Scholar
• Kumagai H, Fujiwara T, Matsubara H, Saeki K (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
  CAS PubMed Google Scholar
• Boiangiu CD, Jayamani E, Brügel D, Herrmann G, Kim J, Forzi L, Hedderich R, Vgenopoulou I, Pierik AJ, Steuber J, Buckel W (2005) Sodium ion pumps and hydrogen production in glutamate fermenting anaerobic bacteria. J Mol Microbiol Biotechnol 10:105–119
  CAS PubMed Google Scholar
• Kim J, Hetzel M, Boiangiu CD, Buckel W (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
  CAS PubMed Google Scholar
• Nakayama Y, Yasui M, Sugahara K, Hayashi M, Unemoto T (2000) Covalently bound flavin in the NqrB and NqrC subunits of Na+-translocating NADH-quinone reductase from Vibrio alginolyticus. FEBS Lett 474:165–168
  CAS PubMed Google Scholar
• Yagi T (1993) The bacterial energy-transducing NADH-quinone oxidoreductases. Biochim Biophys Acta 1141:1–17
  CAS PubMed Google Scholar
• Yagi T, Yano T, Matsuno-Yagi A (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
  CAS PubMed Google Scholar
• Walker JE (1992) The NADH: ubiquinone oxidoreductase (Complex-I) of respiratory chains. Q Rev Biophys 25:253–324
  CAS PubMed Google Scholar
• Fearnley IM, Walker JE (1992) Conservation of sequences of subunits of mitochondrial complex I and their relationships with other proteins. Biochim Biophys Acta 1140:105–134
  CAS PubMed Google Scholar
• Tran-Betcke A, Warnecke U, Böcker C, Zaborosch C, Friedrich B (1990) Cloning and nucleotide sequences of the genes for the subunits of NAD-reducing hydrogenase of Alcaligenes eutrophus H16. J Bacteriol 172:2920–2929
  CAS PubMed Google Scholar
• Schmitz O, Boison G, Hilscher R, Hundeshagen B, Zimmer W, Lottspeich F, Bothe H (1995) Molecular biological analysis of a bidirectional hydrogenase from cyanobacteria. Eur J Biochem 233:266–276
  CAS PubMed Google Scholar
• Malki S, Saimmaime I, De Luca G, Rousset M, Dermoun Z, Belaich JP (1995) Characterization of an operon encoding an NADP-reducing hydrogenase in Desulfovibrio fructosovorans. J Bacteriol 177:2628–2636
  CAS PubMed Google Scholar
• Backiel J, Juarez O, Zagorevski DV, Wang Z, Nilges MJ, Barquera B (2008) Covalent binding of flavins to RnfG and RnfD in the Rnf complex from Vibrio cholerae. Biochemistry 47:11273–11284
  CAS PubMed Google Scholar
• Duffy EB, Barquera B (2006) Membrane topology mapping of the Na+-pumping NADH: quinone oxidoreductase from Vibrio cholerae by PhoA-green fluorescent protein fusion analysis. J Bacteriol 188:8343–8351
  CAS PubMed Google Scholar
• Sääf A, Johansson M, Wallin E, von Heijne G (1999) Divergent evolution of membrane protein topology: the Escherichia coli RnfA and RnfE homologues. Proc Natl Acad Sci USA 96:8540–8544
  PubMed Google Scholar
• Otaka E, Ooi T (1987) Examination of protein sequence homologies: IV. Twenty-seven bacterial ferredoxins. J Mol Evol 26:257–267
  CAS PubMed Google Scholar
• Quinkal I, Davasse V, Gaillard J, Moulis JM (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
  CAS PubMed Google Scholar
• Kerscher S, Dröse S, Zickermann V, Brandt U (2008) The three families of respiratory NADH dehydrogenases. Results Probl Cell Differ 45:185–222
  CAS PubMed Google Scholar
• Juarez O, Athearn K, Gillespie P, Barquera B (2009) Acid residues in the transmembrane helices of the Na+-pumping NADH:quinone oxidoreductase from Vibrio cholerae involved in sodium translocation. Biochemistry 48:9516–9524
  CAS PubMed Google Scholar
• Meier T, Krah A, Bond PJ, Pogoryelov D, Diederichs K, Faraldo-Gomez JD (2009) Complete ion-coordination structure in the rotor ring of Na+-dependent F-ATP synthases. J Mol Biol 391:498–507
  CAS PubMed Google Scholar
• Meier T, Polzer P, Diederichs K, Welte W, Dimroth P (2005) Structure of the rotor ring of F-Type Na+-ATPase from Ilyobacter tartaricus. Science 308:659–662
  CAS PubMed Google Scholar
• Rahlfs S, Aufurth S, Müller V (1999) The Na+-F1FO-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
  CAS PubMed Google Scholar
• Rahlfs S, Müller V (1997) Sequence of subunit c of the Na+-translocating F1FO ATPase of Acetobacterium woodii: proposal for determinants of Na+ specificity as revealed by sequence comparisons. FEBS Lett 404:269–271
  CAS PubMed Google Scholar
• Rahlfs S, Müller V (1999) Sequence of subunit a of the Na+-translocating F1FO-ATPase of Acetobacterium woodii: proposal for residues involved in Na+ binding. FEBS Lett 453:35–40
  CAS PubMed Google Scholar
• 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
• Deckers-Hebestreit G, Altendorf K (1996) The F0F1-type ATP synthases of bacteria: structure and function of the FO complex. Annu Rev Microbiol 50:791–824
  CAS PubMed Google Scholar
• Fillingame RH (1997) Coupling H+ transport and ATP synthesis ln F1F0-ATP synthases: glimpses of interacting parts in a dynamic molecular machine. J Exp Biol 200:217–224
  CAS PubMed Google Scholar
• Thauer RK, Jungermann K, Decker K (1977) Energy conservation in chemotrophic anaerobic bacteria. Bact Rev 41:100–180
  CAS PubMed Google Scholar
• Anthony C (1988) Quinoproteins and energy transduction. In: Anthony C (ed) Bacterial energy transduction. Academic, New York, pp 293–316
  Google Scholar
• Hooper AB, Vannelli T, Bergmann DJ, Arciero DM (1997) Enzymology of the oxidation of ammonia to nitrite by bacteria. Antonie Van Leeuwenhoek 71:59–67
  CAS PubMed Google Scholar
• Poughon L, Dussap CG, Gros JB (2001) Energy model and metabolic flux analysis for autotrophic nitrifiers. Biotechnol Bioeng 72:416–433
  CAS PubMed Google Scholar
• Aleem MI (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
  CAS PubMed Google Scholar
• Arp DJ, Stein LY (2003) Metabolism of inorganic N compounds by ammonia-oxidizing bacteria. Crit Rev Biochem Mol Biol 38:471–495
  CAS PubMed Google Scholar
• Wood PM (1986) Nitrification as a bacterial energy source. In: Prosser JI (ed) Nitrification. IRL, Oxford, pp 39–62
  Google Scholar
• Eck RV, Dayhoff MO (1966) Evolution of the structure of ferredoxin based on living relics of primitive amino acid sequences. Science 152:363–366
  CAS PubMed Google Scholar
• Blaschkowski HP, Neuer G, Ludwig-Festl M, Knappe J (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
  CAS PubMed Google Scholar
• Furdui C, Ragsdale SW (2000) The role of pyruvate ferredoxin oxidoreductase in pyruvate synthesis during autotrophic growth by the Wood–Ljungdahl pathway. J Biol Chem 275:28494–28499
  CAS PubMed Google Scholar
• Shanmugasundaram T, Wood HG (1992) Interaction of ferredoxin with carbon monoxide dehydrogenase from Clostridium thermoaceticum. J Biol Chem 267:897–900
  CAS PubMed Google Scholar
• Jungermann K, Kirchniawy H, Thauer RK (1970) Ferredoxin dependent CO2 reduction to formate in Clostridium pasteurianum. Biochem Biophys Res Commun 41:682–689
  CAS PubMed Google Scholar
• Thauer RK, Rupprecht E, Jungermann K (1970) The synthesis of one-carbon units from CO2 via a new ferredoxin dependent monocarboxylic acid cycle. FEBS Lett 8:304–307
  CAS PubMed Google Scholar
• Thauer RK, Kaster AK, Goenrich M, Schick M, Hiromoto T, Shima S (2010) Hydrogenases from methanogenic archaea, nickel, a novel cofactor, and H2 storage. Annu Rev Biochem 79:507–536
  CAS PubMed Google Scholar
• Hedderich R (2004) Energy-converting [NiFe] hydrogenases from archaea and extremophiles: ancestors of complex I. J Bioenerg Biomembr 36:65–75
  CAS PubMed Google Scholar
• Bott M, Eikmanns B, Thauer RK (1986) Coupling of carbon monoxide oxidation to CO2 and H2 with the phosphorylation of ADP in acetate-grown Methanosarcina barkeri. Eur J Biochem 159:393–398
  CAS PubMed Google Scholar
• Bott M, Thauer RK (1989) Proton translocation coupled to the oxidation of carbon monoxide to CO2 and H2 in Methanosarcina barkeri. Eur J Biochem 179:469–472
  CAS PubMed Google Scholar
• Welte C, Krätzer C, Deppenmeier U (2010) Involvement of Ech hydrogenase in energy conservation of Methanosarcina mazei. FEBS J 277:3396–3403
  Google Scholar
• Thauer RK, Kaster AK, Seedorf H, Buckel W, Hedderich R (2008) Methanogenic archaea: ecologically relevant differences in energy conservation. Nat Rev Microbiol 6:579–591
  CAS PubMed Google Scholar
• Deppenmeier U (2002) The unique biochemistry of methanogenesis. Prog Nucleic Acid Res Mol Biol 71:223–283
  CAS PubMed Google Scholar
• Deppenmeier U, Müller V (2008) Life close to the thermodynamic limit: how methanogenic archaea conserve energy. Results Probl Cell Differ 45:123–152
  CAS PubMed Google Scholar
• Sapra R, Bagramyan K, Adams MWW (2003) A simple energy-conserving system: proton reduction coupled to proton translocation. Proc Natl Acad Sci USA 100:7545–7550
  CAS PubMed Google Scholar
• Pisa KY, Huber H, Thomm M, Müller V (2007) A sodium ion-dependent A1AO ATP synthase from the hyperthermophilic archaeon Pyrococcus furiosus. FEBS J 274:3928–3938
  CAS PubMed Google Scholar
• Friedrich T, Scheide D (2000) The respiratory complex I of bacteria, archaea and eukarya and its module common with membrane-bound multisubunit hydrogenases. FEBS Lett 479:1–5
  CAS PubMed Google Scholar
• Friedrich T, Weiss H (1997) Modular evolution of the respiratory NADH:ubiquinone oxidoreductase and the origin of its modules. J Theor Biol 187:529–540
  CAS PubMed Google Scholar
• Vignais PM, Colbeau A (2004) Molecular biology of microbial hydrogenases. Curr Issues Mol Biol 6:159–188
  CAS PubMed Google Scholar
• Brandt U, Kerscher S, Dröse S, Zwicker K, Zickermann V (2003) Proton pumping by NADH:ubiquinone oxidoreductase. A redox driven conformational change mechanism? FEBS Lett 545:9–17
  CAS PubMed Google Scholar
• Tokuda H, Unemoto T (1984) Na+ is translocated at NADH:quinone oxidoreductase segment in the respiratory chain of Vibrio alginolyticus. J Biol Chem 259:7785–7790
  CAS PubMed Google Scholar
• Tokuda H, Unemoto T (1985) The Na+-motive respiratory chain of marine bacteria. Microbiol Sci 2:65–71
  CAS PubMed Google Scholar
• Barquera B, Hellwig P, Zhou W, Morgan JE, Hase CC, Gosink KK, Nilges M, Bruesehoff PJ, Roth A, Lancaster CR, Gennis RB (2002) Purification and characterization of the recombinant Na+-translocating NADH:quinone oxidoreductase from Vibrio cholerae. Biochemistry 41:3781–3789
  CAS PubMed Google Scholar
• Tokuda H, Udagawa T, Unemoto T (1985) Generation of the electrochemical potential of Na+ by the Na+-motive NADH oxidase in inverted membrane vesicles of Vibrio alginolyticus. FEBS Lett 183:95–98
  CAS PubMed Google Scholar
• Steuber J (2001) Na+-translocation by bacterial NADH:quinone oxidoreductases: an extension to the complex-I family of primary redox pumps. Biochim Biophys Acta 1505:45–56
  CAS PubMed Google Scholar
• Hayashi M, Nakayama Y, Unemoto T (2001) Recent progress in the Na+-translocating NADH-quinone reductase from the marine Vibrio alginolyticus. Biochim Biophys Acta 1505:37–44
  CAS PubMed Google Scholar
• Hayashi M, Nakayama Y, Yasui M, Maeda M, Furuishi K, Unemoto T (2001) FMN is covalently attached to a threonine residue in the NqrB and NqrC subunits of Na+-translocating NADH-quinone reductase from Vibrio alginolyticus. FEBS Lett 488:5–8
  CAS PubMed Google Scholar
• Barquera B, Zhou W, Morgan JE, Gennis RB (2002) Riboflavin is a component of the Na+-pumping NADH-quinone oxidoreductase from Vibrio cholerae. Proc Natl Acad Sci USA 99:10322–10324
  CAS PubMed Google Scholar
• Pfenninger-Li XD, Albracht SPJ, Vanbelzen R, Dimroth P (1996) NADH:Ubiquinone oxidoreductase of Vibrio alginolyticus: Purification, properties, and reconstitution of the Na+ pump. Biochemistry 35:6233–6242
  CAS PubMed Google Scholar
• Zhou W, Bertsova YV, Feng B, Tsatsos P, Verkhovskaya ML, Gennis RB, Bogachev AV, Barquera B (1999) Sequencing and preliminary characterization of the Na+-translocating NADH:ubiquinone oxidoreductase from Vibrio harveyi. Biochemistry 38:16246–16252
  CAS PubMed Google Scholar
• Brandt U (2006) Energy converting NADH:quinone oxidoreductase (complex I). Annu Rev Biochem 75:69–92
  CAS PubMed Google Scholar
• Türk K, Puhar A, Neese F, Bill E, Fritz G, Steuber J (2004) NADH oxidation by the Na+-translocating NADH:quinone oxidoreductase from Vibrio cholerae: functional role of the NqrF subunit. J Biol Chem 279:21349–21355
  PubMed Google Scholar
• Häse CC, Barquera B (2001) Role of sodium bioenergetics in Vibrio cholerae. Biochim Biophys Acta 1505:169–178
  PubMed Google Scholar
• Häse CC, Mekalanos JJ (1999) Effects of changes in membrane sodium flux on virulence gene expression in Vibrio cholerae. Proc Natl Acad Sci USA 96:3183–3187
  PubMed Google Scholar
• Müller V, Aufurth S, Rahlfs S (2001) The Na+ cycle in Acetobacterium woodii: identification and characterization of a Na+-translocating F1FO-ATPase with a mixed oligomer of 8 and 16 kDa proteolipids. Biochim Biophys Acta 1505:108–120
  PubMed Google Scholar
• 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
  Google Scholar
• Köpke M, Held C, Hujer S, Liesegang H, Wiezer A, Wollherr A, Ehrenreich A, Liebl W, Gottschalk G, Dürre P (2010) Clostridium ljungdahlii represents a microbial production platform based on syngas. Proc Natl Acad Sci USA 107:13087–13092
  PubMed Google Scholar
• Stolpe S, Friedrich T (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
  CAS PubMed Google Scholar
• Krebs W, Steuber J, Gemperli AC, Dimroth P (1999) Na+-translocation by the NADH:ubiquinone oxidoreductase (complex I) from Klebsiella pneumoniae. Mol Microbiol 33:590–598
  CAS PubMed Google Scholar
• Gemperli AC, Dimroth P, Steuber J (2003) Sodium ion cycling mediates energy coupling between complex I and ATP synthase. Proc Natl Acad Sci USA 100:839–844
  CAS PubMed Google Scholar
• Efiok BJ, Webster DA (1990) A cytochrome that can pump sodium ion. Biochem Biophys Res Commun 173:370–375
  CAS PubMed Google Scholar
• Hallenbeck PC, Vignais PM (1981) The effect of electron transport inhibitors on nitrogenase activity in the photosynthetic bacterium, Rhodopseudomonas capsulata. FEMS Microbiol Lett 12:15–18
  CAS Google Scholar
• Schmidt GW, Matlin KS, Chua NH (1977) A rapid procedure for selective enrichment of photosynthetic electron transport mutants. Proc Natl Acad Sci USA 74:610–614
  CAS PubMed Google Scholar
• Saeki K, Kumagai H (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
  CAS PubMed Google Scholar
• Desnoues N, Lin M, Guo X, Ma L, Carreño-Lopez R, Elmerich C (2003) Nitrogen fixation genetics and regulation in a Pseudomonas stutzeri strain associated with rice. Microbiology 149:2251–2262
  CAS PubMed Google Scholar
• Cunningham RP, Asahara H, Bank JF, Scholes CP, Salerno JC, Surerus K, Munck E, McCracken J, Peisach J, Emptage MH (1989) Endonuclease III is an iron-sulfur protein. Biochemistry 28:4450–4455
  CAS PubMed Google Scholar
• Faruque SM, Nair GB (2002) Molecular ecology of toxigenic Vibrio cholerae. Microbiol Immunol 46:59–66
  CAS PubMed Google Scholar
• Brüggemann H, Gottschalk G (2004) Insights in metabolism and toxin production from the complete genome sequence of Clostridium tetani. Anaerobe 10:53–68
  PubMed Google Scholar
• Li F, Hinderberger J, Seedorf H, Zhang J, Buckel W, Thauer RK (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
  CAS PubMed Google Scholar
• Herrmann G, Jayamani E, Mai G, Buckel W (2008) Energy conservation via electron-transferring flavoprotein in anaerobic bacteria. J Bacteriol 190:784–791
  CAS PubMed Google Scholar
• Brandt U (1996) Bifurcated ubihydroquinone oxidation in the cytochrome bc1 complex by proton-gated charge transfer. FEBS Lett 387:1–6
  CAS PubMed Google Scholar
• 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
  Google Scholar
• McInerney MJ, Rohlin L, Mouttaki H, Kim U, Krupp RS, Rios-Hernandez L, Sieber J, Struchtemeyer CG, Bhattacharyya A, Campbell JW, Gunsalus RP (2007) The genome of Syntrophus aciditrophicus: life at the thermodynamic limit of microbial growth. Proc Natl Acad Sci USA 104:7600–7605
  PubMed Google Scholar
• Badziong W, Thauer RK, Zeikus JG (1978) Isolation and characterization of Desulfovibrio growing on hydrogen plus sulfate as the sole energy source. Arch Microbiol 116:41–49
  CAS PubMed Google Scholar
• Badziong W, Thauer RK (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
  CAS PubMed Google Scholar
• Strittmatter AW, Liesegang H, Rabus R, Decker I, Amann J, Andres S, Henne A, Fricke WF, Martinez-Arias R, Bartels D, Goesmann A, Krause L, Pühler A, Klenk HP, Richter M, Schüler M, Glöckner FO, Meyerdierks A, Gottschalk G, Amann R (2009) Genome sequence of Desulfobacterium autotrophicum HRM2, a marine sulfate reducer oxidizing organic carbon completely to carbon dioxide. Environ Microbiol 11:1038–1055
  CAS PubMed Google Scholar
• Ferry JG (1992) Biochemistry of methanogenesis. Crit Rev Biochem Mol Biol 27:473–503
  CAS PubMed Google Scholar
• Rother M (2010) Methanogenesis. In: Timmis KN (ed) Handbook of hydrocarbon and lipid microbiology. Springer, Berlin, pp 483–499
  Google Scholar
• Müller V, Winner C, Gottschalk G (1988) Electron transport-driven sodium extrusion during methanogenesis from formaldehyde + H2 by Methanosarcina barkeri. Eur J Biochem 178:519–525
  PubMed Google Scholar
• Gottschalk G, Thauer RK (2001) The Na+-translocating methyltransferase complex from methanogenic archaea. Biochim Biophys Acta 1505:28–36
  CAS PubMed Google Scholar
• Deppenmeier U (2002) Redox-driven proton translocation in methanogenic archaea. Cell Mol Life Sci 59:1–21
  Google Scholar
• Rohlin L, Gunsalus RP (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
  PubMed Google Scholar
• Franzmann PD, Springer N, Ludwig W, Conway de Macario E, Rohde M (1992) A methanogenic archaeon from Ace lake, antarctica: Methanococcoides burtonii sp. nov. Syst Appl Microbiol 15:573–581
  Google Scholar
• Hirokawa T, Boon-Chieng S, Mitaku S (1998) SOSUI: classification and secondary structure prediction system for membrane proteins. Bioinformatics 14:378–379
  CAS PubMed Google Scholar
• Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948
  CAS PubMed Google Scholar