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Vol. 16, No. 1-2, 2009
Issue release date: October 2008
Free Access
J Mol Microbiol Biotechnol 2009;16:38–52
(DOI:10.1159/000142893)

Genomic View of Energy Metabolism in Ralstonia eutropha H16

Cramm R.
Institut für Biologie, Humboldt-Universität zu Berlin, Berlin, Germany
email Corresponding Author

Abstract

Ralstonia eutropha is a strictly respiratory facultative lithoautotrophic β-proteobacterium. In the absence of organic substrates, H2 and CO2 are used as sole sources of energy and carbon. In the absence of oxygen, the organism can respire by denitrification. The recent determination of the complete genome sequence of strain H16 provides the opportunity to reconcile the results of previous physiological and biochemical studies in light of the coding capacity. These analyses revealed genes for several isoenzymes, permit assignment of well-known physiological functions to previously unidentified genes, and suggest the presence of unknown components of energy metabolism. The respiratory chain is fueled by two NADH dehydrogenases, two uptake hydrogenases and at least three formate dehydrogenases. The presence of genes for five quinol oxidases and three cytochrome oxidases indicates that the aerobic respiration chain adapts to varying concentrations of dioxygen. Several additional components may act in balancing or dissipation of redox energy. Paralogous sets of nitrate reductase and nitric oxide reductase genes result in enzymatic redundancy for denitrification.


 goto top of outline Key Words

  • Energy metabolism
  • Ralstonia eutropha
  • Lithoautotrophy
  • Hydrogen oxidation
  • Denitrification
  • Electron transport pathways

 goto top of outline Abstract

Ralstonia eutropha is a strictly respiratory facultative lithoautotrophic β-proteobacterium. In the absence of organic substrates, H2 and CO2 are used as sole sources of energy and carbon. In the absence of oxygen, the organism can respire by denitrification. The recent determination of the complete genome sequence of strain H16 provides the opportunity to reconcile the results of previous physiological and biochemical studies in light of the coding capacity. These analyses revealed genes for several isoenzymes, permit assignment of well-known physiological functions to previously unidentified genes, and suggest the presence of unknown components of energy metabolism. The respiratory chain is fueled by two NADH dehydrogenases, two uptake hydrogenases and at least three formate dehydrogenases. The presence of genes for five quinol oxidases and three cytochrome oxidases indicates that the aerobic respiration chain adapts to varying concentrations of dioxygen. Several additional components may act in balancing or dissipation of redox energy. Paralogous sets of nitrate reductase and nitric oxide reductase genes result in enzymatic redundancy for denitrification.

Copyright © 2008 S. Karger AG, Basel


 goto top of outline References
  1. Adams MA, Jia Z: Structural and biochemical evidence for an enzymatic quinone redox cycle in Escherichia coli: identification of a novel quinol monooxygenase. J Biol Chem 2005;280:8358–8363.
  2. Aragno M, Schlegel HG: The mesophilic hydrogen-oxidizing (knallgas) bacteria; in Balows A, Trüper HG, Dworkin M, Harder W, Schleifer K-H (eds): The Prokaryotes. New York, Springer, 1992, pp 344–384
  3. Bardischewsky F, Fischer J, Holler B, Friedrich CG: SoxV transfers electrons to the periplasm of Paracoccus pantotrophus – an essential reaction for chemotrophic sulfur oxidation. Microbiology 2006;152:465–472.
  4. Barrett EL, Riggs DL: Salmonella typhimurium mutants defective in the formate dehydrogenase linked to nitrate reductase. J Bacteriol 1982;149:554–560.
  5. Bernhard M, Schwartz E, Rietdorf J, Friedrich B: The Alcaligenes eutrophus membrane-bound hydrogenase gene locus encodes functions involved in maturation and electron transport coupling. J Bacteriol 1996;178:4522–4529.
  6. Bernhard M, Benelli B, Hochkoeppler A, Zannoni D, Friedrich B: Functional and structural role of the cytochrome b subunit of the membrane-bound hydrogenase complex of Alcaligenes eutrophus H16. Eur J Biochem 1997;248:179–186.
  7. Bjorklof K, Zickermann V, Finel M: Purification of the 45-kDa, membrane-bound NADH dehydrogenase of Escherichia coli (NDH-2) and analysis of its interaction with ubiquinone analogues. FEBS Lett 2000;467:105–110.
  8. Blokesch M, Paschos A, Theodoratou E, Bauer A, Hube M, Huth S, Bock A: Metal insertion into NiFe-hydrogenases. Biochem Soc Trans 2002;30:674–680.
  9. Bömmer D: Genetic investigation of formate oxidation in Alcaligenes eutrophus: characterization of the cbbBc gene (in German); PhD Thesis, Institute for Microbiology and Genetics, Department of Molecular Physiology, University of Göttingen, Göttingen 1995.
  10. Bömmer D, Schäferjohann J, Bowien B: Identification of cbbBc as an additional distal gene of the chromosomal cbb CO2 fixation operon from Ralstonia eutropha. Arch Microbiol 1996;166:245–251.
  11. Bongers L: Phosphorylation in hydrogen bacteria. J Bacteriol 1967;93:1615–1623.
  12. Bowien B, Kusian B: Genetics and control of CO2 assimilation in the chemoautotroph Ralstonia eutropha. Arch Microbiol 2002;178:85–93.
  13. Bowien B, Schlegel HG: Physiology and biochemistry of aerobic hydrogen-oxidizing bacteria. Annu Rev Microbiol 1981;35:405–452.
  14. Brondino CD, Passeggi MC, Caldeira J, Almendra MJ, Feio MJ, Moura JJ, Moura I: Incorporation of either molybdenum or tungsten into formate dehydrogenase from Desulfovibrio alaskensis NCIMB 13491; EPR assignment of the proximal iron-sulfur cluster to the pterin cofactor in formate dehydrogenases from sulfate-reducing bacteria. J Biol Inorg Chem 2004;9:145–151.
  15. Brzezinski P, Ädelroth P: Design principles of proton-pumping haem-copper oxidases. Curr Opin Struct Biol 2006;16:465–472.
  16. Burgdorf T: Genetic analysis of formate oxidation and molybdopterin biosynthesis in Ralstonia eutropha (in German); PhD Thesis, Department of Molecular Physiology, Georg-August-Universität, Göttingen 1998.
  17. Burgdorf T, Bömmer D, Bowien B: Involvement of an unusual mol operon in molybdopterin cofactor biosynthesis in Ralstonia eutropha. J Mol Microbiol Biotechnol 2001;3:619–629.
  18. Burgdorf T, Lenz O, Buhrke T, van der Linden E, Jones AK, Albracht SP, Friedrich B: [NiFe]-hydrogenases of Ralstonia eutropha H16: modular enzymes for oxygen-tolerant biological hydrogen oxidation. J Mol Microbiol Biotechnol 2005;10:181–196.
  19. Burgdorf T, van der Linden E, Bernhard M, Yin QY, Back JW, Hartog AF, Muijsers AO, de Koster CG, Albracht SP, Friedrich B: The soluble NAD+-reducing [NiFe]-hydrogenase from Ralstonia eutropha H16 consists of six subunits and can be specifically activated by NADPH. J Bacteriol 2005;187:3122–3132.
  20. Cole J: Nitrate reduction to ammonia by enteric bacteria: redundancy, or a strategy for survival during oxygen starvation? FEMS Microbiol Lett 1996;136:1–11.
  21. Cramm R, Pohlmann A, Friedrich B: Purification and characterization of the single-component nitric oxide reductase from Ralstonia eutropha H16. FEBS Lett 1999;460:6–10.
  22. Cramm R, Siddiqui RA, Friedrich B: Primary sequence and evidence for a physiological function of the flavohemoprotein of Alcaligenes eutrophus. J Biol Chem 1994;269:7349–7354.
  23. Cramm R, Siddiqui RA, Friedrich B: Two isofunctional nitric oxide reductases in Alcaligenes eutrophus H16. J Bacteriol 1997;179:6769–6777.
  24. Darrouzet E, Valkova-Valchanova M, Ohnishi T, Daldal F: Structure and function of the bacterial bc1 complex: domain movement, subunit interactions, and emerging rationale engineering attempts. J Bioenerg Biomembr 1999;31:275–288.
  25. De Rienzo F, Gabdoulline RR, Menziani MC, Wade RC: Blue copper proteins: a comparative analysis of their molecular interaction properties. Protein Sci 2000;9:1439–1454.
  26. Dobbek H, Gremer L, Kiefersauer R, Huber R, Meyer O: Catalysis at a dinuclear [CuSMo (=O)OH] cluster in a CO dehydrogenase resolved at 1.1-Å resolution. Proc Natl Acad Sci USA 2002;99:15971–15976.
  27. Drozd JW: Growth energetics in Alcaligenes eutrophus H16. Proc Soc Gen Microbiol 1977;4:72.
  28. Eberz G, Hogrefe C, Kortlüke C, Kamienski A, Friedrich B: Molecular cloning of structural and regulatory hydrogenase (hox) genes of Alcaligenes eutrophus H16. J Bacteriol 1986;168:636–641.
  29. Edwards KJ, Barton JD, Rossjohn J, Thorn JM, Taylor GL, Ollis DL: Structural and sequence comparisons of quinone oxidoreductase, ζ-crystallin, and glucose and alcohol dehydrogenases. Arch Biochem Biophys 1996;328:173–183.
  30. Farver O, Pecht I: Electron transfer in proteins: in search of preferential pathways. FASEB J 1991;5:2554–2559.
  31. Forte E, Urbani A, Saraste M, Sarti P, Brunori M, Giuffre A: The cytochrome cbb3 from Pseudomonas stutzeri displays nitric oxide reductase activity. Eur J Biochem 2001;268:6486–6491.
  32. Friedebold J, Bowien B: Physiological and biochemical characterization of the soluble formate dehydrogenase, a molybdoenzyme from Alcaligenes eutrophus. J Bacteriol 1993;175:4719–4728.
  33. Friedebold J, Mayer F, Bill E, Trautwein AX, Bowien B: Structural and immunological studies on the soluble formate dehydrogenase from Alcaligenes eutrophus. Biol Chem Hoppe Seyler 1995;376:561–568.
  34. Friedrich B, Schwartz E: Molecular biology of hydrogen utilization in aerobic chemolithotrophs. Annu Rev Microbiol 1993;47:351–383.
  35. Friedrich CG, Bardischewsky F, Rother D, Quentmeier A, Fischer J: Prokaryotic sulfur oxidation. Curr Opin Microbiol 2005;8:253–259.
  36. Friedrich CG, Bowien B, Friedrich B: Formate and oxalate metabolism in Alcaligenes eutrophus. J Gen Microbiol 1979;115:185–192.
  37. Friedrich CG, Rother D, Bardischewsky F, Quentmeier A, Fischer J: Oxidation of reduced inorganic sulfur compounds by bacteria: emergence of a common mechanism? Appl Environ Microbiol 2001;67:2873–2882.
  38. Friedrich T, Abelmann A, Brors B, Guenebaut V, Kintscher L, Leonard K, Rasmussen T, Scheide D, Schlitt A, Schulte U, Weiss H: Redox components and structure of the respiratory NADH:ubiquinone oxidoreductase (complex I). Biochim Biophys Acta 1998;1365:215–219.
  39. Garcia-Horsman JA, Barquera B, Rumbley J, Ma J, Gennis RB: The superfamily of heme-copper respiratory oxidases. J Bacteriol 1994; 176:5587–5600.
  40. Gardner AM, Gardner PR: Flavohemoglobin detoxifies nitric oxide in aerobic, but not anaerobic, Escherichia coli. Evidence for a novel inducible anaerobic nitric oxide-scavenging activity. J Biol Chem 2002;277:8166– 8171.
  41. Gläser H, Schlegel HG: Synthesis of enzymes of the tricarboxylic acid cycle in Hydrogenomonas eutropha strain H16 (in German). Arch Mikrobiol 1972;86:315–325.
  42. Glaser P, Danchin A, Kunst F, Zuber P, Nakano MM: Identification and isolation of a gene required for nitrate assimilation and anaerobic growth of Bacillus subtilis. J Bacteriol 1995;177:1112–1115.
  43. Gottschalk G, Eberhardt U, Schlegel HG: Utilization of fructose by Hydrogenomonas H16 (I). Arch Mikrobiol 1964;48:95–108.
  44. Hendriks J, Oubrie A, Castresana J, Urbani A, Gemeinhardt S, Saraste M: Nitric oxide reductases in bacteria. Biochim Biophys Acta 2000;1459:266–273.
  45. Hille R: The mononuclear molybdenum enzymes. Chem Rev 1996;96:2757–2816.
  46. Hille R: Molybdenum-containing hydroxylases. Arch Biochem Biophys 2005;433:107–116.
  47. Hoppensack A, Rehm BH, Steinbüchel A: Analysis of 4-phosphopantetheinylation of polyhydroxybutyrate synthase from Ralstonia eutropha: generation of β-alanine auxotrophic Tn5 mutants and cloning of the panD gene region. J Bacteriol 1999;181:1429–1435.
  48. Horsefield R, Iwata S, Byrne B: Complex II from a structural perspective. Curr Protein Pept Sci 2004;5:107–118.
  49. Iwata S, Ostermeier C, Ludwig B, Michel H: Structure at 2.8 Å resolution of cytochrome c oxidase from Paracoccus denitrificans. Nature 1995;376:660–669.
  50. Jackson JB: Proton translocation by transhydrogenase. FEBS Lett 2003;545:18–24.
  51. Jendrossek D, Kratzin HD, Steinbüchel A: The Alcaligenes eutrophus ldh structural gene encodes a novel type of lactate dehydrogenase. FEMS Microbiol Lett 1993;112:229–235.
  52. Jendrossek D, Krüger N, Steinbüchel A: Characterization of alcohol dehydrogenase genes of derepressible wild-type Alcaligenes eutrophus H16 and constitutive mutants. J Bacteriol 1990;172:4844–4851.
  53. Johnson BF, Stanier RY: Dissimilation of aromatic compounds by Alcaligenes eutrophus. J Bacteriol 1971;107:468–475.
  54. Jones CW, Brice JM, Downs AJ, Drozd JW: Bacterial respiration-linked proton translocation and its relationship to respiratory-chain composition. Eur J Biochem 1975;52:265–271.
  55. Jünemann S: Cytochrome bd terminal oxidase. Biochim Biophys Acta 1997;1321:107–127.
  56. Kersters K, De Ley J: Genus Alcaligenes Castellani and Chalmers 1919; in Krieg NR, Holt JG (eds): Bergey’s Manual of Systematic Bacteriology. Baltimore, Williams & Wilkins, 1984, vol 1, pp 361–373.
  57. Kita K, Konishi K, Anraku Y: Terminal oxidases of Escherichia coli aerobic respiratory chain. II. Purification and properties of cytochrome b558-d complex from cells grown with limited oxygen and evidence of branched electron-carrying systems. J Biol Chem 1984;259:3375–3381.
  58. Kleihues L, Lenz O, Bernhard M, Buhrke T, Friedrich B: The H2 sensor of Ralstonia eutropha is a member of the subclass of regulatory [NiFe] hydrogenases. J Bacteriol 2000;182:2716–2724.
  59. Knüttel K, Schneider K, Erkens A, Plass W, Müller A, Bill E, Trautwein AX: Redox properties of the metal centres in the membrane-bound hydrogenase from Alcaligenes eutrophus CH34. Bull Pol Acad Sci Chem 1994;42:495–511.
  60. Kömen R, Zannoni D, Ingledew WJ, Schmidt K: The electron transport system of Alcaligenes eutrophus H16. I. Spectroscopic and thermodynamic properties. Arch Microbiol 1991a; 155:382–390.

    External Resources

  61. Kömen R, Zannoni D, Schmidt K: The electron transport system of Alcaligenes eutrophus H16. II. Respiratory activities and effect of specific inhibitors. Arch Microbiol 1991b; 155:436–443.
  62. Kuhn M, Steinbüchel A, Schlegel HG: Hydrogen evolution by strictly aerobic hydrogen bacteria under anaerobic conditions. J Bacteriol 1984;159:633–639.
  63. Kusian B, Bowien B: Organization and regulation of cbb CO2 assimilation genes in autotrophic bacteria. FEMS Microbiol Rev 1997;21:135–155.
  64. Kusian B, Sultemeyer D, Bowien B: Carbonic anhydrase is essential for growth of Ralstonia eutropha at ambient CO2 concentrations. J Bacteriol 2002;184:5018–5026.
  65. Lancaster CR: Succinate:quinone oxidoreductases: an overview. Biochim Biophys Acta 2002;1553:1–6.
  66. Lemos RS, Fernandes AS, Pereira MM, Gomes CM, Teixeira M: Quinol:fumarate oxidoreductases and succinate:quinone oxidoreductases: phylogenetic relationships, metal centres and membrane attachment. Biochim Biophys Acta 2002;1553:158–170.
  67. Lenz O, Bernhard M, Buhrke T, Schwartz E, Friedrich B: The hydrogen-sensing apparatus in Ralstonia eutropha. J Mol Microbiol Biotechnol 2002;4:255–262.
  68. Lind C, Cadenas E, Hochstein P, Ernster L: DT-diaphorase: purification, properties, and function. Methods Enzymol 1990;186:287–301.
  69. Masuda N, Church GM: Escherichia coli gene expression responsive to levels of the response regulator EvgA. J Bacteriol 2002;184:6225–6234.
  70. Melo AM, Bandeiras TM, Teixeira M: New insights into type II NAD(P)H:quinone oxidoreductases. Microbiol Mol Biol Rev 2004;68:603–616.
  71. Mercer NA, McKelvey JR, Fioravanti CF: Hymenolepis diminuta: catalysis of transmembrane proton translocation by mitochondrial NADPH→NAD transhydrogenase. Exp Parasitol 1999;91:52–58.
  72. Moir JW, Wood NJ: Nitrate and nitrite transport in bacteria. Cell Mol Life Sci 2001;58:215–224.
  73. Moura JJ, Brondino CD, Trincao J, Romao MJ: Mo and W bis-MGD enzymes: nitrate reductases and formate dehydrogenases. J Biol Inorg Chem 2004;9:791–799.
  74. Nomenclature Committee of the International Union of Biochemistry (NC-IUB): Nomenclature of electron-transfer proteins. Recommendations 1989. J Biol Chem 1992;267:665–677.

    External Resources

  75. O’Brien PJ: Molecular mechanisms of quinone cytotoxicity. Chem Biol Interact 1991;80:1–41.
  76. Oglesby AG, Murphy ER, Iyer VR, Payne SM: Fur regulates acid resistance in Shigella flexneri via RyhB and ydeP. Mol Microbiol 2005;58:1354–1367.
  77. Oh JI, Bowien B: Structural analysis of the fds operon encoding the NAD+-linked formate dehydrogenase of Ralstonia eutropha. J Biol Chem 1998;273:26349–26360.
  78. Orawski G, Bardischewsky F, Quentmeier A, Rother D, Friedrich CG: The periplasmic thioredoxin SoxS plays a key role in activation in vivo of chemotrophic sulfur oxidation of Paracoccus pantotrophus. Microbiology 2007;153:1081–1086.
  79. Oubrie A, Gemeinhardt S, Field S, Marritt S, Thomson AJ, Saraste M, Richardson DJ: Properties of a soluble domain of subunit C of a bacterial nitric oxide reductase. Biochemistry 2002;41:10858–10865.
  80. Pereira MM, Santana M, Teixeira M: A novel scenario for the evolution of haem-copper oxygen reductases. Biochim Biophys Acta 2001;1505:185–208.
  81. Persson B, Zigler JS Jr, Jornvall H: A super-family of medium-chain dehydrogenases/reductases (MDR). Sub-lines including ζ-crystallin, alcohol and polyol dehydrogenases, quinone oxidoreductase enoyl reductases, VAT-1 and other proteins. Eur J Biochem 1994;226:15–22.
  82. Pfitzner J, Schlegel HG: Denitrification in Hydrogenomonas eutropha strain H 16. Arch Mikrobiol 1973;90:199–211.
  83. Philippot L: Denitrifying genes in bacterial and Archaeal genomes. Biochim Biophys Acta 2002;1577:355–376.
  84. Pitcher RS, Watmough NJ: The bacterial cytochrome cbb3 oxidases. Biochim Biophys Acta 2004;1655:388–399.
  85. Pohlmann A, Cramm R, Schmelz K, Friedrich B: A novel NO-responding regulator controls the reduction of nitric oxide in Ralstonia eutropha. Mol Microbiol 2000;38:626–638.
  86. Pohlmann A, Fricke WF, Reinecke F, Kusian B, Liesegang H, Cramm R, Eitinger T, Ewering C, Potter M, Schwartz E, Strittmatter A, Voss I, Gottschalk G, Steinbüchel A, Friedrich B, Bowien B: Genome sequence of the bioplastic-producing ‘Knallgas’ bacterium Ralstonia eutropha H16. Nat Biotechnol 2006;24:1257–1262.
  87. Poole RK, Hughes MN: New functions for the ancient globin family: bacterial responses to nitric oxide and nitrosative stress. Mol Microbiol 2000;36:775–783.
  88. Potter L, Angove H, Richardson D, Cole J: Nitrate reduction in the periplasm of Gram-negative bacteria. Adv Microb Physiol 2001;45:51–112.
  89. Preisig O, Zufferey R, Thöny-Meyer L, Appleby CA, Hennecke H: A high-affinity cbb3-type cytochrome oxidase terminates the symbiosis-specific respiratory chain of Bradyrhizobium japonicum. J Bacteriol 1996;178:1532–1538.
  90. Probst I: Respiration in Hydrogen Bacteria. Boca Raton, CRC Press, 1980, vol 2, pp 159–181.
  91. Probst I, Schlegel HG: Respiratory components and oxidase activities in Alcaligenes eutrophus. Biochim Biophys Acta 1976;440:412–428.
  92. Probst I, Wolf G, Schlegel HG: An oxygen-binding flavohemoprotein from Alcaligenes eutrophus. Biochim Biophys Acta 1979;576:471–478.
  93. Rentzsch A, Krummeck-Weiss G, Hofer A, Bartuschka A, Ostermann K, Rödel G: Mitochondrial copper metabolism in yeast: mutational analysis of Sco1p involved in the biogenesis of cytochrome c oxidase. Curr Genet 1999;35:103–108.
  94. Repaske R, Lizotte CL: The electron transport system of Hydrogenomonas eutropha. II. Reduced nicotinamide adenine dinucleotide-menadione reductase. J Biol Chem 1965;240:4774–4779.
  95. Richardson DJ, Berks BC, Russell DA, Spiro S, Taylor CJ: Functional, biochemical and genetic diversity of prokaryotic nitrate reductases. Cell Mol Life Sci 2001;58:165–178.
  96. Römermann D, Friedrich B: Denitrification by Alcaligenes eutrophus is plasmid dependent. J Bacteriol 1985;162:852–854.
  97. Sanchez AM, Andrews J, Hussein I, Bennett GN, San KY: Effect of overexpression of a soluble pyridine nucleotide transhydrogenase (UdhA) on the production of poly(3-hydroxybutyrate) in Escherichia coli. Biotechnol Prog 2006;22:420–425.
  98. Sann R, Kostka S, Friedrich B: A cytochrome cd1-type nitrite reductase mediates the first step of denitrification in Alcaligenes eutrophus. Arch Microbiol 1994;161:453–459.
  99. Saraiva LM, Vicente JB, Teixeira M: The role of the flavodiiron proteins in microbial nitric oxide detoxification. Adv Microb Physiol 2004;49:77–129.
  100. Saraste M, Castresana J: Cytochrome oxidase evolved by tinkering with denitrification enzymes. FEBS Lett 1994;341:1–4.
  101. Saraste M, Metso T, Nakari T, Jalli T, Lauraeus M, Van der Oost J: The Bacillus subtilis cytochrome-c oxidase. Variations on a conserved protein theme. Eur J Biochem 1991;195:517–525.
  102. Sawers G: The hydrogenases and formate dehydrogenases of Escherichia coli. Antonie Van Leeuwenhoek 1994;66:57–88.
  103. Schlindwein C, Giordano G, Santini CL, Mandrand MA: Identification and expression of the Escherichia coli fdhD and fdhE genes, which are involved in the formation of respiratory formate dehydrogenase. J Bacteriol 1990;172:6112–6121.
  104. Schneider K, Cammack R, Schlegel HG, Hall DO: The iron-sulphur centres of soluble hydrogenase from Alcaligenes eutrophus. Biochim Biophys Acta 1979;578:445–461.
  105. Schwartz E, Henne A, Cramm R, Eitinger T, Friedrich B, Gottschalk G: Complete nucleotide sequence of pHG1: a Ralstonia eutropha H16 megaplasmid encoding key enzymes of H2-based lithoautotrophy and anaerobiosis. J Mol Biol 2003;332:369–383.
  106. Siddiqui RA, Warnecke-Eberz U, Hengsberger A, Schneider B, Kostka S, Friedrich B: Structure and function of a periplasmic nitrate reductase in Alcaligenes eutrophus H16. J Bacteriol 1993;175:5867–5876.
  107. Siedow A, Cramm R, Siddiqui RA, Friedrich B: A megaplasmid-borne anaerobic ribonucleotide reductase in Alcaligenes eutrophus H16. J Bacteriol 1999;181:4919–4928.
  108. Simon J: Enzymology and bioenergetics of respiratory nitrite ammonification. FEMS Microbiol Rev 2002;26:285–309.
  109. Steinbüchel A, Kuhn M, Niedrig M, Schlegel HG: Fermentation enzymes in strictly aerobic bacteria: comparative studies on strains of the genus Alcaligenes and on Nocardia opaca and Xanthobacter autotrophicus. J Gen Microbiol 1983;129:2825–2835.
  110. Steinbüchel A, Schlegel HG: Physiology and molecular genetics of poly(β-hydroxy-alkanoic acid) synthesis in Alcaligenes eutrophus. Mol Microbiol 1991;5:535–542.
  111. Swem DL, Swem LR, Setterdahl A, Bauer CE: Involvement of SenC in assembly of cytochrome c oxidase in Rhodobacter capsulatus. J Bacteriol 2005;187:8081–8087.
  112. Tamagnini P, Axelsson R, Lindberg P, Oxelfelt F, Wunschiers R, Lindblad P: Hydrogenases and hydrogen metabolism of cyanobacteria. Microbiol Mol Biol Rev 2002;66:1–20.
  113. Thöny-Meyer L: Cytochrome c maturation: a complex pathway for a simple task? Biochem Soc Trans 2002;30:633–638.
  114. Van der Linden E, Burgdorf T, Bernhard M, Bleijlevens B, Friedrich B, Albracht SP: The soluble [NiFe]-hydrogenase from Ralstonia eutropha contains four cyanides in its active site, one of which is responsible for the insensitivity towards oxygen. J Biol Inorg Chem 2004;9:616–626.
  115. Van der Linden E, Faber BW, Bleijlevens B, Burgdorf T, Bernhard M, Friedrich B, Albracht SP: Selective release and function of one of the two FMN groups in the cytoplasmic NAD+-reducing [NiFe]-hydrogenase from Ralstonia eutropha. Eur J Biochem 2004;271:801–808.
  116. Van der Oost J, de Boer AP, de Gier JW, Zumft WG, Stouthamer AH, van Spanning RJ: The heme-copper oxidase family consists of three distinct types of terminal oxidases and is related to nitric oxide reductase. FEMS Microbiol Lett 1994;121:1–9.
  117. Vicente JB, Teixeira M: Redox and spectroscopic properties of the Escherichia coli nitric oxide-detoxifying system involving flavorubredoxin and its NADH-oxidizing redox partner. J Biol Chem 2005;280:34599–34608.
  118. Vignais PM, Colbeau A: Molecular biology of microbial hydrogenases. Curr Issues Mol Biol 2004;6:159–188.
  119. Volbeda A, Charon MH, Piras C, Hatchikian EC, Frey M, Fontecilla-Camps JC: Crystal structure of the nickel-iron hydrogenase from Desulfovibrio gigas. Nature 1995;373:580–587.
  120. Vollbrecht D, Schlegel HG, Stoschek G, Janczikowski A: Excretion of metabolites by hydrogen bacteria. IV. Respiration rate-dependent formation of primary metabolites and of poly-3-hydroxybutanoate. Eur J Appl Microbiol 1979;7:267–276.
  121. Wang G, Maier RJ: An NADPH quinone reductase of Helicobacter pylori plays an important role in oxidative stress resistance and host colonization. Infect Immun 2004;72:1391–1396.
  122. Warnecke-Eberz U, Friedrich B: Three nitrate reductase activities in Alcaligenes eutrophus. Arch Microbiol 1993;159:405–409.
  123. Wikström M, Verkhovsky MI: Towards the mechanism of proton pumping by the haem-copper oxidases. Biochim Biophys Acta 2006;1757:1047–1051.
  124. Yagi T, Yano T, Di Bernardo S, Matsuno-Yagi A: Procaryotic complex I (NDH-1), an overview. Biochim Biophys Acta 1998;1364:125–133.
  125. Zhu Z, Yao J, Johns T, Fu K, De Bie I, Macmillan C, Cuthbert AP, Newbold RF, Wang J, Chevrette M, Brown GK, Brown RM, Shoubridge EA: SURF1, encoding a factor involved in the biogenesis of cytochrome c oxidase, is mutated in Leigh syndrome. Nat Genet 1998;20:337–343.
  126. Zumft WG: Cell biology and molecular basis of denitrification. Microbiol Mol Biol Rev 1997;61:533–616.
  127. Zumft WG: Biogenesis of the bacterial respiratory CuA, Cu-S enzyme nitrous oxide reductase. J Mol Microbiol Biotechnol 2005;10:154–166.
  128. Zumft WG: Nitric oxide reductases of prokaryotes with emphasis on the respiratory, heme-copper oxidase type. J Inorg Biochem 2005;99:194–215.
  129. Zumft WG, Kroneck PM: Respiratory transformation of nitrous oxide (N2O) to dinitrogen by bacteria and archaea. Adv Microb Physiol 2006;52:107–227.

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 goto top of outline Author Contacts

Rainer Cramm
Institut für Biologie/Mikrobiologie, Humboldt-Universität zu Berlin
Chausseestrasse 117
DE–10115 Berlin (Germany)
Tel. +49 30 2093 8111, Fax +49 30 2093 8102, E Mail rainer.cramm@rz.hu-berlin.de


 goto top of outline Article Information

Published online: October 29, 2008
Number of Print Pages : 15
Number of Figures : 1, Number of Tables : 1, Number of References : 129


 goto top of outline Publication Details

Journal of Molecular Microbiology and Biotechnology

Vol. 16, No. 1-2, Year 2009 (Cover Date: October 2008)

Journal Editor: Saier Jr. M.H. (La Jolla, Calif.)
ISSN: 1464–1801 (Print), eISSN: 1660–2412 (Online)

For additional information: http://www.karger.com/MMB


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Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher or, in the case of photocopying, direct payment of a specified fee to the Copyright Clearance Center.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in goverment regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.

Abstract

Ralstonia eutropha is a strictly respiratory facultative lithoautotrophic β-proteobacterium. In the absence of organic substrates, H2 and CO2 are used as sole sources of energy and carbon. In the absence of oxygen, the organism can respire by denitrification. The recent determination of the complete genome sequence of strain H16 provides the opportunity to reconcile the results of previous physiological and biochemical studies in light of the coding capacity. These analyses revealed genes for several isoenzymes, permit assignment of well-known physiological functions to previously unidentified genes, and suggest the presence of unknown components of energy metabolism. The respiratory chain is fueled by two NADH dehydrogenases, two uptake hydrogenases and at least three formate dehydrogenases. The presence of genes for five quinol oxidases and three cytochrome oxidases indicates that the aerobic respiration chain adapts to varying concentrations of dioxygen. Several additional components may act in balancing or dissipation of redox energy. Paralogous sets of nitrate reductase and nitric oxide reductase genes result in enzymatic redundancy for denitrification.



 goto top of outline Author Contacts

Rainer Cramm
Institut für Biologie/Mikrobiologie, Humboldt-Universität zu Berlin
Chausseestrasse 117
DE–10115 Berlin (Germany)
Tel. +49 30 2093 8111, Fax +49 30 2093 8102, E Mail rainer.cramm@rz.hu-berlin.de


 goto top of outline Article Information

Published online: October 29, 2008
Number of Print Pages : 15
Number of Figures : 1, Number of Tables : 1, Number of References : 129


 goto top of outline Publication Details

Journal of Molecular Microbiology and Biotechnology

Vol. 16, No. 1-2, Year 2009 (Cover Date: October 2008)

Journal Editor: Saier Jr. M.H. (La Jolla, Calif.)
ISSN: 1464–1801 (Print), eISSN: 1660–2412 (Online)

For additional information: http://www.karger.com/MMB


Copyright / Drug Dosage

Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher or, in the case of photocopying, direct payment of a specified fee to the Copyright Clearance Center.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in goverment regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.

References

  1. Adams MA, Jia Z: Structural and biochemical evidence for an enzymatic quinone redox cycle in Escherichia coli: identification of a novel quinol monooxygenase. J Biol Chem 2005;280:8358–8363.
  2. Aragno M, Schlegel HG: The mesophilic hydrogen-oxidizing (knallgas) bacteria; in Balows A, Trüper HG, Dworkin M, Harder W, Schleifer K-H (eds): The Prokaryotes. New York, Springer, 1992, pp 344–384
  3. Bardischewsky F, Fischer J, Holler B, Friedrich CG: SoxV transfers electrons to the periplasm of Paracoccus pantotrophus – an essential reaction for chemotrophic sulfur oxidation. Microbiology 2006;152:465–472.
  4. Barrett EL, Riggs DL: Salmonella typhimurium mutants defective in the formate dehydrogenase linked to nitrate reductase. J Bacteriol 1982;149:554–560.
  5. Bernhard M, Schwartz E, Rietdorf J, Friedrich B: The Alcaligenes eutrophus membrane-bound hydrogenase gene locus encodes functions involved in maturation and electron transport coupling. J Bacteriol 1996;178:4522–4529.
  6. Bernhard M, Benelli B, Hochkoeppler A, Zannoni D, Friedrich B: Functional and structural role of the cytochrome b subunit of the membrane-bound hydrogenase complex of Alcaligenes eutrophus H16. Eur J Biochem 1997;248:179–186.
  7. Bjorklof K, Zickermann V, Finel M: Purification of the 45-kDa, membrane-bound NADH dehydrogenase of Escherichia coli (NDH-2) and analysis of its interaction with ubiquinone analogues. FEBS Lett 2000;467:105–110.
  8. Blokesch M, Paschos A, Theodoratou E, Bauer A, Hube M, Huth S, Bock A: Metal insertion into NiFe-hydrogenases. Biochem Soc Trans 2002;30:674–680.
  9. Bömmer D: Genetic investigation of formate oxidation in Alcaligenes eutrophus: characterization of the cbbBc gene (in German); PhD Thesis, Institute for Microbiology and Genetics, Department of Molecular Physiology, University of Göttingen, Göttingen 1995.
  10. Bömmer D, Schäferjohann J, Bowien B: Identification of cbbBc as an additional distal gene of the chromosomal cbb CO2 fixation operon from Ralstonia eutropha. Arch Microbiol 1996;166:245–251.
  11. Bongers L: Phosphorylation in hydrogen bacteria. J Bacteriol 1967;93:1615–1623.
  12. Bowien B, Kusian B: Genetics and control of CO2 assimilation in the chemoautotroph Ralstonia eutropha. Arch Microbiol 2002;178:85–93.
  13. Bowien B, Schlegel HG: Physiology and biochemistry of aerobic hydrogen-oxidizing bacteria. Annu Rev Microbiol 1981;35:405–452.
  14. Brondino CD, Passeggi MC, Caldeira J, Almendra MJ, Feio MJ, Moura JJ, Moura I: Incorporation of either molybdenum or tungsten into formate dehydrogenase from Desulfovibrio alaskensis NCIMB 13491; EPR assignment of the proximal iron-sulfur cluster to the pterin cofactor in formate dehydrogenases from sulfate-reducing bacteria. J Biol Inorg Chem 2004;9:145–151.
  15. Brzezinski P, Ädelroth P: Design principles of proton-pumping haem-copper oxidases. Curr Opin Struct Biol 2006;16:465–472.
  16. Burgdorf T: Genetic analysis of formate oxidation and molybdopterin biosynthesis in Ralstonia eutropha (in German); PhD Thesis, Department of Molecular Physiology, Georg-August-Universität, Göttingen 1998.
  17. Burgdorf T, Bömmer D, Bowien B: Involvement of an unusual mol operon in molybdopterin cofactor biosynthesis in Ralstonia eutropha. J Mol Microbiol Biotechnol 2001;3:619–629.
  18. Burgdorf T, Lenz O, Buhrke T, van der Linden E, Jones AK, Albracht SP, Friedrich B: [NiFe]-hydrogenases of Ralstonia eutropha H16: modular enzymes for oxygen-tolerant biological hydrogen oxidation. J Mol Microbiol Biotechnol 2005;10:181–196.
  19. Burgdorf T, van der Linden E, Bernhard M, Yin QY, Back JW, Hartog AF, Muijsers AO, de Koster CG, Albracht SP, Friedrich B: The soluble NAD+-reducing [NiFe]-hydrogenase from Ralstonia eutropha H16 consists of six subunits and can be specifically activated by NADPH. J Bacteriol 2005;187:3122–3132.
  20. Cole J: Nitrate reduction to ammonia by enteric bacteria: redundancy, or a strategy for survival during oxygen starvation? FEMS Microbiol Lett 1996;136:1–11.
  21. Cramm R, Pohlmann A, Friedrich B: Purification and characterization of the single-component nitric oxide reductase from Ralstonia eutropha H16. FEBS Lett 1999;460:6–10.
  22. Cramm R, Siddiqui RA, Friedrich B: Primary sequence and evidence for a physiological function of the flavohemoprotein of Alcaligenes eutrophus. J Biol Chem 1994;269:7349–7354.
  23. Cramm R, Siddiqui RA, Friedrich B: Two isofunctional nitric oxide reductases in Alcaligenes eutrophus H16. J Bacteriol 1997;179:6769–6777.
  24. Darrouzet E, Valkova-Valchanova M, Ohnishi T, Daldal F: Structure and function of the bacterial bc1 complex: domain movement, subunit interactions, and emerging rationale engineering attempts. J Bioenerg Biomembr 1999;31:275–288.
  25. De Rienzo F, Gabdoulline RR, Menziani MC, Wade RC: Blue copper proteins: a comparative analysis of their molecular interaction properties. Protein Sci 2000;9:1439–1454.
  26. Dobbek H, Gremer L, Kiefersauer R, Huber R, Meyer O: Catalysis at a dinuclear [CuSMo (=O)OH] cluster in a CO dehydrogenase resolved at 1.1-Å resolution. Proc Natl Acad Sci USA 2002;99:15971–15976.
  27. Drozd JW: Growth energetics in Alcaligenes eutrophus H16. Proc Soc Gen Microbiol 1977;4:72.
  28. Eberz G, Hogrefe C, Kortlüke C, Kamienski A, Friedrich B: Molecular cloning of structural and regulatory hydrogenase (hox) genes of Alcaligenes eutrophus H16. J Bacteriol 1986;168:636–641.
  29. Edwards KJ, Barton JD, Rossjohn J, Thorn JM, Taylor GL, Ollis DL: Structural and sequence comparisons of quinone oxidoreductase, ζ-crystallin, and glucose and alcohol dehydrogenases. Arch Biochem Biophys 1996;328:173–183.
  30. Farver O, Pecht I: Electron transfer in proteins: in search of preferential pathways. FASEB J 1991;5:2554–2559.
  31. Forte E, Urbani A, Saraste M, Sarti P, Brunori M, Giuffre A: The cytochrome cbb3 from Pseudomonas stutzeri displays nitric oxide reductase activity. Eur J Biochem 2001;268:6486–6491.
  32. Friedebold J, Bowien B: Physiological and biochemical characterization of the soluble formate dehydrogenase, a molybdoenzyme from Alcaligenes eutrophus. J Bacteriol 1993;175:4719–4728.
  33. Friedebold J, Mayer F, Bill E, Trautwein AX, Bowien B: Structural and immunological studies on the soluble formate dehydrogenase from Alcaligenes eutrophus. Biol Chem Hoppe Seyler 1995;376:561–568.
  34. Friedrich B, Schwartz E: Molecular biology of hydrogen utilization in aerobic chemolithotrophs. Annu Rev Microbiol 1993;47:351–383.
  35. Friedrich CG, Bardischewsky F, Rother D, Quentmeier A, Fischer J: Prokaryotic sulfur oxidation. Curr Opin Microbiol 2005;8:253–259.
  36. Friedrich CG, Bowien B, Friedrich B: Formate and oxalate metabolism in Alcaligenes eutrophus. J Gen Microbiol 1979;115:185–192.
  37. Friedrich CG, Rother D, Bardischewsky F, Quentmeier A, Fischer J: Oxidation of reduced inorganic sulfur compounds by bacteria: emergence of a common mechanism? Appl Environ Microbiol 2001;67:2873–2882.
  38. Friedrich T, Abelmann A, Brors B, Guenebaut V, Kintscher L, Leonard K, Rasmussen T, Scheide D, Schlitt A, Schulte U, Weiss H: Redox components and structure of the respiratory NADH:ubiquinone oxidoreductase (complex I). Biochim Biophys Acta 1998;1365:215–219.
  39. Garcia-Horsman JA, Barquera B, Rumbley J, Ma J, Gennis RB: The superfamily of heme-copper respiratory oxidases. J Bacteriol 1994; 176:5587–5600.
  40. Gardner AM, Gardner PR: Flavohemoglobin detoxifies nitric oxide in aerobic, but not anaerobic, Escherichia coli. Evidence for a novel inducible anaerobic nitric oxide-scavenging activity. J Biol Chem 2002;277:8166– 8171.
  41. Gläser H, Schlegel HG: Synthesis of enzymes of the tricarboxylic acid cycle in Hydrogenomonas eutropha strain H16 (in German). Arch Mikrobiol 1972;86:315–325.
  42. Glaser P, Danchin A, Kunst F, Zuber P, Nakano MM: Identification and isolation of a gene required for nitrate assimilation and anaerobic growth of Bacillus subtilis. J Bacteriol 1995;177:1112–1115.
  43. Gottschalk G, Eberhardt U, Schlegel HG: Utilization of fructose by Hydrogenomonas H16 (I). Arch Mikrobiol 1964;48:95–108.
  44. Hendriks J, Oubrie A, Castresana J, Urbani A, Gemeinhardt S, Saraste M: Nitric oxide reductases in bacteria. Biochim Biophys Acta 2000;1459:266–273.
  45. Hille R: The mononuclear molybdenum enzymes. Chem Rev 1996;96:2757–2816.
  46. Hille R: Molybdenum-containing hydroxylases. Arch Biochem Biophys 2005;433:107–116.
  47. Hoppensack A, Rehm BH, Steinbüchel A: Analysis of 4-phosphopantetheinylation of polyhydroxybutyrate synthase from Ralstonia eutropha: generation of β-alanine auxotrophic Tn5 mutants and cloning of the panD gene region. J Bacteriol 1999;181:1429–1435.
  48. Horsefield R, Iwata S, Byrne B: Complex II from a structural perspective. Curr Protein Pept Sci 2004;5:107–118.
  49. Iwata S, Ostermeier C, Ludwig B, Michel H: Structure at 2.8 Å resolution of cytochrome c oxidase from Paracoccus denitrificans. Nature 1995;376:660–669.
  50. Jackson JB: Proton translocation by transhydrogenase. FEBS Lett 2003;545:18–24.
  51. Jendrossek D, Kratzin HD, Steinbüchel A: The Alcaligenes eutrophus ldh structural gene encodes a novel type of lactate dehydrogenase. FEMS Microbiol Lett 1993;112:229–235.
  52. Jendrossek D, Krüger N, Steinbüchel A: Characterization of alcohol dehydrogenase genes of derepressible wild-type Alcaligenes eutrophus H16 and constitutive mutants. J Bacteriol 1990;172:4844–4851.
  53. Johnson BF, Stanier RY: Dissimilation of aromatic compounds by Alcaligenes eutrophus. J Bacteriol 1971;107:468–475.
  54. Jones CW, Brice JM, Downs AJ, Drozd JW: Bacterial respiration-linked proton translocation and its relationship to respiratory-chain composition. Eur J Biochem 1975;52:265–271.
  55. Jünemann S: Cytochrome bd terminal oxidase. Biochim Biophys Acta 1997;1321:107–127.
  56. Kersters K, De Ley J: Genus Alcaligenes Castellani and Chalmers 1919; in Krieg NR, Holt JG (eds): Bergey’s Manual of Systematic Bacteriology. Baltimore, Williams & Wilkins, 1984, vol 1, pp 361–373.
  57. Kita K, Konishi K, Anraku Y: Terminal oxidases of Escherichia coli aerobic respiratory chain. II. Purification and properties of cytochrome b558-d complex from cells grown with limited oxygen and evidence of branched electron-carrying systems. J Biol Chem 1984;259:3375–3381.
  58. Kleihues L, Lenz O, Bernhard M, Buhrke T, Friedrich B: The H2 sensor of Ralstonia eutropha is a member of the subclass of regulatory [NiFe] hydrogenases. J Bacteriol 2000;182:2716–2724.
  59. Knüttel K, Schneider K, Erkens A, Plass W, Müller A, Bill E, Trautwein AX: Redox properties of the metal centres in the membrane-bound hydrogenase from Alcaligenes eutrophus CH34. Bull Pol Acad Sci Chem 1994;42:495–511.
  60. Kömen R, Zannoni D, Ingledew WJ, Schmidt K: The electron transport system of Alcaligenes eutrophus H16. I. Spectroscopic and thermodynamic properties. Arch Microbiol 1991a; 155:382–390.

    External Resources

  61. Kömen R, Zannoni D, Schmidt K: The electron transport system of Alcaligenes eutrophus H16. II. Respiratory activities and effect of specific inhibitors. Arch Microbiol 1991b; 155:436–443.
  62. Kuhn M, Steinbüchel A, Schlegel HG: Hydrogen evolution by strictly aerobic hydrogen bacteria under anaerobic conditions. J Bacteriol 1984;159:633–639.
  63. Kusian B, Bowien B: Organization and regulation of cbb CO2 assimilation genes in autotrophic bacteria. FEMS Microbiol Rev 1997;21:135–155.
  64. Kusian B, Sultemeyer D, Bowien B: Carbonic anhydrase is essential for growth of Ralstonia eutropha at ambient CO2 concentrations. J Bacteriol 2002;184:5018–5026.
  65. Lancaster CR: Succinate:quinone oxidoreductases: an overview. Biochim Biophys Acta 2002;1553:1–6.
  66. Lemos RS, Fernandes AS, Pereira MM, Gomes CM, Teixeira M: Quinol:fumarate oxidoreductases and succinate:quinone oxidoreductases: phylogenetic relationships, metal centres and membrane attachment. Biochim Biophys Acta 2002;1553:158–170.
  67. Lenz O, Bernhard M, Buhrke T, Schwartz E, Friedrich B: The hydrogen-sensing apparatus in Ralstonia eutropha. J Mol Microbiol Biotechnol 2002;4:255–262.
  68. Lind C, Cadenas E, Hochstein P, Ernster L: DT-diaphorase: purification, properties, and function. Methods Enzymol 1990;186:287–301.
  69. Masuda N, Church GM: Escherichia coli gene expression responsive to levels of the response regulator EvgA. J Bacteriol 2002;184:6225–6234.
  70. Melo AM, Bandeiras TM, Teixeira M: New insights into type II NAD(P)H:quinone oxidoreductases. Microbiol Mol Biol Rev 2004;68:603–616.
  71. Mercer NA, McKelvey JR, Fioravanti CF: Hymenolepis diminuta: catalysis of transmembrane proton translocation by mitochondrial NADPH→NAD transhydrogenase. Exp Parasitol 1999;91:52–58.
  72. Moir JW, Wood NJ: Nitrate and nitrite transport in bacteria. Cell Mol Life Sci 2001;58:215–224.
  73. Moura JJ, Brondino CD, Trincao J, Romao MJ: Mo and W bis-MGD enzymes: nitrate reductases and formate dehydrogenases. J Biol Inorg Chem 2004;9:791–799.
  74. Nomenclature Committee of the International Union of Biochemistry (NC-IUB): Nomenclature of electron-transfer proteins. Recommendations 1989. J Biol Chem 1992;267:665–677.

    External Resources

  75. O’Brien PJ: Molecular mechanisms of quinone cytotoxicity. Chem Biol Interact 1991;80:1–41.
  76. Oglesby AG, Murphy ER, Iyer VR, Payne SM: Fur regulates acid resistance in Shigella flexneri via RyhB and ydeP. Mol Microbiol 2005;58:1354–1367.
  77. Oh JI, Bowien B: Structural analysis of the fds operon encoding the NAD+-linked formate dehydrogenase of Ralstonia eutropha. J Biol Chem 1998;273:26349–26360.
  78. Orawski G, Bardischewsky F, Quentmeier A, Rother D, Friedrich CG: The periplasmic thioredoxin SoxS plays a key role in activation in vivo of chemotrophic sulfur oxidation of Paracoccus pantotrophus. Microbiology 2007;153:1081–1086.
  79. Oubrie A, Gemeinhardt S, Field S, Marritt S, Thomson AJ, Saraste M, Richardson DJ: Properties of a soluble domain of subunit C of a bacterial nitric oxide reductase. Biochemistry 2002;41:10858–10865.
  80. Pereira MM, Santana M, Teixeira M: A novel scenario for the evolution of haem-copper oxygen reductases. Biochim Biophys Acta 2001;1505:185–208.
  81. Persson B, Zigler JS Jr, Jornvall H: A super-family of medium-chain dehydrogenases/reductases (MDR). Sub-lines including ζ-crystallin, alcohol and polyol dehydrogenases, quinone oxidoreductase enoyl reductases, VAT-1 and other proteins. Eur J Biochem 1994;226:15–22.
  82. Pfitzner J, Schlegel HG: Denitrification in Hydrogenomonas eutropha strain H 16. Arch Mikrobiol 1973;90:199–211.
  83. Philippot L: Denitrifying genes in bacterial and Archaeal genomes. Biochim Biophys Acta 2002;1577:355–376.
  84. Pitcher RS, Watmough NJ: The bacterial cytochrome cbb3 oxidases. Biochim Biophys Acta 2004;1655:388–399.
  85. Pohlmann A, Cramm R, Schmelz K, Friedrich B: A novel NO-responding regulator controls the reduction of nitric oxide in Ralstonia eutropha. Mol Microbiol 2000;38:626–638.
  86. Pohlmann A, Fricke WF, Reinecke F, Kusian B, Liesegang H, Cramm R, Eitinger T, Ewering C, Potter M, Schwartz E, Strittmatter A, Voss I, Gottschalk G, Steinbüchel A, Friedrich B, Bowien B: Genome sequence of the bioplastic-producing ‘Knallgas’ bacterium Ralstonia eutropha H16. Nat Biotechnol 2006;24:1257–1262.
  87. Poole RK, Hughes MN: New functions for the ancient globin family: bacterial responses to nitric oxide and nitrosative stress. Mol Microbiol 2000;36:775–783.
  88. Potter L, Angove H, Richardson D, Cole J: Nitrate reduction in the periplasm of Gram-negative bacteria. Adv Microb Physiol 2001;45:51–112.
  89. Preisig O, Zufferey R, Thöny-Meyer L, Appleby CA, Hennecke H: A high-affinity cbb3-type cytochrome oxidase terminates the symbiosis-specific respiratory chain of Bradyrhizobium japonicum. J Bacteriol 1996;178:1532–1538.
  90. Probst I: Respiration in Hydrogen Bacteria. Boca Raton, CRC Press, 1980, vol 2, pp 159–181.
  91. Probst I, Schlegel HG: Respiratory components and oxidase activities in Alcaligenes eutrophus. Biochim Biophys Acta 1976;440:412–428.
  92. Probst I, Wolf G, Schlegel HG: An oxygen-binding flavohemoprotein from Alcaligenes eutrophus. Biochim Biophys Acta 1979;576:471–478.
  93. Rentzsch A, Krummeck-Weiss G, Hofer A, Bartuschka A, Ostermann K, Rödel G: Mitochondrial copper metabolism in yeast: mutational analysis of Sco1p involved in the biogenesis of cytochrome c oxidase. Curr Genet 1999;35:103–108.
  94. Repaske R, Lizotte CL: The electron transport system of Hydrogenomonas eutropha. II. Reduced nicotinamide adenine dinucleotide-menadione reductase. J Biol Chem 1965;240:4774–4779.
  95. Richardson DJ, Berks BC, Russell DA, Spiro S, Taylor CJ: Functional, biochemical and genetic diversity of prokaryotic nitrate reductases. Cell Mol Life Sci 2001;58:165–178.
  96. Römermann D, Friedrich B: Denitrification by Alcaligenes eutrophus is plasmid dependent. J Bacteriol 1985;162:852–854.
  97. Sanchez AM, Andrews J, Hussein I, Bennett GN, San KY: Effect of overexpression of a soluble pyridine nucleotide transhydrogenase (UdhA) on the production of poly(3-hydroxybutyrate) in Escherichia coli. Biotechnol Prog 2006;22:420–425.
  98. Sann R, Kostka S, Friedrich B: A cytochrome cd1-type nitrite reductase mediates the first step of denitrification in Alcaligenes eutrophus. Arch Microbiol 1994;161:453–459.
  99. Saraiva LM, Vicente JB, Teixeira M: The role of the flavodiiron proteins in microbial nitric oxide detoxification. Adv Microb Physiol 2004;49:77–129.
  100. Saraste M, Castresana J: Cytochrome oxidase evolved by tinkering with denitrification enzymes. FEBS Lett 1994;341:1–4.
  101. Saraste M, Metso T, Nakari T, Jalli T, Lauraeus M, Van der Oost J: The Bacillus subtilis cytochrome-c oxidase. Variations on a conserved protein theme. Eur J Biochem 1991;195:517–525.
  102. Sawers G: The hydrogenases and formate dehydrogenases of Escherichia coli. Antonie Van Leeuwenhoek 1994;66:57–88.
  103. Schlindwein C, Giordano G, Santini CL, Mandrand MA: Identification and expression of the Escherichia coli fdhD and fdhE genes, which are involved in the formation of respiratory formate dehydrogenase. J Bacteriol 1990;172:6112–6121.
  104. Schneider K, Cammack R, Schlegel HG, Hall DO: The iron-sulphur centres of soluble hydrogenase from Alcaligenes eutrophus. Biochim Biophys Acta 1979;578:445–461.
  105. Schwartz E, Henne A, Cramm R, Eitinger T, Friedrich B, Gottschalk G: Complete nucleotide sequence of pHG1: a Ralstonia eutropha H16 megaplasmid encoding key enzymes of H2-based lithoautotrophy and anaerobiosis. J Mol Biol 2003;332:369–383.
  106. Siddiqui RA, Warnecke-Eberz U, Hengsberger A, Schneider B, Kostka S, Friedrich B: Structure and function of a periplasmic nitrate reductase in Alcaligenes eutrophus H16. J Bacteriol 1993;175:5867–5876.
  107. Siedow A, Cramm R, Siddiqui RA, Friedrich B: A megaplasmid-borne anaerobic ribonucleotide reductase in Alcaligenes eutrophus H16. J Bacteriol 1999;181:4919–4928.
  108. Simon J: Enzymology and bioenergetics of respiratory nitrite ammonification. FEMS Microbiol Rev 2002;26:285–309.
  109. Steinbüchel A, Kuhn M, Niedrig M, Schlegel HG: Fermentation enzymes in strictly aerobic bacteria: comparative studies on strains of the genus Alcaligenes and on Nocardia opaca and Xanthobacter autotrophicus. J Gen Microbiol 1983;129:2825–2835.
  110. Steinbüchel A, Schlegel HG: Physiology and molecular genetics of poly(β-hydroxy-alkanoic acid) synthesis in Alcaligenes eutrophus. Mol Microbiol 1991;5:535–542.
  111. Swem DL, Swem LR, Setterdahl A, Bauer CE: Involvement of SenC in assembly of cytochrome c oxidase in Rhodobacter capsulatus. J Bacteriol 2005;187:8081–8087.
  112. Tamagnini P, Axelsson R, Lindberg P, Oxelfelt F, Wunschiers R, Lindblad P: Hydrogenases and hydrogen metabolism of cyanobacteria. Microbiol Mol Biol Rev 2002;66:1–20.
  113. Thöny-Meyer L: Cytochrome c maturation: a complex pathway for a simple task? Biochem Soc Trans 2002;30:633–638.
  114. Van der Linden E, Burgdorf T, Bernhard M, Bleijlevens B, Friedrich B, Albracht SP: The soluble [NiFe]-hydrogenase from Ralstonia eutropha contains four cyanides in its active site, one of which is responsible for the insensitivity towards oxygen. J Biol Inorg Chem 2004;9:616–626.
  115. Van der Linden E, Faber BW, Bleijlevens B, Burgdorf T, Bernhard M, Friedrich B, Albracht SP: Selective release and function of one of the two FMN groups in the cytoplasmic NAD+-reducing [NiFe]-hydrogenase from Ralstonia eutropha. Eur J Biochem 2004;271:801–808.
  116. Van der Oost J, de Boer AP, de Gier JW, Zumft WG, Stouthamer AH, van Spanning RJ: The heme-copper oxidase family consists of three distinct types of terminal oxidases and is related to nitric oxide reductase. FEMS Microbiol Lett 1994;121:1–9.
  117. Vicente JB, Teixeira M: Redox and spectroscopic properties of the Escherichia coli nitric oxide-detoxifying system involving flavorubredoxin and its NADH-oxidizing redox partner. J Biol Chem 2005;280:34599–34608.
  118. Vignais PM, Colbeau A: Molecular biology of microbial hydrogenases. Curr Issues Mol Biol 2004;6:159–188.
  119. Volbeda A, Charon MH, Piras C, Hatchikian EC, Frey M, Fontecilla-Camps JC: Crystal structure of the nickel-iron hydrogenase from Desulfovibrio gigas. Nature 1995;373:580–587.
  120. Vollbrecht D, Schlegel HG, Stoschek G, Janczikowski A: Excretion of metabolites by hydrogen bacteria. IV. Respiration rate-dependent formation of primary metabolites and of poly-3-hydroxybutanoate. Eur J Appl Microbiol 1979;7:267–276.
  121. Wang G, Maier RJ: An NADPH quinone reductase of Helicobacter pylori plays an important role in oxidative stress resistance and host colonization. Infect Immun 2004;72:1391–1396.
  122. Warnecke-Eberz U, Friedrich B: Three nitrate reductase activities in Alcaligenes eutrophus. Arch Microbiol 1993;159:405–409.
  123. Wikström M, Verkhovsky MI: Towards the mechanism of proton pumping by the haem-copper oxidases. Biochim Biophys Acta 2006;1757:1047–1051.
  124. Yagi T, Yano T, Di Bernardo S, Matsuno-Yagi A: Procaryotic complex I (NDH-1), an overview. Biochim Biophys Acta 1998;1364:125–133.
  125. Zhu Z, Yao J, Johns T, Fu K, De Bie I, Macmillan C, Cuthbert AP, Newbold RF, Wang J, Chevrette M, Brown GK, Brown RM, Shoubridge EA: SURF1, encoding a factor involved in the biogenesis of cytochrome c oxidase, is mutated in Leigh syndrome. Nat Genet 1998;20:337–343.
  126. Zumft WG: Cell biology and molecular basis of denitrification. Microbiol Mol Biol Rev 1997;61:533–616.
  127. Zumft WG: Biogenesis of the bacterial respiratory CuA, Cu-S enzyme nitrous oxide reductase. J Mol Microbiol Biotechnol 2005;10:154–166.
  128. Zumft WG: Nitric oxide reductases of prokaryotes with emphasis on the respiratory, heme-copper oxidase type. J Inorg Biochem 2005;99:194–215.
  129. Zumft WG, Kroneck PM: Respiratory transformation of nitrous oxide (N2O) to dinitrogen by bacteria and archaea. Adv Microb Physiol 2006;52:107–227.

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