1887

Abstract

The prokaryotic cytoplasmic membrane not only maintains cell integrity and forms a barrier between the cell and its outside environment, but is also the location for essential biochemical processes. Microbial model systems provide excellent bases for the study of fundamental problems in membrane biology including signal transduction, chemotaxis, solute transport and, as will be the topic of this review, energy metabolism. Bacterial respiration requires a diverse array of complex, multi-subunit, cofactor-containing redox enzymes, many of which are embedded within, or located on the extracellular side of, the membrane. The biosynthesis of these enzymes therefore requires carefully controlled expression, assembly, targeting and transport processes. Here, focusing on the molybdenum-containing respiratory enzymes central to anaerobic respiration in , recent descriptions of a chaperone-mediated ‘proofreading’ system involved in coordinating assembly and export of complex extracellular enzymes will be discussed. The paradigm proofreading chaperones are members of a large group of proteins known as the TorD family, and recent research in this area highlights common principles that underpin biosynthesis of both exported and non-exported respiratory enzymes.

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2007-03-01
2019-10-14
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References

  1. Afshar, S., Johnson, E., de Vries, S. & Schröder, I. ( 2001; ). Properties of a thermostable nitrate reductase from the hyperthermophilic archaeon Pyrobaculum aerophilum. J Bacteriol 183, 5491–5495.[CrossRef]
    [Google Scholar]
  2. Alami, M., Lüke, I., Deitermann, S., Eisner, G., Koch, H. G., Brunner, J. & Müller, M. ( 2003; ). Differential interactions between a twin-arginine signal peptide and its translocase in Escherichia coli. Mol Cell 12, 937–946.[CrossRef]
    [Google Scholar]
  3. Alder, N. N. & Theg, S. M. ( 2003; ). Energetics of protein transport across biological membranes. a study of the thylakoid ΔpH-dependent/cpTat pathway. Cell 112, 231–242.[CrossRef]
    [Google Scholar]
  4. Anthony, C. ( 2004; ). The quinoprotein dehydrogenases for methanol and glucose. Arch Biochem Biophys 428, 2–9.[CrossRef]
    [Google Scholar]
  5. Aravind, L. & Koonin, E. V. ( 1998a; ). A novel family of predicted phosphoesterases includes Drosophila prune protein and bacterial RecJ exonuclease. Trends Biochem Sci 23, 17–19.[CrossRef]
    [Google Scholar]
  6. Aravind, L. & Koonin, E. V. ( 1998b; ). Phosphoesterase domains associated with DNA polymerases of diverse origins. Nucleic Acids Res 26, 3746–3752.[CrossRef]
    [Google Scholar]
  7. Aravind, L. & Koonin, E. V. ( 1998c; ). The HD domain defines a new superfamily of metal-dependent phosphohydrolases. Trends Biochem Sci 23, 469–472.[CrossRef]
    [Google Scholar]
  8. Bachmann, J., Bauer, B., Zwicker, K., Ludwig, B. & Anderka, O. ( 2006; ). The Rieske protein from Paracoccus denitrificans is inserted into the cytoplasmic membrane by the twin-arginine translocase. FEBS J 273, 4817–4830.[CrossRef]
    [Google Scholar]
  9. Balk, J. & Lobreaux, S. ( 2005; ). Biogenesis of iron-sulfur proteins in plants. Trends Plant Sci 10, 324–331.[CrossRef]
    [Google Scholar]
  10. Behrendt, J., Standar, K., Lindenstrauss, U. & Brüser, T. ( 2004; ). Topological studies on the twin-arginine translocase component TatC. FEMS Microbiol Lett 234, 303–308.[CrossRef]
    [Google Scholar]
  11. Bendtsen, J. D., Nielsen, H., Widdick, D. A., Palmer, T. & Brünak, S. ( 2005; ). Prediction of twin-arginine signal peptides. BMC Bioinformatics 6, 167.[CrossRef]
    [Google Scholar]
  12. Berks, B. C. ( 1996; ). A common export pathway for proteins binding complex redox cofactors? Mol Microbiol 22, 393–404.[CrossRef]
    [Google Scholar]
  13. Berks, B. C., Ferguson, S. J., Moir, J. W. & Richardson, D. J. ( 1995; ). Enzymes and associated electron transport systems that catalyse the respiratory reduction of nitrogen oxides and oxyanions. Biochim Biophys Acta 1232, 97–173.[CrossRef]
    [Google Scholar]
  14. Berks, B. C., Palmer, T. & Sargent, F. ( 2003; ). The Tat protein translocation pathway and its role in microbial physiology. Adv Microb Physiol 47, 187–254.
    [Google Scholar]
  15. Berks, B. C., Palmer, T. & Sargent, F. ( 2005; ). Protein targeting by the bacterial twin-arginine translocation (Tat) pathway. Curr Opin Microbiol 8, 174–181.[CrossRef]
    [Google Scholar]
  16. Bernhard, M., Schwartz, E., Rietdorf, J. & Friedrich, B. ( 1996; ). The Alcaligenes eutrophus membrane-bound hydrogenase gene locus encodes functions involved in maturation and electron transport coupling. J Bacteriol 178, 4522–4529.
    [Google Scholar]
  17. Bertero, M. G., Rothery, R. A., Palak, M., Hou, C., Lim, D., Blasco, F., Weiner, J. H. & Strynadka, N. C. ( 2003; ). Insights into the respiratory electron transfer pathway from the structure of nitrate reductase A. Nat Struct Biol 10, 681–687.[CrossRef]
    [Google Scholar]
  18. Bilous, P. T., Cole, S. T., Anderson, W. F. & Weiner, J. H. ( 1988; ). Nucleotide sequence of the dmsABC operon encoding the anaerobic dimethyl sulphoxide reductase of Escherichia coli. Mol Microbiol 2, 785–795.[CrossRef]
    [Google Scholar]
  19. Blasco, F., Dos Santos, J.-P., Magalon, A., Frixon, C., Guigliarelli, B., Santini, C.-L. & Giordano, G. ( 1998; ). NarJ is a specific chaperone required for molybdenum cofactor assembly in nitrate reductase A of Escherichia coli. Mol Microbiol 28, 435–447.[CrossRef]
    [Google Scholar]
  20. Böck, A., King, P. W., Blokesch, M. & Posewitz, M. C. ( 2006; ). Maturation of hydrogenases. Adv Microb Physiol 51, 1–71.
    [Google Scholar]
  21. Bogsch, E. G., Sargent, F., Stanley, N. R., Berks, B. C., Robinson, C. & Palmer, T. ( 1998; ). An essential component of a novel bacterial protein export system with homologues in plastids and mitochondria. J Biol Chem 273, 18003–18006.[CrossRef]
    [Google Scholar]
  22. Bolhuis, A. ( 2002; ). Protein transport in the halophilic archaeon Halobacterium sp. NRC-1: a major role for the twin-arginine translocation pathway? Microbiology 148, 3335–3346.
    [Google Scholar]
  23. Bolhuis, A., Mathers, J. E., Thomas, J. D., Barrett, C. M. & Robinson, C. ( 2001; ). TatB and TatC form a functional and structural unit of the twin-arginine translocase from Escherichia coli. J Biol Chem 276, 20213–20219.[CrossRef]
    [Google Scholar]
  24. Brokx, S. J., Rothery, R. A., Zhang, G., Ng, D. P. & Weiner, J. H. ( 2005; ). Characterization of an Escherichia coli sulfite oxidase homologue reveals the role of a conserved active site cysteine in assembly and function. Biochemistry 44, 10339–10348.[CrossRef]
    [Google Scholar]
  25. Buchanan, G., Küper, J., Mendel, R. R., Schwarz, G. & Palmer, T. ( 2001; ). Characterisation of the mob locus of Rhodobacter sphaeroides WS8: mobA is the only gene required for molybdopterin guanine dinucleotide synthesis. Arch Microbiol 176, 62–68.[CrossRef]
    [Google Scholar]
  26. Butland, G., Zhang, J. W., Yang, W., Sheung, A., Wong, P., Greenblatt, J. F., Emili, A. & Zamble, D. B. ( 2006; ). Interactions of the Escherichia coli hydrogenase biosynthetic proteins: HybG complex formation. FEBS Lett 580, 677–681.[CrossRef]
    [Google Scholar]
  27. Chaddock, A. M., Mant, A., Karnauchov, I., Brink, S., Herrmann, R. G., Klösgen, R.-B. & Robinson, C. ( 1995; ). A new type of signal peptide: central role of a twin-arginine motif in transfer signals for the delta pH-dependent thylakoidal protein translocase. EMBO J 14, 2715–2722.
    [Google Scholar]
  28. Chan, C. S., Howell, J. M., Workentine, M. L. & Turner, R. J. ( 2006; ). Twin-arginine translocase may have a role in the chaperone function of NarJ from Escherichia coli. Biochem Biophys Res Commun 343, 244–251.[CrossRef]
    [Google Scholar]
  29. Chanal, A., Santini, C.-L. & Wu, L.-F. ( 1998; ). Potential receptor function of three homologous components, TatA, TatB and TatE, of the twin-arginine signal sequence-dependent metalloenzyme translocation pathway in Escherichia coli. Mol Microbiol 30, 674–676.[CrossRef]
    [Google Scholar]
  30. Chou, Y. T. & Gierasch, L. M. ( 2005; ). The conformation of a signal peptide bound by Escherichia coli preprotein translocase SecA. J Biol Chem 280, 32753–32760.[CrossRef]
    [Google Scholar]
  31. Creighton, A. M., Hulford, A., Mant, A., Robinson, D. & Robinson, C. ( 1995; ). A monomeric, tightly folded stromal intermediate on the delta pH-dependent thylakoidal protein transport pathway. J Biol Chem 270, 1663–1669.[CrossRef]
    [Google Scholar]
  32. Czjzek, M., Dos Santos, J.-P., Pommier, J., Giordano, G., Mejean, V. & Haser, R. ( 1998; ). Crystal structure of oxidized trimethylamine N-oxide reductase from Shewanella massilia at 2.5 Å resolution. J Mol Biol 284, 435–447.[CrossRef]
    [Google Scholar]
  33. Dabney-Smith, C., Mori, H. & Cline, K. ( 2006; ). Oligomers of Tha4 organize at the thylakoid Tat translocase during protein transport. J Biol Chem 281, 5476–5483.
    [Google Scholar]
  34. Dekker, N., Cox, R. C., Kramer, R. A. & Egmond, M. R. ( 2001; ). Substrate specificity of the integral membrane protease OmpT determined by spatially addressed peptide libraries. Biochemistry 40, 1694–1701.[CrossRef]
    [Google Scholar]
  35. de Leeuw, E., Granjon, T., Porcelli, I., Alami, M., Carr, S. B., Müller, M., Sargent, F., Palmer, T. & Berks, B. C. ( 2002; ). Oligomeric properties and signal peptide binding by Escherichia coli Tat protein transport complexes. J Mol Biol 322, 1135–1146.[CrossRef]
    [Google Scholar]
  36. Delisa, M. P., Tullman, D. & Georgiou, G. ( 2003; ). Folding quality control in the export of proteins by the bacterial twin-arginine translocation pathway. Proc Natl Acad Sci U S A 100, 6115–6120.[CrossRef]
    [Google Scholar]
  37. Dilks, K., Rose, R. W., Hartmann, E. & Pohlschröder, M. ( 2003; ). Prokaryotic utilization of the twin-arginine translocation pathway: a genomic survey. J Bacteriol 185, 1478–1483.[CrossRef]
    [Google Scholar]
  38. Dobbek, H., Gremer, L., Meyer, O. & Huber, R. ( 1999; ). Crystal structure and mechanism of CO dehydrogenase, a molybdo iron-sulfur flavoprotein containing S-selanylcysteine. Proc Natl Acad Sci U S A 96, 8884–8889.[CrossRef]
    [Google Scholar]
  39. Doudna, J. A. & Batey, R. T. ( 2004; ). Structural insights into the signal recognition particle. Annu Rev Biochem 73, 539–557.[CrossRef]
    [Google Scholar]
  40. Dreusch, A., Bürgisser, D. M., Heizmann, C. W. & Zumft, W. G. ( 1997; ). Lack of copper insertion into unprocessed cytoplasmic nitrous oxide reductase generated by an R20D substitution in the arginine consensus motif of the signal peptide. Biochim Biophys Acta 1319, 311–318.[CrossRef]
    [Google Scholar]
  41. Drew, D., Sjostrand, D., Nilsson, J., Urbig, T., Chin, C. N., de Gier, J. W. & von Heijne, G. ( 2002; ). Rapid topology mapping of Escherichia coli inner-membrane proteins by prediction and PhoA/GFP fusion analysis. Proc Natl Acad Sci U S A 99, 2690–2695.[CrossRef]
    [Google Scholar]
  42. Dridge, E. J., Richardson, D. J., Lewis, R. J. & Butler, C. S. ( 2006; ). Developing structure-based models to predict substrate specificity of D-group (type II) molybdenum enzymes: application to a molybdoenzyme of unknown function from Archaeoglobus fulgidus. Biochem Soc Trans 34, 118–121.[CrossRef]
    [Google Scholar]
  43. Dubini, A. & Sargent, F. ( 2003; ). Assembly of Tat-dependent [NiFe] hydrogenases: identification of precursor-binding accessory proteins. FEBS Lett 549, 141–146.[CrossRef]
    [Google Scholar]
  44. Ellis, R. J. & Hartl, F. U. ( 1999; ). Principles of protein folding in the cellular environment. Curr Opin Struct Biol 9, 102–110.[CrossRef]
    [Google Scholar]
  45. Enoch, H. G. & Lester, R. L. ( 1975; ). The purification and properties of formate dehydrogenase and nitrate reductase from Escherichia coli. J Biol Chem 250, 6693–6705.
    [Google Scholar]
  46. Ezraty, B., Bos, J., Barras, F. & Aussel, L. ( 2005; ). Methionine sulfoxide reduction and assimilation in Escherichia coli: new role for the biotin sulfoxide reductase BisC. J Bacteriol 187, 231–237.[CrossRef]
    [Google Scholar]
  47. Field, S. J., Thornton, N. P., Anderson, L. J., Gates, A. J., Reilly, A., Jepson, B. J., Richardson, D. J., George, S. J., Cheesman, M. R. & Butt, J. N. ( 2005; ). Reductive activation of nitrate reductases. Dalton Trans 3580–3586.
    [Google Scholar]
  48. Finazzi, G., Chasen, C., Wollman, F. A. & de Vitry, C. ( 2003; ). Thylakoid targeting of Tat passenger proteins shows no ΔpH dependence in vivo. EMBO J 22, 807–815.[CrossRef]
    [Google Scholar]
  49. Fischer, K., Barbier, G. G., Hecht, H. J., Mendel, R. R., Campbell, W. H. & Schwarz, G. ( 2005; ). Structural basis of eukaryotic nitrate reduction: crystal structures of the nitrate reductase active site. Plant Cell 17, 1167–1179.[CrossRef]
    [Google Scholar]
  50. Focia, P. J., Shepotinovskaya, I. V., Seidler, J. A. & Freymann, D. M. ( 2004; ). Heterodimeric GTPase core of the SRP targeting complex. Science 303, 373–377.[CrossRef]
    [Google Scholar]
  51. Friedrich, B., Hogrefe, C. & Schlegel, H. G. ( 1981; ). Naturally occurring genetic transfer of hydrogen-oxidizing ability between strains of Alcaligenes eutrophus. J Bacteriol 147, 198–205.
    [Google Scholar]
  52. Galperin, M. Y., Nikolskaya, A. N. & Koonin, E. V. ( 2001; ). Novel domains of the prokaryotic two-component signal transduction systems. FEMS Microbiol Lett 203, 11–21.[CrossRef]
    [Google Scholar]
  53. Genest, O., Ilbert, M., Mejean, V. & Iobbi-Nivol, C. ( 2005; ). TorD, an essential chaperone for TorA molybdoenzyme maturation at high temperature. J Biol Chem 280, 15644–15648.[CrossRef]
    [Google Scholar]
  54. Genest, O., Seduk, F., Ilbert, M., Mejean, V. & Iobbi-Nivol, C. ( 2006a; ). Signal peptide protection by specific chaperone. Biochem Biophys Res Commun 339, 991–995.[CrossRef]
    [Google Scholar]
  55. Genest, O., Seduk, F., Theraulaz, L., Mejean, V. & Iobbi-Nivol, C. ( 2006b; ). Chaperone protection of immature molybdoenzyme during molybdenum cofactor limitation. FEMS Microbiol Lett 265, 51–55.[CrossRef]
    [Google Scholar]
  56. Gohlke, U., Pullan, L., McDevitt, C. A., Porcelli, I., de Leeuw, E., Palmer, T., Saibil, H. R. & Berks, B. C. ( 2005; ). The TatA component of the twin-arginine protein transport system forms channel complexes of variable diameter. Proc Natl Acad Sci U S A 102, 10482–10486.[CrossRef]
    [Google Scholar]
  57. Gralnick, J. A., Vali, H., Lies, D. P. & Newman, D. K. ( 2006; ). Extracellular respiration of dimethyl sulfoxide by Shewanella oneidensis strain MR-1. Proc Natl Acad Sci U S A 103, 4669–4674.[CrossRef]
    [Google Scholar]
  58. Harris, A. G. & Hazell, S. L. ( 2003; ). Localisation of Helicobacter pylori catalase in both the periplasm and cytoplasm, and its dependence on the twin-arginine target protein, KapA, for activity. FEMS Microbiol Lett 229, 283–289.[CrossRef]
    [Google Scholar]
  59. Hatzixanthis, K., Palmer, T. & Sargent, F. ( 2003; ). A subset of bacterial inner membrane proteins integrated by the twin-arginine translocase. Mol Microbiol 49, 1377–1390.[CrossRef]
    [Google Scholar]
  60. Hatzixanthis, K., Clarke, T. A., Oubrie, A., Richardson, D. J., Turner, R. J. & Sargent, F. ( 2005; ). Signal peptide-chaperone interactions on the twin-arginine protein transport pathway. Proc Natl Acad Sci U S A 102, 8460–8465.[CrossRef]
    [Google Scholar]
  61. Hensel, M., Hinsley, A. P., Nikolaus, T., Sawers, G. & Berks, B. C. ( 1999; ). The genetic basis of tetrathionate respiration in Salmonella typhimurium. Mol Microbiol 32, 275–287.[CrossRef]
    [Google Scholar]
  62. Hinsley, A. P. & Berks, B. C. ( 2002; ). Specificity of respiratory pathways involved in the reduction of sulfur compounds by Salmonella enterica. Microbiology 148, 3631–3638.
    [Google Scholar]
  63. Hynds, P. J., Robinson, D. & Robinson, C. ( 1998; ). The Sec-independent twin-arginine translocation system can transport both tightly folded and malfolded proteins across the thylakoid membrane. J Biol Chem 273, 34868–34874.[CrossRef]
    [Google Scholar]
  64. Ilbert, M., Mejean, V., Giudici-Orticoni, M. T., Samama, J.-P. & Iobbi-Nivol, C. ( 2003; ). Involvement of a mate chaperone (TorD) in the maturation pathway of molybdoenzyme TorA. J Biol Chem 278, 28787–28792.[CrossRef]
    [Google Scholar]
  65. Ilbert, M., Mejean, V. & Iobbi-Nivol, C. ( 2004; ). Functional and structural analysis of members of the TorD family, a large chaperone family dedicated to molybdoproteins. Microbiology 150, 935–943.[CrossRef]
    [Google Scholar]
  66. Jack, R. L., Buchanan, G., Dubini, A., Hatzixanthis, K., Palmer, T. & Sargent, F. ( 2004; ). Coordinating assembly and export of complex bacterial proteins. EMBO J 23, 3962–3972.[CrossRef]
    [Google Scholar]
  67. Jack, R. L., Dubini, A., Palmer, T. & Sargent, F. ( 2005; ). Common principles in the biosynthesis of diverse enzymes. Biochem Soc Trans 33, 105–107.[CrossRef]
    [Google Scholar]
  68. Janssen, D. B., Oppentocht, J. E. & Pölarends, G. J. ( 2001; ). Microbial dehalogenation. Curr Opin Biotechnol 12, 254–258.[CrossRef]
    [Google Scholar]
  69. Johnson, J. L., Indermaur, L. W. & Rajagopalan, K. V. ( 1991; ). Molybdenum cofactor biosynthesis in Escherichia coli. Requirement of the chlB gene product for the formation of molybdopterin guanine dinucleotide. J Biol Chem 266, 12140–12145.
    [Google Scholar]
  70. Johnson, D. C., Dean, D. R., Smith, A. D. & Johnson, M. K. ( 2005; ). Structure, function, and formation of biological iron-sulfur clusters. Annu Rev Biochem 74, 247–281.[CrossRef]
    [Google Scholar]
  71. Jongbloed, J. D., van der Ploeg, R. & van Dijl, J.-M. ( 2006; ). Bifunctional TatA subunits in minimal Tat protein translocases. Trends Microbiol 14, 2–4.[CrossRef]
    [Google Scholar]
  72. Jormakka, M., Tornröth, S., Byrne, B. & Iwata, S. ( 2002; ). Molecular basis of proton motive force generation: structure of formate dehydrogenase-N. Science 295, 1863–1868.[CrossRef]
    [Google Scholar]
  73. Jormakka, M., Byrne, B. & Iwata, S. ( 2003; ). Protonmotive force generation by a redox loop mechanism. FEBS Lett 545, 25–30.[CrossRef]
    [Google Scholar]
  74. Jormakka, M., Richardson, D. J., Byrne, B. & Iwata, S. ( 2004; ). Architecture of NarGH reveals a structural classification of Mo-bisMGD enzymes. Structure 12, 95–104.[CrossRef]
    [Google Scholar]
  75. Khangulov, S. V., Gladyshev, V. N., Dismukes, G. C. & Stadtman, T. C. ( 1998; ). Selenium-containing formate dehydrogenase-H from Escherichia coli: a molybdopterin enzyme that catalyzes formate oxidation without oxygen transfer. Biochemistry 37, 3518–3528.[CrossRef]
    [Google Scholar]
  76. Ki, J. J., Kawarasaki, Y., Gam, J., Harvey, B. R., Iverson, B. L. & Georgiou, G. ( 2004; ). A periplasmic fluorescent reporter protein and its application in high-throughput membrane protein topology analysis. J Mol Biol 341, 901–909.[CrossRef]
    [Google Scholar]
  77. Kipping, M., Lilie, H., Lindenstrauss, U., Andreesen, J. R., Griesinger, C., Carlomagno, T. & Brüser, T. ( 2003; ). Structural studies on a twin-arginine signal sequence. FEBS Lett 550, 18–22.[CrossRef]
    [Google Scholar]
  78. Kisker, C., Schindelin, H. & Rees, D. C. ( 1997; ). Molybdenum-cofactor-containing enzymes: structure and mechanism. Annu Rev Biochem 66, 233–267.[CrossRef]
    [Google Scholar]
  79. Koonin, E. V. ( 1996; ). A duplicated catalytic motif in a new superfamily of phosphohydrolases and phospholipid synthases that includes poxvirus envelope proteins. Trends Biochem Sci 21, 242–243.[CrossRef]
    [Google Scholar]
  80. Lee, P. A., Orriss, G. L., Buchanan, G., Greene, N. P., Bond, P. J., Punginelli, C., Jack, R. L., Sansom, M. S., Berks, B. C. & Palmer, T. ( 2006; ). Cysteine-scanning mutagenesis and disulfide mapping studies of the conserved domain of the twin-arginine translocase TatB component. J Biol Chem 281, 34072–34085.[CrossRef]
    [Google Scholar]
  81. Leimkuhler, S. & Klipp, W. ( 1999; ). Role of XdhC in molybdenum cofactor insertion into xanthine dehydrogenase of Rhodobacter capsulatus. J Bacteriol 181, 2745–2751.
    [Google Scholar]
  82. Leimkuhler, S., Kern, M., Solomon, P. S., McEwan, A. G., Schwarz, G., Mendel, R. R. & Klipp, W. ( 1998; ). Xanthine dehydrogenase from the phototrophic purple bacterium Rhodobacter capsulatus is more similar to its eukaryotic counterparts than to prokaryotic molybdenum enzymes. Mol Microbiol 27, 853–869.[CrossRef]
    [Google Scholar]
  83. Li, S. Y., Chang, B. Y. & Lin, S. C. ( 2006; ). Coexpression of TorD enhances the transport of GFP via the Tat pathway. J Biotechnol 122, 412–421.[CrossRef]
    [Google Scholar]
  84. Lill, R. & Mühlenhoff, U. ( 2005; ). Iron-sulfur-protein biogenesis in eukaryotes. Trends Biochem Sci 30, 133–141.[CrossRef]
    [Google Scholar]
  85. Lledo, B., Martinez-Espinosa, R. M., Marhuenda-Egea, F. C. & Bonete, M. J. ( 2004; ). Respiratory nitrate reductase from haloarchaeon Haloferax mediterranei: biochemical and genetic analysis. Biochim Biophys Acta 1674, 50–59.[CrossRef]
    [Google Scholar]
  86. Loschi, L., Brokx, S. J., Hills, T. L., Zhang, G., Bertero, M. G., Lovering, A. L., Weiner, J. H. & Strynadka, N. C. ( 2004; ). Structural and biochemical identification of a novel bacterial oxidoreductase. J Biol Chem 279, 50391–50400.[CrossRef]
    [Google Scholar]
  87. Lubitz, S. P. & Weiner, J. H. ( 2003; ). The Escherichia coli ynfEFGHI operon encodes polypeptides which are paralogues of dimethyl sulfoxide reductase (DmsABC). Arch Biochem Biophys 418, 205–216.[CrossRef]
    [Google Scholar]
  88. Maeda, S. & Omata, T. ( 2004; ). A novel gene (narM) required for expression of nitrate reductase activity in the cyanobacterium Synechococcus elongatus strain PCC7942. J Bacteriol 186, 2107–2114.[CrossRef]
    [Google Scholar]
  89. Mandrand-Berthelot, M.-A., Couchoux-Luthaud, G., Santini, C.-L. & Giordano, G. ( 1988; ). Mutants of Escherichia coli specifically deficient in respiratory formate dehydrogenase activity. J Gen Microbiol 134, 3129–3139.
    [Google Scholar]
  90. Mayer, M. P., Laufen, T., Paal, K., McCarty, J. S. & Bukau, B. ( 1999; ). Investigation of the interaction between DnaK and DnaJ by surface plasmon resonance spectroscopy. J Mol Biol 289, 1131–1144.[CrossRef]
    [Google Scholar]
  91. McAlpine, A. S., McEwan, A. G. & Bailey, S. ( 1998; ). The high resolution crystal structure of DMSO reductase in complex with DMSO. J Mol Biol 275, 613–623.[CrossRef]
    [Google Scholar]
  92. McCrindle, S. L., Kappler, U. & McEwan, A. G. ( 2005; ). Microbial dimethylsulfoxide and trimethylamine-N-oxide respiration. Adv Microb Physiol 50, 147–198.
    [Google Scholar]
  93. McDevitt, C. A., Hugenholtz, P., Hanson, G. R. & McEwan, A. G. ( 2002; ). Molecular analysis of dimethyl sulphide dehydrogenase from Rhodovulum sulfidophilum: its place in the dimethyl sulphoxide reductase family of microbial molybdopterin-containing enzymes. Mol Microbiol 44, 1575–1587.[CrossRef]
    [Google Scholar]
  94. McDevitt, C. A., Hicks, M. G., Palmer, T. & Berks, B. C. ( 2005; ). Characterisation of Tat protein transport complexes carrying inactivating mutations. Biochem Biophys Res Commun 329, 693–698.[CrossRef]
    [Google Scholar]
  95. Mejean, V., Iobbi-Nivol, C., Lepelletie, M., Giordano, G., Chippaux, M. & Pascal, M. C. ( 1994; ). TMAO anaerobic respiration in Escherichia coli: involvement of the tor operon. Mol Microbiol 11, 1169–1179.[CrossRef]
    [Google Scholar]
  96. Mitchell, P. ( 1961; ). Coupling of phosphorylation to electron and hydrogen transfer by a chemiosmotic type of mechanism. Nature 191, 144–148.[CrossRef]
    [Google Scholar]
  97. Mitchell, P. & Moyle, J. ( 1967; ). Chemiosmotic hypothesis of oxidative phophorylation. Nature 213, 137–139.[CrossRef]
    [Google Scholar]
  98. Mori, H. & Cline, K. ( 2002; ). A twin arginine signal peptide and the pH gradient trigger reversible assembly of the thylakoid ΔpH/Tat translocase. J Cell Biol 157, 205–210.[CrossRef]
    [Google Scholar]
  99. Moriya, N., Minamino, T., Hughes, K. T., MacNab, R. M. & Namba, K. ( 2006; ). The type III flagellar export specificity switch is dependent on FliK ruler and a molecular clock. J Mol Biol 359, 466–477.[CrossRef]
    [Google Scholar]
  100. Mulrooney, S. B. & Hausinger, R. P. ( 2003; ). Nickel uptake and utilization by microorganisms. FEMS Microbiol Rev 27, 239–261.[CrossRef]
    [Google Scholar]
  101. Neumann, M., Schulte, M., Junemann, N., Stocklein, W. & Leimkuhler, S. ( 2006; ). Rhodobacter capsulatus XdhC is involved in molybdenum cofactor binding and insertion into xanthine dehydrogenase. J Biol Chem 281, 15701–15708.[CrossRef]
    [Google Scholar]
  102. Nilavongse, A., Brondijk, T. H., Overton, T. W., Richardson, D. J., Leach, E. R. & Cole, J. A. ( 2006; ). The NapF protein of the Escherichia coli periplasmic nitrate reductase system: demonstration of a cytoplasmic location and interaction with the catalytic subunit, NapA. Microbiology 152, 3227–3237.[CrossRef]
    [Google Scholar]
  103. Nivière, V., Wong, S. L. & Voordouw, G. ( 1992; ). Site-directed mutagenesis of the hydrogenase signal peptide consensus box prevents export of a β-lactamase fusion protein. J Gen Microbiol 138, 2173–2183.[CrossRef]
    [Google Scholar]
  104. Oates, J., Mathers, J., Mangels, D., Kühlbrandt, W., Robinson, C. & Model, K. ( 2003; ). Consensus structural features of purified bacterial TatABC complexes. J Mol Biol 330, 277–286.[CrossRef]
    [Google Scholar]
  105. Oates, J., Barrett, C. M., Barnett, J. P., Byrne, K. G., Bolhuis, A. & Robinson, C. ( 2005; ). The Escherichia coli twin-arginine translocation apparatus incorporates a distinct form of TatABC complex, spectrum of modular TatA complexes and minor TatAB complex. J Mol Biol 346, 295–305.[CrossRef]
    [Google Scholar]
  106. Olmo-Mira, M. F., Gavira, M., Richardson, D. J., Castillo, F., Moreno-Vivian, C. & Roldan, M. D. ( 2004; ). NapF is a cytoplasmic iron-sulfur protein required for Fe–S cluster assembly in the periplasmic nitrate reductase. J Biol Chem 279, 49727–49735.[CrossRef]
    [Google Scholar]
  107. Oresnik, I. J., Ladner, C. L. & Turner, R. J. ( 2001; ). Identification of a twin-arginine leader-binding protein. Mol Microbiol 40, 323–331.[CrossRef]
    [Google Scholar]
  108. Palmer, T. & Berks, B. C. ( 2003; ). Moving folded proteins across the bacterial cell membrane. Microbiology 149, 547–556.[CrossRef]
    [Google Scholar]
  109. Papish, A. L., Ladner, C. L. & Turner, R. J. ( 2003; ). The twin-arginine leader-binding protein, DmsD, interacts with the TatB and TatC subunits of the Escherichia coli twin-arginine translocase. J Biol Chem 278, 32501–32506.[CrossRef]
    [Google Scholar]
  110. Paveglio, M. T., Tang, J. S., Unger, R. E. & Barrett, E. L. ( 1988; ). Formate-nitrate respiration in Salmonella typhimurium: studies of two rha-linked fdn genes. J Bacteriol 170, 213–217.
    [Google Scholar]
  111. Pierson, D. E. & Campbell, A. ( 1990; ). Cloning and nucleotide sequence of bisC, the structural gene for biotin sulfoxide reductase in Escherichia coli. J Bacteriol 172, 2194–2198.
    [Google Scholar]
  112. Pommier, J., Mejean, V., Giordano, G. & Iobbi-Nivol, C. ( 1998; ). TorD, a cytoplasmic chaperone that interacts with the unfolded trimethylamine N-oxide reductase enzyme (TorA) in Escherichia coli. J Biol Chem 273, 16615–16620.[CrossRef]
    [Google Scholar]
  113. Pop, O., Martin, U., Abel, C. & Müller, J. P. ( 2002; ). The twin-arginine signal peptide of PhoD and the TatAd/Cd proteins of Bacillus subtilis form an autonomous Tat translocation system. J Biol Chem 277, 3268–3273.[CrossRef]
    [Google Scholar]
  114. Porcelli, I., de Leeuw, E., Wallis, R., van den Brink-van der Laan, E., de Kruijff, B., Wallace, B. A., Palmer, T. & Berks, B. C. ( 2002; ). Characterization and membrane assembly of the TatA component of the Escherichia coli twin-arginine protein transport system. Biochemistry 41, 13690–13697.[CrossRef]
    [Google Scholar]
  115. Potter, L. C. & Cole, J. A. ( 1999; ). Essential roles for the products of the napABCD genes, but not napFGH, in periplasmic nitrate reduction by Escherichia coli K-12. Biochem J 344, 69–76.[CrossRef]
    [Google Scholar]
  116. Rabus, R., Kübe, M., Heider, J., Beck, A., Heitmann, K., Widdel, F. & Reinhardt, R. ( 2005; ). The genome sequence of an anaerobic aromatic-degrading denitrifying bacterium, strain EbN1. Arch Microbiol 183, 27–36.[CrossRef]
    [Google Scholar]
  117. Ray, N., Oates, J., Turner, R. J. & Robinson, C. ( 2003; ). DmsD is required for the biogenesis of DMSO reductase in Escherichia coli but not for the interaction of the DmsA signal peptide with the Tat apparatus. FEBS Lett 534, 156–160.[CrossRef]
    [Google Scholar]
  118. Richardson, D. J. ( 2000; ). Bacterial respiration: a flexible process for a changing environment. Microbiology 146, 551–571.
    [Google Scholar]
  119. Richardson, D. J., Berks, B. C., Russell, D. A., Spiro, S. & Taylor, C. J. ( 2001; ). Functional, biochemical and genetic diversity of prokaryotic nitrate reductases. Cell Mol Life Sci 58, 165–178.[CrossRef]
    [Google Scholar]
  120. Richter, S. & Brüser, T. ( 2005; ). Targeting of unfolded PhoA to the Tat translocon of Escherichia coli. J Biol Chem 280, 42723–42730.[CrossRef]
    [Google Scholar]
  121. Rodrigue, A., Chanal, A., Beck, K., Müller, M. & Wu, L.-F. ( 1999; ). Co-translocation of a periplasmic enzyme complex by a hitchhiker mechanism through the bacterial Tat pathway. J Biol Chem 274, 13223–13228.[CrossRef]
    [Google Scholar]
  122. Rose, R. W., Brüser, T., Kissinger, J. C. & Pohlschröder, M. ( 2002; ). Adaptation of protein secretion to extremely high-salt conditions by extensive use of the twin-arginine translocation pathway. Mol Microbiol 45, 943–950.[CrossRef]
    [Google Scholar]
  123. Rossmann, M. G., Liljas, A., Branden, C. I. & Bansazak, L. J. ( 1975; ). Evolutionary relationships among dehydrogenases. In The Enzymes, vol. 11. Edited by I. P. D. Boyer. New York: Academic Press.
  124. Rothery, R. A., Bertero, M. G., Cammack, R., Palak, M., Blasco, F., Strynadka, N. C. & Weiner, J. H. ( 2004; ). The catalytic subunit of Escherichia coli nitrate reductase A contains a novel [4Fe-4S] cluster with a high-spin ground state. Biochemistry 43, 5324–5333.[CrossRef]
    [Google Scholar]
  125. Rubio, L. M., Flores, E. & Herrero, A. ( 2002; ). Purification, cofactor analysis, and site-directed mutagenesis of Synechococcus ferredoxin-nitrate reductase. Photosynth Res 72, 13–26.[CrossRef]
    [Google Scholar]
  126. Ryan, R. P., Fouhy, Y., Lucey, J. F., Crossman, L. C., Spiro, S., He, Y. W., Zhang, L. H., Heeb, S., Camara, M. & other authors ( 2006; ). Cell-cell signaling in Xanthomonas campestris involves an HD-GYP domain protein that functions in cyclic di-GMP turnover. Proc Natl Acad Sci U S A 103, 6712–6717.[CrossRef]
    [Google Scholar]
  127. Sambasivarao, D., Turner, R. J., Simala-Grant, J. L., Shaw, G., Hu, J. & Weiner, J. H. ( 2000; ). Multiple roles for the twin arginine leader sequence of dimethyl sulfoxide reductase of Escherichia coli. J Biol Chem 275, 22526–22531.[CrossRef]
    [Google Scholar]
  128. San Miguel, M., Marrington, R., Rodger, P. M., Rodger, A. & Robinson, C. ( 2003; ). An Escherichia coli twin-arginine signal peptide switches between helical and unstructured conformations depending on the hydrophobicity of the environment. Eur J Biochem 270, 3345–3352.[CrossRef]
    [Google Scholar]
  129. Santiago, B., Schubel, U., Egelsee, C. & Meyer, O. ( 1999; ). Sequence analysis, characterization and CO-specific transcription of the cox gene cluster on the megaplasmid pHCG3 of Oligotropha carboxidovorans. Gene 236, 115–124.[CrossRef]
    [Google Scholar]
  130. Santini, C.-L., Ize, B., Chanal, A., Müller, M., Giordano, G. & Wu, L.-F. ( 1998; ). A novel Sec-independent periplasmic protein translocation pathway in Escherichia coli. EMBO J 17, 101–112.[CrossRef]
    [Google Scholar]
  131. Sarfo, K. J., Winstone, T. L., Papish, A. L., Howell, J. M., Kadir, H., Vogel, H. J. & Turner, R. J. ( 2004; ). Folding forms of Escherichia coli DmsD, a twin-arginine leader binding protein. Biochem Biophys Res Commun 315, 397–403.[CrossRef]
    [Google Scholar]
  132. Sargent, F., Bogsch, E. G., Stanley, N. R., Wexler, M., Robinson, C., Berks, B. C. & Palmer, T. ( 1998a; ). Overlapping functions of components of a bacterial Sec-independent protein export pathway. EMBO J 17, 3640–3650.[CrossRef]
    [Google Scholar]
  133. Sargent, F., Ballantine, S. P., Rugman, P. A., Palmer, T. & Boxer, D. H. ( 1998b; ). Reassignment of the gene encoding the Escherichia coli hydrogenase 2 small subunit – identification of a soluble precursor of the small subunit in a hypB mutant. Eur J Biochem 255, 746–754.[CrossRef]
    [Google Scholar]
  134. Sargent, F., Stanley, N. R., Berks, B. C. & Palmer, T. ( 1999; ). Sec-independent protein translocation in Escherichia coli: a distinct and pivotal role for the TatB protein. J Biol Chem 274, 36073–36082.[CrossRef]
    [Google Scholar]
  135. Sargent, F., Gohlke, U., de Leeuw, E., Stanley, N. R., Palmer, T., Saibil, H. R. & Berks, B. C. ( 2001; ). Purified components of the Escherichia coli Tat protein transport system form a double-layered ring structure. Eur J Biochem 268, 3361–3367.[CrossRef]
    [Google Scholar]
  136. Sargent, F., Berks, B. C. & Palmer, T. ( 2002; ). Assembly of membrane-bound respiratory complexes by the Tat protein-transport system. Arch Microbiol 178, 77–84.[CrossRef]
    [Google Scholar]
  137. Sargent, F., Berks, B. C. & Palmer, T. ( 2006; ). Pathfinders and trailblazers: a prokaryotic targeting system for transport of folded proteins. FEMS Microbiol Lett 254, 198–207.[CrossRef]
    [Google Scholar]
  138. Schindelin, H., Kisker, C., Hilton, J., Rajagopalan, K. V. & Rees, D. C. ( 1996; ). Crystal structure of DMSO reductase: redox-linked changes in molybdopterin coordination. Science 272, 1615–1621.[CrossRef]
    [Google Scholar]
  139. Schlindwein, C., Giordano, G., Santini, C.-L. & Mandrand, M.-A. ( 1990; ). Identification and expression of the Escherichia coli fdhD and fdhE genes, which are involved in the formation of respiratory formate dehydrogenase. J Bacteriol 172, 6112–6121.
    [Google Scholar]
  140. Schneider, F., Lowe, J., Hüber, R., Schindelin, H., Kisker, C. & Knablein, J. ( 1996; ). Crystal structure of dimethyl sulfoxide reductase from Rhodobacter capsulatus at 1.88 Å resolution. J Mol Biol 263, 53–69.[CrossRef]
    [Google Scholar]
  141. Schwarz, G. ( 2005; ). Molybdenum cofactor biosynthesis and deficiency. Cell Mol Life Sci 62, 2792–2810.[CrossRef]
    [Google Scholar]
  142. Settles, A. M., Yonetani, A., Baron, A., Bush, D. R., Cline, K. & Martienssen, R. ( 1997; ). Sec-independent protein translocation by the maize Hcf106 protein. Science 278, 1467–1470.[CrossRef]
    [Google Scholar]
  143. Shaw, A. L., Leimkuhler, S., Klipp, W., Hanson, G. R. & McEwan, A. G. ( 1999; ). Mutational analysis of the dimethyl sulfoxide respiratory (dor) operon of Rhodobacter capsulatus. Microbiology 145, 1409–1420.[CrossRef]
    [Google Scholar]
  144. Soballe, B. & Poole, R. K. ( 1999; ). Microbial ubiquinones: multiple roles in respiration, gene regulation and oxidative stress management. Microbiology 145, 1817–1830.[CrossRef]
    [Google Scholar]
  145. Stan, T., Ahting, U., Dembowski, M., Kunkele, K. P., Nussberger, S., Neupert, W. & Rapaport, D. ( 2000; ). Recognition of preproteins by the isolated TOM complex of mitochondria. EMBO J 19, 4895–4902.[CrossRef]
    [Google Scholar]
  146. Stanley, N. R., Sargent, F., Buchanan, G., Shi, J., Stewart, V., Palmer, T. & Berks, B. C. ( 2002; ). Behaviour of topological marker proteins targeted to the Tat protein transport pathway. Mol Microbiol 43, 1005–1021.[CrossRef]
    [Google Scholar]
  147. Stevens, J. M., Daltrop, O., Allen, J. W. & Ferguson, S. J. ( 2004; ). C-type cytochrome formation: chemical and biological enigmas. Acc Chem Res 37, 999–1007.[CrossRef]
    [Google Scholar]
  148. Stewart, V., Lin, J. T. & Berg, B. L. ( 1991; ). Genetic evidence that genes fdhD and fdhE do not control synthesis of formate dehydrogenase-N in Escherichia coli K-12. J Bacteriol 173, 4417–4423.
    [Google Scholar]
  149. Temple, C. A. & Rajagopalan, K. V. ( 2000; ). Mechanism of assembly of the bis(molybdopteringuanine dinucleotide) molybdenum cofactor in Rhodobacter sphaeroides dimethyl sulfoxide reductase. J Biol Chem 275, 40202–40210.[CrossRef]
    [Google Scholar]
  150. Theg, S. M., Cline, K., Finazzi, G. & Wollman, F. A. ( 2005; ). The energetics of the chloroplast Tat protein transport pathway revisited. Trends Plant Sci 10, 153–154.[CrossRef]
    [Google Scholar]
  151. Tokuda, H. & Matsuyama, S. ( 2004; ). Sorting of lipoproteins to the outer membrane in E. coli. Biochim Biophys Acta 1693, 5–13.[CrossRef]
    [Google Scholar]
  152. Tranier, S., Mortier-Barriere, I., Ilbert, M., Birck, C., Iobbi-Nivol, C., Mejean, V. & Samama, J.-P. ( 2002; ). Characterization and multiple molecular forms of TorD from Shewanella massilia, the putative chaperone of the molybdoenzyme TorA. Protein Sci 11, 2148–2157.
    [Google Scholar]
  153. Tranier, S., Iobbi-Nivol, C., Birck, C., Ilbert, M., Mortier-Barriere, I., Mejean, V. & Samama, J.-P. ( 2003; ). A novel protein fold and extreme domain swapping in the dimeric TorD chaperone from Shewanella massilia. Structure 11, 165–174.[CrossRef]
    [Google Scholar]
  154. Truglio, J. J., Theis, K., Leimkühler, S., Rappa, R., Rajagopalan, K. V. & Kisker, C. ( 2002; ). Crystal structures of the active and alloxanthine-inhibited forms of xanthine dehydrogenase from Rhodobacter capsulatus. Structure 10, 115–125.[CrossRef]
    [Google Scholar]
  155. Turner, R. J., Papish, A. L. & Sargent, F. ( 2004; ). Sequence analysis of bacterial redox enzyme maturation proteins (REMPs). Can J Microbiol 50, 225–238.[CrossRef]
    [Google Scholar]
  156. Vandeputte-Rutten, L., Kramer, R. A., Kroon, J., Dekker, N., Egmond, M. R. & Gros, P. ( 2001; ). Crystal structure of the outer membrane protease OmpT from Escherichia coli suggests a novel catalytic site. EMBO J 20, 5033–5039.[CrossRef]
    [Google Scholar]
  157. van Dongen, W., Hagen, W., van den Berg, W. & Veeger, C. ( 1988; ). Evidence for an unusual mechanism of membrane translocation of the periplasmic hydrogenase of Desulfovibrio vulgaris (Hildenborough), as derived from expression in Escherichia coli. FEMS Microbiol Lett 50, 5–9.
    [Google Scholar]
  158. van Keulen, G., Alderson, J., White, J. & Sawers, R. G. ( 2005; ). Nitrate respiration in the actinomycete Streptomyces coelicolor. Biochem Soc Trans 33, 210–212.[CrossRef]
    [Google Scholar]
  159. Vergnes, A., Pommier, J., Toci, R., Blasco, F., Giordano, G. & Magalon, A. ( 2006; ). NarJ chaperone binds on two distinct sites of the aponitrate reductase of Escherichia coli to coordinate molybdenum cofactor insertion and assembly. J Biol Chem 281, 2170–2176.[CrossRef]
    [Google Scholar]
  160. Voelker, R. & Barkan, A. ( 1995; ). Two nuclear mutations disrupt distinct pathways for targeting proteins to the chloroplast thylakoid. EMBO J 14, 3905–3914.
    [Google Scholar]
  161. von Rozycki, T., Yen, M. R., Lende, E. E. & Saier, M. H., Jr ( 2004; ). The YedZ family: possible heme binding proteins that can be fused to transporters and electron carriers. J Mol Microbiol Biotechnol 8, 129–140.[CrossRef]
    [Google Scholar]
  162. Vrontou, E. & Economou, A. ( 2004; ). Structure and function of SecA, the preprotein translocase nanomotor. Biochim Biophys Acta 694, 67–80.
    [Google Scholar]
  163. Walker, J. E., Saraste, M., Runswick, M. J. & Gay, N. J. ( 1982; ). Distantly related sequences in the α- and β-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J 1, 945–951.
    [Google Scholar]
  164. Weiner, J. H., Bilous, P. T., Shaw, G. M., Lubitz, S. P., Frost, L., Thomas, G. H., Cole, J. A. & Turner, R. J. ( 1998; ). A novel and ubiquitous system for membrane targeting and secretion of cofactor-containing proteins. Cell 93, 93–101.[CrossRef]
    [Google Scholar]
  165. Widdick, D. A., Dilks, K., Chandra, G., Bottrill, A., Naldrett, M., Pohlschröder, M. & Palmer, T. ( 2006; ). The twin-arginine translocation pathway is a major route of protein export in Streptomyces coelicolor. Proc Natl Acad Sci U S A 103, 17927–17932.[CrossRef]
    [Google Scholar]
  166. Winstone, T. L., Workentine, M. L., Sarfo, K. J., Binding, A. J., Haslam, B. D. & Turner, R. J. ( 2006; ). Physical nature of signal peptide binding to DmsD. Arch Biochem Biophys 455, 89–97.[CrossRef]
    [Google Scholar]
  167. Wu, L.-F., Chanal, A. & Rodrigue, A. ( 2000; ). Membrane targeting and translocation of bacterial hydrogenases. Arch Microbiol 173, 319–324.[CrossRef]
    [Google Scholar]
  168. Xi, H., Schneider, B. L. & Reitzer, L. ( 2000; ). Purine catabolism in Escherichia coli and function of xanthine dehydrogenase in purine salvage. J Bacteriol 182, 5332–5341.[CrossRef]
    [Google Scholar]
  169. Yakunin, A. F., Proudfoot, M., Kuznetsova, E., Savchenko, A., Brown, G., Arrowsmith, C. H. & Edwards, A. M. ( 2004; ). The HD domain of the Escherichia coli tRNA nucleotidyltransferase has 2′,3′-cyclic phosphodiesterase, 2′-nucleotidase, and phosphatase activities. J Biol Chem 279, 36819–36827.[CrossRef]
    [Google Scholar]
  170. Yamagata, A., Kakuta, Y., Masui, R. & Fukuyama, K. ( 2002; ). The crystal structure of exonuclease RecJ bound to Mn2+ ion suggests how its characteristic motifs are involved in exonuclease activity. Proc Natl Acad Sci U S A 99, 5908–5912.[CrossRef]
    [Google Scholar]
  171. Yates, M. G., de Souza, E. M. & Kahindi, J. H. ( 1997; ). Oxygen, hydrogen and nitrogen fixation in Azotobacter. Soil Biol Biochem 29, 863–869.[CrossRef]
    [Google Scholar]
  172. Yoshimatsu, K., Araya, O. & Fujiwara, T. ( 2007; ). Haloarcula marismortui cytochrome b-561 is encoded by the narC gene in the dissimilatory nitrate reductase operon. Extremophiles 11, 41–47.[CrossRef]
    [Google Scholar]
  173. Zafra, O., Cava, F., Blasco, F., Magalon, A. & Berenguer, J. ( 2005; ). Membrane-associated maturation of the heterotetrameric nitrate reductase of Thermus thermophilus. J Bacteriol 187, 3990–3996.[CrossRef]
    [Google Scholar]
  174. Zajicek, R. S., Allen, J. W., Cartron, M. L., Richardson, D. J. & Ferguson, S. J. ( 2004; ). Paracoccus pantotrophus NapC can reductively activate cytochrome cd 1 nitrite reductase. FEBS Lett 565, 48–52.[CrossRef]
    [Google Scholar]
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