1887

Abstract

This review argues that knowledge of microbial physiology and metabolism is a prerequisite to understanding mechanisms of pathogenicity. The ability of to cope with stresses such as those found during infection requires a sialyltransferase to sialylate its lipopolysaccharide using host-derived CMP-NANA in the human bloodstream, the ability to oxidize lactate that is abundant in the human body, outer-membrane lipoproteins that provide the first line of protection against oxidative and nitrosative stress, regulation of NO reduction independently from the nitrite reductase that forms NO, an extra haem group on the C-terminal extension of a cytochrome oxidase subunit, and a respiratory capacity far in excess of metabolic requirements. These properties are all normal components of neisserial physiology; they would all fail rigid definitions of a pathogenicity determinant. In anaerobic cultures of enteric bacteria, duplicate pathways for nitrate reduction to ammonia provide a selective advantage when nitrate is either abundant or scarce. Selection of these alternative pathways is in part regulated by two parallel two-component regulatory systems. NarX–NarL primarily ensures that nitrate is reduced in preference to thermodynamically less favourable terminal electron acceptors, but NarQ–NarP facilitates reduction of limited quantities of nitrate or other, less favourable, terminal electron acceptors in preference to fermentative growth. How enteric bacteria repair damage caused by nitrosative and oxidative damage inflicted by host defences is less well understood. In both and , parallel pathways that duplicate particular biochemical functions are far from redundant, but fulfil specific physiological roles.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.059048-0
2012-06-01
2019-10-23
Loading full text...

Full text loading...

/deliver/fulltext/micro/158/6/1402.html?itemId=/content/journal/micro/10.1099/mic.0.059048-0&mimeType=html&fmt=ahah

References

  1. Abou-Jaoudé A. , Chippaux M. , Pascal M.-C. , Casse F. . ( 1977; ). Formate: a new electron donor for nitrite reduction in Escherichia coli K12. . Biochem Biophys Res Commun 78:, 579–583. [CrossRef] [PubMed]
    [Google Scholar]
  2. Almeida C. C. , Romão C. V. , Lindley P. F. , Teixeira M. , Saraiva L. M. . ( 2006; ). The role of the hybrid cluster protein in oxidative stress defense. . J Biol Chem 281:, 32445–32450. [CrossRef] [PubMed]
    [Google Scholar]
  3. Anjum M. F. , Stevanin T. M. , Read R. C. , Moir J. W. . ( 2002; ). Nitric oxide metabolism in Neisseria meningitidis . . J Bacteriol 184:, 2987–2993. [CrossRef] [PubMed]
    [Google Scholar]
  4. Arendsen A. , Hadden J. , Card G. , McAlpine A. S. , Bailey S. , Zaitsev V. , Duke E. H. M. , Lindley P. , Kröckel M. et al. ( 1998; ). The “prismane” protein resolved: Xray structure at 1.7 Å and multiple spectroscopy of two novel 4Fe clusters. . J Biol Inorg Chem 3:, 81–95. [CrossRef]
    [Google Scholar]
  5. Aspholm M. , Aas F. E. , Harrison O. B. , Quinn D. , Vik Å. , Viburiene R. , Tønjum T. , Moir J. , Maiden M. C. J. , Koomey M. . ( 2010; ). Structural alterations in a component of cytochrome c oxidase and molecular evolution of pathogenic Neisseria in humans. . PLoS Pathog 6:, e1001055. [CrossRef] [PubMed]
    [Google Scholar]
  6. Beaumont H. J. E. , Lens S. I. , Reijnders W. N. M. , Westerhoff H. V. , van Spanning R. J. M. . ( 2004; ). Expression of nitrite reductase in Nitrosomonas europaea involves NsrR, a novel nitrite-sensitive transcription repressor. . Mol Microbiol 54:, 148–158. [CrossRef] [PubMed]
    [Google Scholar]
  7. Bodenmiller D. M. , Spiro S. . ( 2006; ). The yjeB (nsrR) gene of Escherichia coli encodes a nitric oxide-sensitive transcriptional regulator. . J Bacteriol 188:, 874–881. [CrossRef] [PubMed]
    [Google Scholar]
  8. Browning D. F. , Lee D. J. , Wolfe A. J. , Cole J. A. , Busby S. J. W. . ( 2006; ). The Escherichia coli K-12 NarL and NarP proteins insulate the nrf promoter from the effects of integration host factor. . J Bacteriol 188:, 7449–7456. [CrossRef] [PubMed]
    [Google Scholar]
  9. Browning D. F. , Cole J. A. , Busby S. J. W. . ( 2008; ). Regulation by nucleoid-associated proteins at the Escherichia coli nir operon promoter. . J Bacteriol 190:, 7258–7267. [CrossRef] [PubMed]
    [Google Scholar]
  10. Browning D. F. , Lee D. J. , Spiro S. , Busby S. J. W. . ( 2010; ). Down-regulation of the Escherichia coli K-12 nrf promoter by binding of the NsrR nitric oxide-sensing transcription repressor to an upstream site. . J Bacteriol 192:, 3824–3828. [CrossRef] [PubMed]
    [Google Scholar]
  11. Butlin K. R. , Postgate J. R. . ( 1953; ). Microbial formation of sulphide and sulphur. Microbial Metabolism, Symp 6th Congr int Microbiol p. 126..
    [Google Scholar]
  12. Cabello P. , Pino C. , Olmo-Mira M. F. , Castillo F. , Roldán M. D. , Moreno-Vivián C. . ( 2004; ). Hydroxylamine assimilation by Rhodobacter capsulatus E1F1: requirement of the hcp gene (hybrid cluster protein) located in the nitrate assimilation nas gene region for hydroxylamine reduction. . J Biol Chem 279:, 45485–45494. [CrossRef] [PubMed]
    [Google Scholar]
  13. Calmels S. , Ohshima H. , Bartsch H. . ( 1988; ). Calmels S. , Ohshima H. , Bartsch H. . ( 1988; ). Nitrosamine formation by denitrifying and non-denitrifying bacteria: implication of nitrite reductase and nitrate reductase in nitrosation catalysis. . J Gen Microbiol 134:, 221–226.[PubMed]
    [Google Scholar]
  14. Chismon D. L. , Browning D. F. , Farrant G. K. , Busby S. J. . ( 2010; ). Unusual organization, complexity and redundancy at the Escherichia coli hcp-hcr operon promoter. . Biochem J 430:, 61–68. [CrossRef] [PubMed]
    [Google Scholar]
  15. Clark V. L. , Campbell L. A. , Palermo D. A. , Evans T. M. , Klimpel K. W. . ( 1987; ). Induction and repression of outer membrane proteins by anaerobic growth of Neisseria gonorrhoeae . . Infect Immun 55:, 1359–1364.[PubMed]
    [Google Scholar]
  16. Clark V. L. , Knapp J. S. , Thompson S. , Klimpel K. W. . ( 1988; ). Presence of antibodies to the major anaerobically induced gonococcal outer membrane protein in sera from patients with gonococcal infections. . Microb Pathog 5:, 381–390. [CrossRef] [PubMed]
    [Google Scholar]
  17. Constantinidou C. , Hobman J. L. , Griffiths L. , Patel M. D. , Penn C. W. , Cole J. A. , Overton T. W. . ( 2006; ). A reassessment of the FNR regulon and transcriptomic analysis of the effects of nitrate, nitrite, NarXL, and NarQP as Escherichia coli K12 adapts from aerobic to anaerobic growth. . J Biol Chem 281:, 4802–4815. [CrossRef] [PubMed]
    [Google Scholar]
  18. Corker H. , Poole R. K. . ( 2003; ). Nitric oxide formation by Escherichia coli. Dependence on nitrite reductase, the NO-sensing regulator Fnr, and flavohemoglobin Hmp. . J Biol Chem 278:, 31584–31592. [CrossRef] [PubMed]
    [Google Scholar]
  19. Cruz-Ramos H. , Crack J. , Wu G. , Hughes M. N. , Scott C. , Thomson A. J. , Green J. , Poole R. K. . ( 2002; ). NO sensing by FNR: regulation of the Escherichia coli NO-detoxifying flavohaemoglobin, Hmp. . EMBO J 21:, 3235–3244. [CrossRef] [PubMed]
    [Google Scholar]
  20. D’Autréaux B. , Tucker N. P. , Dixon R. , Spiro S. . ( 2005; ). A non-haem iron centre in the transcription factor NorR senses nitric oxide. . Nature 437:, 769–772. [CrossRef] [PubMed]
    [Google Scholar]
  21. Filenko N. S. , Spiro S. , Browning D. F. , Squire D. , Overton T. W. , Cole J. , Constantinidou C. . ( 2007; ). The NsrR regulon of Escherichia coli K-12 includes genes encoding the hybrid cluster protein and the periplasmic, respiratory nitrite reductase. . J Bacteriol 189:, 4410–4417. [CrossRef] [PubMed]
    [Google Scholar]
  22. Gardner A. M. , Gardner P. R. . ( 2002; ). Flavohemoglobin detoxifies nitric oxide in aerobic, but not anaerobic, cultures of Escherichia coli. Evidence for a novel inducible nitric oxide-scavenging activity. . J Biol Chem 277:, 8166–8171. [CrossRef] [PubMed]
    [Google Scholar]
  23. Gardner A. M. , Gessner C. R. , Gardner P. R. . ( 2003; ). Regulation of the nitric oxide reduction operon (norRVW) in Escherichia coli. Role of NorR and σ54 in the nitric oxide stress response. . J Biol Chem 278:, 10081–10086. [CrossRef] [PubMed]
    [Google Scholar]
  24. Gilberthorpe N. J. , Poole R. K. . ( 2008; ). Nitric oxide homeostasis in Salmonella typhimurium: roles of respiratory nitrate reductase and flavohemoglobin. . J Biol Chem 283:, 11146–11154. [CrossRef] [PubMed]
    [Google Scholar]
  25. Gomes C. M. , Giuffrè A. , Forte E. , Vicente J. B. , Saraiva L. M. , Brunori M. , Teixeira M. . ( 2002; ). A novel type of nitric-oxide reductase. Escherichia coli flavorubredoxin. . J Biol Chem 277:, 25273–25276. [CrossRef] [PubMed]
    [Google Scholar]
  26. Grainger D. C. , Aiba H. , Hurd D. , Browning D. F. , Busby S. J. . ( 2007; ). Transcription factor distribution in Escherichia coli: studies with FNR protein. . Nucleic Acids Res 35:, 269–278. [CrossRef] [PubMed]
    [Google Scholar]
  27. Gray C. T. , Wimpenny J. W. T. , Hughes D. E. , Mossman M. R. . ( 1966; ). Regulation of metabolism in facultative bacteria. I. Structural and functional changes in Escherichia coli associated with shifts between the aerobic and anaerobic states. . Biochim Biophys Acta 117:, 22–32. [CrossRef] [PubMed]
    [Google Scholar]
  28. Green J. , Bennett B. , Jordan P. , Ralph E. T. , Thomson A. J. , Guest J. R. . ( 1996; ). Reconstitution of the [4Fe-4S] cluster in FNR and demonstration of the aerobic-anaerobic transcription switch in vitro . . Biochem J 316:, 887–892.[PubMed]
    [Google Scholar]
  29. Hausladen A. , Gow A. J. , Stamler J. S. . ( 1998; ). Nitrosative stress: metabolic pathway involving the flavohaemoglobin. . Proc Natl Acad Sci U S A 95:, 14100–14105. [CrossRef]
    [Google Scholar]
  30. Hopper A. , Tovell N. , Cole J. A. . ( 2009; ). A physiologically significant role in nitrite reduction of the CcoP subunit of the cytochrome oxidase cbb3 from Neisseria gonorrhoeae . . FEMS Microbiol Lett 301:, 232–240. [CrossRef] [PubMed]
    [Google Scholar]
  31. Householder T. C. , Fozo E. M. , Cardinale J. A. , Clark V. L. . ( 2000; ). Gonococcal nitric oxide reductase is encoded by a single gene, norB, which is required for anaerobic growth and is induced by nitric oxide. . Infect Immun 68:, 5241–5246. [CrossRef] [PubMed]
    [Google Scholar]
  32. Hutchings M. I. , Shearer N. , Wastell S. , van Spanning R. J. , Spiro S. . ( 2000; ). Heterologous NNR-mediated nitric oxide signaling in Escherichia coli . . J Bacteriol 182:, 6434–6439. [CrossRef] [PubMed]
    [Google Scholar]
  33. Jackson R. H. , Cornish-Bowden A. , Cole J. A. . ( 1981; ). Prosthetic groups of the NADH-dependent nitrite reductase from Escherichia coli K12. . Biochem J 193:, 861–867.[PubMed]
    [Google Scholar]
  34. Ji X.-B. , Hollocher T. C. . ( 1988; ). Mechanism for nitrosation of 2,3-diaminonaphthalene by Escherichia coli: enzymatic production of NO followed by O2-dependent chemical nitrosation. . Appl Environ Microbiol 54:, 1791–1794.[PubMed]
    [Google Scholar]
  35. Johnson S. R. , Steiner B. M. , Perkins G. H. . ( 1996; ). Cloning and characterization of the catalase gene of Neisseria gonorrhoeae: use of the gonococcus as a host organism for recombinant DNA. . Infect Immun 64:, 2627–2634.[PubMed]
    [Google Scholar]
  36. Justino M. C. , Vicente J. B. , Teixeira M. , Saraiva L. M. . ( 2005; ). New genes implicated in the protection of anaerobically grown Escherichia coli against nitric oxide. . J Biol Chem 280:, 2636–2643. [CrossRef] [PubMed]
    [Google Scholar]
  37. Justino M. C. , Almeida C. C. , Gonçalves V. L. , Teixeira M. , Saraiva L. M. . ( 2006; ). Escherichia coli YtfE is a di-iron protein with an important function in assembly of iron-sulphur clusters. . FEMS Microbiol Lett 257:, 278–284. [CrossRef] [PubMed]
    [Google Scholar]
  38. Justino M. C. , Almeida C. C. , Teixeira M. , Saraiva L. M. . ( 2007; ). Escherichia coli di-iron YtfE protein is necessary for the repair of stress-damaged iron-sulfur clusters. . J Biol Chem 282:, 10352–10359. [CrossRef] [PubMed]
    [Google Scholar]
  39. Kartal B. , Maalcke W. J. , de Almeida N. M. , Cirpus I. , Gloerich J. , Geerts W. , Op den Camp H. J. , Harhangi H. R. , Janssen-Megens E. M. et al. ( 2011; ). Molecular mechanism of anaerobic ammonium oxidation. . Nature 479:, 127–130. [CrossRef] [PubMed]
    [Google Scholar]
  40. Khoroshilova N. , Popescu C. , Münck E. , Beinert H. , Kiley P. J. . ( 1997; ). Iron-sulfur cluster disassembly in the FNR protein of Escherichia coli by O2: [4Fe-4S] to [2Fe-2S] conversion with loss of biological activity. . Proc Natl Acad Sci U S A 94:, 6087–6092. [CrossRef] [PubMed]
    [Google Scholar]
  41. Knapp J. S. , Clark V. L. . ( 1984; ). Anaerobic growth of Neisseria gonorrhoeae coupled to nitrite reduction. . Infect Immun 46:, 176–181.[PubMed]
    [Google Scholar]
  42. Li Y. , Hopper A. , Overton T. W. , Squire D. J. P. , Cole J. , Tovell N. . ( 2010; ). Organization of the electron transfer chain to oxygen in the obligate human pathogen Neisseria gonorrhoeae: roles for cytochromes c4 and c5 , but not cytochrome c2 , in oxygen reduction. . J Bacteriol 192:, 2395–2406. [CrossRef] [PubMed]
    [Google Scholar]
  43. Lin H.-Y. , Bledsoe P. J. , Stewart V. . ( 2007; ). Activation of yeaR-yoaG operon transcription by the nitrate-responsive regulator NarL is independent of oxygen-responsive regulator Fnr in Escherichia coli K-12. . J Bacteriol 189:, 7539–7548. [CrossRef] [PubMed]
    [Google Scholar]
  44. Lissenden S. , Mohan S. , Overton T. , Regan T. , Crooke H. , Cardinale J. A. , Householder T. C. , Adams P. , O’Conner C. D. et al. ( 2000; ). Identification of transcription activators that regulate gonococcal adaptation from aerobic to anaerobic or oxygen-limited growth. . Mol Microbiol 37:, 839–855. [CrossRef] [PubMed]
    [Google Scholar]
  45. Martinez-Espinosa R. M. , Dridge E. J. , Bonete M. J. , Butt J. N. , Butler C. S. , Sargent F. , Richardson D. J. . ( 2007; ). Look on the positive side! The orientation, identification and bioenergetics of ‘Archaeal’ membrane-bound nitrate reductases. . FEMS Microbiol Lett 276:, 129–139. [CrossRef] [PubMed]
    [Google Scholar]
  46. Mesa S. , Bedmar E. J. , Chanfon A. , Hennecke H. , Fischer H. M. . ( 2003; ). Bradyrhizobium japonicum NnrR, a denitrification regulator, expands the FixLJ-FixK2 regulatory cascade. . J Bacteriol 185:, 3978–3982. [CrossRef] [PubMed]
    [Google Scholar]
  47. Metheringham R. , Cole J. A. . ( 1997; ). A reassessment of the genetic determinants, the effect of growth conditions and the availability of an electron donor on the nitrosating activity of Escherichia coli K-12. . Microbiology 143:, 2647–2656. [CrossRef] [PubMed]
    [Google Scholar]
  48. Morse S. A. . ( 1979; ). The biology of the gonococcus. . Crit Rev Microbiol 7:, 93–189.[CrossRef]
    [Google Scholar]
  49. Morse S. A. , Bartenstein L. . ( 1974; ). Factors affecting autolysis of Neisseria gonorrhoeae . . Proc Soc Exp Biol Med 145:, 1418–1421.[PubMed] [CrossRef]
    [Google Scholar]
  50. Nairn C. A. , Cole J. A. , Patel P. V. , Parsons N. J. , Fox J. E. , Smith H. . ( 1988; ). Cytidine 5′-monophospho-N-acetylneuraminic acid or a related compound is the low Mr factor from human red blood cells which induces gonococcal resistance to killing by human serum. . J Gen Microbiol 134:, 3295–3306.[PubMed]
    [Google Scholar]
  51. Overeijnder M. L. , Hagen W. R. , Hagedoorn P.-L. . ( 2009; ). A thermostable hybrid cluster protein from Pyrococcus furiosus: effects of the loss of a three helix bundle subdomain. . J Biol Inorg Chem 14:, 703–710. [CrossRef] [PubMed]
    [Google Scholar]
  52. Overton T. W. , Whitehead R. , Li Y. , Snyder L. A. S. , Saunders N. J. , Smith H. , Cole J. A. . ( 2006; ). Coordinated regulation of the Neisseria gonorrhoeae-truncated denitrification pathway by the nitric oxide-sensitive repressor, NsrR, and nitrite-insensitive NarQ-NarP. . J Biol Chem 281:, 33115–33126. [CrossRef] [PubMed]
    [Google Scholar]
  53. Overton T. W. , Justino M. C. , Li Y. , Baptista J. M. , Melo A. M. , Cole J. A. , Saraiva L. M. . ( 2008; ). Widespread distribution in pathogenic bacteria of di-iron proteins that repair oxidative and nitrosative damage to iron-sulfur centers. . J Bacteriol 190:, 2004–2013. [CrossRef] [PubMed]
    [Google Scholar]
  54. Page L. , Griffiths L. , Cole J. A. . ( 1990; ). Different physiological roles of two independent pathways for nitrite reduction to ammonia by enteric bacteria. . Arch Microbiol 154:, 349–354. [CrossRef] [PubMed]
    [Google Scholar]
  55. Parsons N. J. , Patel P. V. , Tan E. L. , Andrade J. R. C. , Nairn C. A. , Goldner M. , Cole J. A. , Smith H. . ( 1988; ). Cytidine 5′-monophospho-N-acetyl neuraminic acid and a low molecular weight factor from human blood cells induce lipopolysaccharide alteration in gonococci when conferring resistance to killing by human serum. . Microb Pathog 5:, 303–309. [CrossRef] [PubMed]
    [Google Scholar]
  56. Partridge J. D. , Bodenmiller D. M. , Humphrys M. S. , Spiro S. . ( 2009; ). NsrR targets in the Escherichia coli genome: new insights into DNA sequence requirements for binding and a role for NsrR in the regulation of motility. . Mol Microbiol 73:, 680–694. [CrossRef] [PubMed]
    [Google Scholar]
  57. Pascal M.-C. , Burini J.-F. , Chippaux M. . ( 1984; ). Regulation of the trimethylamine N-oxide (TMAO) reductase in Escherichia coli: analysis of tor:Mud1 operon fusion. . Mol Gen Genet 195:, 351–355. [CrossRef] [PubMed]
    [Google Scholar]
  58. Pitcher R. S. , Watmough N. J. . ( 2004; ). The bacterial cytochrome cbb3 oxidases. . Biochim Biophys Acta 1655:, 388–399. [CrossRef] [PubMed]
    [Google Scholar]
  59. Poock S. R. , Leach E. R. , Moir J. W. B. , Cole J. A. , Richardson D. J. . ( 2002; ). Respiratory detoxification of nitric oxide by the cytochrome c nitrite reductase of Escherichia coli . . J Biol Chem 277:, 23664–23669. [CrossRef] [PubMed]
    [Google Scholar]
  60. Poole R. K. , Anjum M. F. , Membrillo-Hernández J. , Kim S. O. , Hughes M. N. , Stewart V. . ( 1996; ). Nitric oxide, nitrite, and Fnr regulation of hmp (flavohemoglobin) gene expression in Escherichia coli K-12. . J Bacteriol 178:, 5487–5492.[PubMed]
    [Google Scholar]
  61. Postgate J. R. . ( 1956; ). Cytochrome c 3 and desulphoviridin; pigments of the anaerobe Desulphovibrio desulphuricans . . J Gen Microbiol 14:, 545–572.[PubMed] [CrossRef]
    [Google Scholar]
  62. Potter L. C. , Millington P. , Griffiths L. , Thomas G. H. , Cole J. A. . ( 1999; ). Competition between Escherichia coli strains expressing either a periplasmic or a membrane-bound nitrate reductase: does Nap confer a selective advantage during nitrate-limited growth?. Biochem J 344:, 77–84. [CrossRef] [PubMed]
    [Google Scholar]
  63. Preisig O. , Anthamatten D. , Hennecke H. . ( 1993; ). Genes for a microaerobically induced oxidase complex in Bradyrhizobium japonicum are essential for a nitrogen-fixing endosymbiosis. . Proc Natl Acad Sci U S A 90:, 3309–3313. [CrossRef] [PubMed]
    [Google Scholar]
  64. Pullan S. T. , Gidley M. D. , Jones R. A. , Barrett J. , Stevanin T. M. , Read R. C. , Green J. , Poole R. K. . ( 2007; ). Nitric oxide in chemostat-cultured Escherichia coli is sensed by Fnr and other global regulators: unaltered methionine biosynthesis indicates lack of S nitrosation. . J Bacteriol 189:, 1845–1855. [CrossRef] [PubMed]
    [Google Scholar]
  65. Rabin R. S. , Stewart V. . ( 1993; ). Dual response regulators (NarL and NarP) interact with dual sensors (NarX and NarQ) to control nitrate- and nitrite-regulated gene expression in Escherichia coli K-12. . J Bacteriol 175:, 3259–3268.[PubMed]
    [Google Scholar]
  66. Ralt D. , Wishnok J. S. , Fitts R. , Tannenbaum S. R. . ( 1988; ). Bacterial catalysis of nitrosation: involvement of the nar operon of Escherichia coli . . J Bacteriol 170:, 359–364.[PubMed]
    [Google Scholar]
  67. Rankin L. D. , Bodenmiller D. M. , Partridge J. D. , Nishino S. F. , Spain J. C. , Spiro S. . ( 2008; ). Escherichia coli NsrR regulates a pathway for the oxidation of 3-nitrotyramine to 4-hydroxy-3-nitrophenylacetate. . J Bacteriol 190:, 6170–6177. [CrossRef] [PubMed]
    [Google Scholar]
  68. Rey L. , Maier R. J. . ( 1997; ). Cytochrome c terminal oxidase pathways of Azotobacter vinelandii: analysis of cytochrome c4 and c5 mutants and up-regulation of cytochrome c-dependent pathways with N2 fixation. . J Bacteriol 179:, 7191–7196.[PubMed]
    [Google Scholar]
  69. Richardson A. R. , Dunman P. M. , Fang F. C. . ( 2006; ). The nitrosative stress response of Staphylococcus aureus is required for resistance to innate immunity. . Mol Microbiol 61:, 927–939. [CrossRef] [PubMed]
    [Google Scholar]
  70. Rock J. D. , Thomson M. J. , Read R. C. , Moir J. W. B. . ( 2007; ). Regulation of denitrification genes in Neisseria meningitidis by nitric oxide and the repressor NsrR. . J Bacteriol 189:, 1138–1144. [CrossRef] [PubMed]
    [Google Scholar]
  71. Rodionov D. A. , Dubchak I. L. , Arkin A. P. , Alm E. J. , Gelfand M. S. . ( 2005; ). Dissimilatory metabolism of nitrogen oxides in bacteria: comparative reconstruction of transcriptional networks. . PLOS Comput Biol 1:, e55. [CrossRef] [PubMed]
    [Google Scholar]
  72. Seib K. L. , Wu H.-J. , Kidd S. P. , Apicella M. A. , Jennings M. P. , McEwan A. G. . ( 2006; ). Defenses against oxidative stress in Neisseria gonorrhoeae: a system tailored for a challenging environment. . Microbiol Mol Biol Rev 70:, 344–361. [CrossRef] [PubMed]
    [Google Scholar]
  73. Showe M. K. , DeMoss J. A. . ( 1968; ). Localization and regulation of synthesis of nitrate reductase in Escherichia coli . . J Bacteriol 95:, 1305–1313.[PubMed]
    [Google Scholar]
  74. Smith M. S. . ( 1983; ). Nitrous oxide production by Escherichia coli is correlated with nitrate reductase activity. . Appl Environ Microbiol 45:, 1545–1547.[PubMed]
    [Google Scholar]
  75. Spiro S. , Guest J. R. . ( 1990; ). FNR and its role in oxygen-regulated gene expression in Escherichia coli . . FEMS Microbiol Rev 6:, 399–428. [CrossRef] [PubMed]
    [Google Scholar]
  76. Squire D. J. P. , Xu M. , Cole J. A. , Busby S. J. W. , Browning D. F. . ( 2009; ). Competition between NarL-dependent activation and Fis-dependent repression controls expression from the Escherichia coli yeaR and ogt promoters. . Biochem J 420:, 249–257. [CrossRef] [PubMed]
    [Google Scholar]
  77. Stevanin T. M. , Ioannidis N. , Mills C. E. , Kim S. O. , Hughes M. N. , Poole R. K. . ( 2000; ). Flavohemoglobin Hmp affords inducible protection for Escherichia coli respiration, catalyzed by cytochromes bo′ or bd, from nitric oxide. . J Biol Chem 275:, 35868–35875. [CrossRef] [PubMed]
    [Google Scholar]
  78. Stevanin T. M. , Poole R. K. , Demoncheaux E. A. , Read R. C. . ( 2002; ). Flavohemoglobin Hmp protects Salmonella enterica serovar Typhimurium from nitric oxide-related killing by human macrophages. . Infect Immun 70:, 4399–4405. [CrossRef] [PubMed]
    [Google Scholar]
  79. Stewart V. . ( 1982; ). Requirement of Fnr and NarL functions for nitrate reductase expression in Escherichia coli K-12. . J Bacteriol 151:, 1320–1325.[PubMed]
    [Google Scholar]
  80. Stewart V. . ( 1993; ). Nitrate regulation of anaerobic respiratory gene expression in Escherichia coli . . Mol Microbiol 9:, 425–434. [CrossRef] [PubMed]
    [Google Scholar]
  81. Svensson L. , Poljakovic M. , Säve S. , Gilberthorpe N. , Schön T. , Strid S. , Corker H. , Poole R. K. , Persson K. . ( 2010; ). Role of flavohemoglobin in combating nitrosative stress in uropathogenic Escherichia coli–implications for urinary tract infection. . Microb Pathog 49:, 59–66. [CrossRef] [PubMed]
    [Google Scholar]
  82. Thöny-Meyer L. , Beck C. , Preisig O. , Hennecke H. . ( 1994; ). The ccoNOQP gene cluster codes for a cb-type cytochrome oxidase that functions in aerobic respiration of Rhodobacter capsulatus . . Mol Microbiol 14:, 705–716. [CrossRef] [PubMed]
    [Google Scholar]
  83. Todorovic S. , Justino M. C. , Wellenreuther G. , Hildebrandt P. , Murgida D. H. , Meyer-Klaucke W. , Saraiva L. M. . ( 2008; ). Iron-sulfur repair YtfE protein from Escherichia coli: structural characterization of the di-iron center. . J Biol Inorg Chem 13:, 765–770. [CrossRef] [PubMed]
    [Google Scholar]
  84. Tovell N. . ( 2008; ). The role and regulation of the c-type cytochrome complement of Neisseria gonorrhoeae. PhD thesis, University of Birmingham, Birmingham, UK..
  85. Tucker N. P. , Hicks M. G. , Clarke T. A. , Crack J. C. , Chandra G. , Le Brun N. E. , Dixon R. , Hutchings M. I. . ( 2008; ). The transcriptional repressor protein NsrR senses nitric oxide directly via a [2Fe-2S] cluster. . PLoS ONE 3:, e3623. [CrossRef] [PubMed]
    [Google Scholar]
  86. Turner S. , Reid E. , Smith H. , Cole J. . ( 2003; ). A novel cytochrome c peroxidase from Neisseria gonorrhoeae: a lipoprotein from a Gram-negative bacterium. . Biochem J 373:, 865–873. [CrossRef] [PubMed]
    [Google Scholar]
  87. Turner S. M. , Moir J. W. B. , Griffiths L. , Overton T. W. , Smith H. , Cole J. A. . ( 2005; ). Mutational and biochemical analysis of cytochrome c′, a nitric oxide-binding lipoprotein important for adaptation of Neisseria gonorrhoeae to oxygen-limited growth. . Biochem J 388:, 545–553. [CrossRef] [PubMed]
    [Google Scholar]
  88. van den Berg W. A. M. , Hagen W. R. , van Dongen W. M. A. M. . ( 2000; ). The hybrid-cluster (“prismane protein”) from Escherichia coli. Characterization of the hybrid-cluster protein, redox properties of the [2Fe-2S] and [4Fe-2S-2O] clusters and identification of an associated NADH oxidoreductase containing FAD and [2Fe-2S]. . Eur J Biochem 267:, 666–676. [CrossRef] [PubMed]
    [Google Scholar]
  89. van Wonderen J. H. , Burlat B. , Richardson D. J. , Cheesman M. R. , Butt J. N. . ( 2008; ). The nitric oxide reductase activity of cytochrome c nitrite reductase from Escherichia coli . . J Biol Chem 283:, 9587–9594. [CrossRef] [PubMed]
    [Google Scholar]
  90. Vine C. E. , Cole J. A. . ( 2011a; ). Nitrosative stress in Escherichia coli: reduction of nitric oxide. . Biochem Soc Trans 39:, 213–215. [CrossRef] [PubMed]
    [Google Scholar]
  91. Vine C. E. , Cole J. A. . ( 2011b; ). Unresolved sources, sinks, and pathways for the recovery of enteric bacteria from nitrosative stress. . FEMS Microbiol Lett 325:, 99–107. [CrossRef] [PubMed]
    [Google Scholar]
  92. Vine C. E. , Justino M. C. , Saraiva L. , Cole J. A. . ( 2010; ). Detection by whole genome microarrays of a spontaneous 126-gene deletion during construction of a ytfE mutant: confirmation that a ytfE mutation results in loss of repair of iron-sulfur centres in proteins damaged by oxidative or nitrosative stress. . J Microbiol Methods 81:, 77–79. [CrossRef] [PubMed]
    [Google Scholar]
  93. Vine C. E. , Purewal S. K. , Cole J. A. . ( 2011; ). NsrR-dependent method for detecting nitric oxide accumulation in the Escherichia coli cytoplasm and enzymes involved in NO production. . FEMS Microbiol Lett 325:, 108–114. [CrossRef] [PubMed]
    [Google Scholar]
  94. Wang H. , Gunsalus R. P. . ( 2000; ). The nrfA and nirB nitrite reductase operons in Escherichia coli are expressed differently in response to nitrate than to nitrite. . J Bacteriol 182:, 5813–5822. [CrossRef] [PubMed]
    [Google Scholar]
  95. Ward M. E. , Watt P. J. , Glynn A. A. . ( 1970; ). Gonococci in urethral exudates possess a virulence factor lost on subculture. . Nature 227:, 382–384. [CrossRef] [PubMed]
    [Google Scholar]
  96. Weiss B. . ( 2006; ). Evidence for mutagenesis by nitric oxide during nitrate metabolism in Escherichia coli . . J Bacteriol 188:, 829–833. [CrossRef] [PubMed]
    [Google Scholar]
  97. Whitehead R. N. , Overton T. W. , Snyder L. A. S. , McGowan S. J. , Smith H. , Cole J. A. , Saunders N. J. . ( 2007; ). The small FNR regulon of Neisseria gonorrhoeae: comparison with the larger Escherichia coli FNR regulon and interaction with the NarQ-NarP regulon. . BMC Genomics 8:, 35. [CrossRef] [PubMed]
    [Google Scholar]
  98. Wolfe M. T. , Heo J. , Garavelli J. S. , Ludden P. W. . ( 2002; ). Hydroxylamine reductase activity of the hybrid cluster protein from Escherichia coli . . J Bacteriol 184:, 5898–5902. [CrossRef] [PubMed]
    [Google Scholar]
  99. Zumft W. G. . ( 1997; ). Cell biology and molecular basis of denitrification. . Microbiol Mol Biol Rev 61:, 533–616.[PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.059048-0
Loading
/content/journal/micro/10.1099/mic.0.059048-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error