Legless pathogens: How bacterial physiology provides the key to understanding pathogenicity

Microbiology (United Kingdom)

Volumn 158, Issue 6, 2012, Pages 1402-1413

  Cole, Jeffrey A ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMMONIA; BACTERIAL PROTEIN; CYTOCHROME C OXIDASE; HEME; LACTIC ACID; LIPOPOLYSACCHARIDE; NARL PROTEIN; NARP PROTEIN; NARQ PROTEIN; NARX PROTEIN; NITRATE; NITRIC OXIDE; NITRITE REDUCTASE; OXYGEN; SIALYLTRANSFERASE; UNCLASSIFIED DRUG;

ANAEROBIC FERMENTATION; ARTICLE; BACTERIAL GROWTH; BACTERIAL METABOLISM; BACTERIAL PHENOMENA AND FUNCTIONS; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; BACTERIUM; BACTERIUM CULTURE; BACTERIUM ISOLATE; BLOOD FLOW; CARBOXY TERMINAL SEQUENCE; DNA DAMAGE; DNA REPAIR; ELECTRON; ENTEROBACTERIACEAE; ESCHERICHIA COLI; HOST; HOST RESISTANCE; HUMAN; MOLECULAR MIMICRY; NEISSERIA GONORRHOEAE; NITROSATIVE STRESS; OXIDATIVE STRESS; OXYGEN STARVATION; PATHOGENESIS; PRIORITY JOURNAL; RESPIRATORY BURST; SIALYLATION; SIGNAL TRANSDUCTION; STARVATION; THERMODYNAMICS;

ANIMALS; BACTERIAL PROTEINS; ESCHERICHIA COLI; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; NEISSERIA GONORRHOEAE;

BACTERIA (MICROORGANISMS); ENTEROBACTERIACEAE; ESCHERICHIA COLI; NEISSERIA GONORRHOEAE;

EID: 84861904133     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.059048-0     Document Type: Article

References (99)

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.
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.
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.
4. Arendsen, A., Hadden, J., Card, G., McAlpine, A. S., Bailey, S., Zaitsev, V., Duke, E. H. M., Lindley, P., Krösckel, M. & other authors (1998). The "prismane" protein resolved: Xray structure at 1.7 A ° and multiple spectroscopy of two novel 4Fe clusters. J Biol Inorg Chem 3, 81-95.
5. Aspholm, M., Aas, F. E., Harrison, O. B., Quinn, D., Vik, A°., 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.
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.
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.
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.
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.
10. Browning, D. F., Lee, D. J., Spiro, S. & Busby, S. J. W. (2010). Downregulation 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.
11. Butlin, K. R. & Postgate, J. R. (1953). Microbial formation of sulphide and sulphur. Microbial Metabolism, Symp 6th Congr int Microbiol p. 126.
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.
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.
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.
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.
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.
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.
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.
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.
20. D'Autréaux, B., Tucker, N. P., Dixon, R. & Spiro, S. (2005). A nonhaem iron centre in the transcription factor NorR senses nitric oxide. Nature 437, 769-772.
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.
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.
23. 54in the nitric oxide stress response. J Biol Chem 278, 10081-10086.
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.
25. Gomes, C. M., Giuffré, 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.
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.
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.
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.
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.
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.
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.
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.
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.
34. 2-dependent chemical nitrosation. Appl Environ Microbiol 54, 1791-1794.
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.
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.
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.
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.
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. & other authors (2011). Molecular mechanism of anaerobic ammonium oxidation. Nature 479, 127-130.
40. 2: [4Fe-4S] to [2Fe-2S] conversion with loss of biological activity. Proc Natl Acad Sci U S A 94, 6087-6092.
41. Knapp, J. S. & Clark, V. L. (1984). Anaerobic growth of Neisseria gonorrhoeae coupled to nitrite reduction. Infect Immun 46, 176-181.
42. 2, in oxygen reduction. J Bacteriol 192, 2395-2406.
43. Lin, H.-Y., Bledsoe, P. J. & Stewart, V. (2007). Activation of yeaRyoaG 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.
44. Lissenden, S., Mohan, S., Overton, T., Regan, T., Crooke, H., Cardinale, J. A., Householder, T. C., Adams, P., O'Conner, C. D. & other authors (2000). Identification of transcription activators that regulate gonococcal adaptation from aerobic to anaerobic or oxygenlimited growth. Mol Microbiol 37, 839-855.
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.
46. 2regulatory cascade. J Bacteriol 185, 3978-3982.
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.
48. Morse, S. A. (1979). The biology of the gonococcus. Crit Rev Microbiol 7, 93-189.
49. Morse, S. A. & Bartenstein, L. (1974). Factors affecting autolysis of Neisseria gonorrhoeae. Proc Soc Exp Biol Med 145, 1418-1421.
50. rfactor from human red blood cells which induces gonococcal resistance to killing by human serum. J Gen Microbiol 134, 3295-3306.
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.
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 oxidesensitive repressor, NsrR, and nitrite-insensitive NarQ-NarP. J Biol Chem 281, 33115-33126.
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.
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.
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 59-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.
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.
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.
58. 3oxidases. Biochim Biophys Acta 1655, 388-399.
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.
60. Poole, R. K., Anjum, M. F., Membrillo-Herná ndez, 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.
61. 3and desulphoviridin; pigments of the anaerobe Desulphovibrio desulphuricans. J Gen Microbiol 14, 545-572.
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.
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.
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.
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.
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.
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.
68. 2fixation. J Bacteriol 179, 7191-7196.
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.
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.
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.
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.
73. Showe, M. K. & DeMoss, J. A. (1968). Localization and regulation of synthesis of nitrate reductase in Escherichia coli. J Bacteriol 95, 1305-1313.
74. Smith, M. S. (1983). Nitrous oxide production by Escherichia coli is correlated with nitrate reductase activity. Appl Environ Microbiol 45, 1545-1547.
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.
76. Squire, D. J. P., Xu, M., Cole, J. A., Busby, S. J. W. & Browning, D. F. (2009). Competition between NarL-dependent activation and Fisdependent repression controls expression from the Escherichia coli yeaR and ogt promoters. Biochem J 420, 249-257.
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 bo9 or bd, from nitric oxide. J Biol Chem 275, 35868-35875.
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.
79. Stewart, V. (1982). Requirement of Fnr and NarL functions for nitrate reductase expression in Escherichia coli K-12. J Bacteriol 151, 1320-1325.
80. Stewart, V. (1993). Nitrate regulation of anaerobic respiratory gene expression in Escherichia coli. Mol Microbiol 9, 425-434.
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.
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.
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.
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.
86. Turner, S., Reid, E., Smith, H. & Cole, J. (2003). A novel cytochrome c peroxidase from Neisseria gonorrhoeae: a lipoprotein from a Gramnegative bacterium. Biochem J 373, 865-873.
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 c9, a nitric oxide-binding lipoprotein important for adaptation of Neisseria gonorrhoeae to oxygen-limited growth. Biochem J 388, 545-553.
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.
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.
90. Vine, C. E. & Cole, J. A. (2011a). Nitrosative stress in Escherichia coli: reduction of nitric oxide. Biochem Soc Trans 39, 213-215.
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.
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.
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.
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.
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.
96. Weiss, B. (2006). Evidence for mutagenesis by nitric oxide during nitrate metabolism in Escherichia coli. J Bacteriol 188, 829-833.
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.
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.
99. Zumft, W. G. (1997). Cell biology and molecular basis of denitrification. Microbiol Mol Biol Rev 61, 533-616.