The oxidative and nitrosative stress defence network of Wolinella succinogenes: Cytochrome c nitrite reductase mediates the stress response to nitrite, nitric oxide, hydroxylamine and hydrogen peroxide

Environmental Microbiology

Volumn 13, Issue 9, 2011, Pages 2478-2494

  Kern, Melanie ^a   Volz, Jennifer ^a   Simon, Jörg ^a  

^a DARMSTADT UNIVERSITY OF TECHNOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME A1; CYTOCHROME C; CYTOCHROME C1; HYDROGEN PEROXIDE; HYDROXYLAMINE; ISOENZYME; NITRATE; NITRATE REDUCTASE; NITRATE REDUCTASE (CYTOCHROME); NITRIC OXIDE; NITRIC OXIDE DONOR; NITRITE;

ARTICLE; CYTOPLASM; ENZYMOLOGY; GENETICS; INDEL MUTATION; METABOLISM; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; WOLINELLA;

CYTOCHROMES A1; CYTOCHROMES C; CYTOCHROMES C1; CYTOPLASM; HYDROGEN PEROXIDE; HYDROXYLAMINE; INDEL MUTATION; ISOENZYMES; NITRATE REDUCTASES; NITRATES; NITRIC OXIDE; NITRIC OXIDE DONORS; NITRITES; OXIDATION-REDUCTION; OXIDATIVE STRESS; PERIPLASM; WOLINELLA;

EPSILONPROTEOBACTERIA; WOLINELLA SUCCINOGENES;

EID: 80052636384     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2011.02520.x     Document Type: Article

References (58)

1. Almeida, C.C., Romao, C.V., Lindley, P.F., Teixeira, M., and Saraiva, L.M. (2006) The role of the hybrid cluster protein in oxidative stress defense. J Biol Chem 281: 32445-32450.
2. Atack, J.M., and Kelly, D.J. (2007) Structure, mechanism and physiological roles of bacterial cytochrome c peroxidases. Adv Microb Physiol 52: 73-106.
3. Atack, J.M., and Kelly, D.J. (2008) Contribution of the stereospecific methionine sulphoxide reductases MsrA and MsrB to oxidative and nitrosative stress resistance in the food-borne pathogen Campylobacter jejuni. Microbiology 154: 2219-2230.
4. Atack, J.M., and Kelly, D.J. (2009) Oxidative stress in Campylobacter jejuni: responses, resistance and regulation. Future Microbiol 4: 677-690.
5. Atack, J.M., Harvey, P., Jones, M.A., and Kelly, D.J. (2008) The Campylobacter jejuni thiol peroxidases Tpx and Bcp both contribute to aerotolerance and peroxide-mediated stress resistance but have distinct substrate specificities. J Bacteriol 190: 5279-5290.
6. Baar, C., Eppinger, M., Raddatz, G., Simon, J., Lanz, C., Klimmek, O., etal. (2003) Complete genome sequenceand analysis of Wolinella succinogenes. Proc Natl Acad Sci USA 100: 11690-11695.
7. Baillon, M.-L.A., van Vliet, A.H.M., Ketley, J.M., Constantinidou, C., and Penn, C.W. (1999) An iron-regulated alkyl hydroperoxide reductase (AhpC) confers aerotolerance and oxidative stress resistance to the microaerophilic pathogen Campylobacter jejuni. J Bacteriol 181: 4798-4804.
8. Baker, L.M.S., Raudonikiene, A., Hoffman, P.S., and Poole, L.B. (2001) Essential thioredoxin-dependent peroxiredoxin system from Helicobacter pylori: genetic and kinetic characterization. J Bacteriol 183: 1961-1973.
9. Bingham-Ramos, L.K., and Hendrixson, D.R. (2008) Characterization of two putative cytochrome c peroxidises of Campylobacter jejuni involved in promoting commensal colonization of poultry. Infect Immun 76: 1105-1114.
10. Bode, C., Goebell, H., and Stähler, E. (1968) Zur Eliminierung von Trübungsfehlern bei der Eiweißbestimmung mit der Biuretmethode. Z Klin Chem Klin Biochem 6: 418-422.
11. Bykov, D., and Neese, F. (2011) Substrate binding and activation in the active site of cytochrome c nitrite reductase: a density functional study. J Biol Inorg Chem 16: 417-430.
12. Cabello, P., Pino, C., Olmo-Mira, M.F., Castillo, F., Roldan, M.D., and Moreno-Vivian, C. (2004) Hydroxylamine assimilation by Rhodobacter capsulatus E1F1. J Biol Chem 279: 45485-45494.
13. Campbell, B.J., Engel, A.S., Porter, M.L., and Takai, K. (2006) The versatile epsilon-proteobacteria: key players in sulphidic habitats. Nat Rev Microbiol 4: 458-468.
14. Comtois, S.L., Gidley, M.D., and Kelly, D.J. (2003) Role of the thioredoxin system and the thiol-peroxidases Tpx and Bcp in mediating resistance to oxidative and nitrosative stress in Helicobacter pylori. Microbiology 149: 121-129.
15. Cunha, C.A., Macieira, S., Dias, J.M., Almeida, G., Goncalves, L.L., Costa, C., etal. (2003) Cytochrome c nitrite reductase from Desulfovibrio desulfuricans ATCC 27774. J Biol Chem 278: 17455-17465.
16. Deepa, B., Balasubramanian, N., and Nagaraja, K.S. (2004) Spectrophotometric determination of hydroxylamine and its derivatives in pharmaceuticals. Chem Pharm Bull 52: 1473-1475.
17. Einsle, O., Messerschmidt, A., Huber, R., Kroneck, P.M.H., and Neese, F. (2002) Mechanism of the six-electron reduction of nitrite to ammonia by cytochrome c nitrite reductase. J Am Chem Soc 124: 11737-11745.
18. Elvers, K.T., Wu, G., Gilberthorpe, N.J., Poole, R.K., and Park, S.F. (2004) Role of an inducible single-domain hemoglobin in mediating resistance to nitric oxide and nitrosative stress in Campylobacter jejuni and Campylobacter coli. J Bacteriol 186: 5332-5341.
19. Fang, F.C. (2004) Antimicrobial reactive oxygen and nitrogen species: concepts and controversies. Nat Rev Microbiol 2: 820-832.
20. Imlay, J.A. (2006) Iron-sulphur clusters and the problem with oxygen. Mol Microbiol 59: 1073-1082.
21. Imlay, J.A. (2008) Cellular defences against superoxide and hydrogen peroxide. Annu Rev Biochem 77: 755-776.
22. Iovine, N.M., Pursnani, S., Voldman, A., Wasserman, G., Blaser, M.J., and Weinrauch, Y. (2008) Reactive nitrogen species contribute to innate host defence against Campylobacter jejuni. Infect Immun 76: 986-993.
23. Kern, M., and Simon, J. (2009a) Electron transport chains and bioenergetics of respiratory nitrogen metabolism in Wolinella succinogenes and other Epsilonproteobacteria. Biochim Biophys Acta 1787: 646-656.
24. Kern, M., and Simon, J. (2009b) Periplasmic nitrate reduction in Wolinella succinogenes: cytoplasmic NapF facilitates NapA maturation and requires the menaquinol dehydrogenase NapH for membrane attachment. Microbiology 155: 2784-2794.
25. Kern, M., and Simon, J. (2011) Production of recombinant multiheme cytochromes c in Wolinella succinogenes. Meth Enzymol 486: 429-446.
26. Kern, M., Eisel, F., Scheithauer, J., Kranz, R.G., and Simon, J. (2010) Substrate specificity of three cytochrome c haem lyase isoenzymes from Wolinella succinogenes: unconventional haem c binding motifs are not sufficient for haem c attachment by NrfI and CcsA1. Mol Microbiol 75: 122-137.
27. Kern, M., Winkler, C., and Simon, J. (2011) Respiratory nitrogen metabolism and nitrosative stress defence in ε-proteobacteria: the role of NssR-type transcription regulators. Biochem Soc Trans 39: 299-302.
28. Klimmek, O., Dietrich, W., Dancea, F., Lin, Y.-J., Pfeiffer, S., Löhr, F., etal. (2004) Sulfur respiration. In Respiration in Bacteria and Archaea. Zannoni, D. (ed.). Dordrecht, the Netherlands: Springer, pp. 217-232.
29. Kröger, A., Geisler, V., and Duchêne, A. (1994) Isolation of Wolinella succinogenes hydrogenase, Chromatofocusing. In A Practical Guide to Membrane Protein Purification. von Jagow, G., and Schägger, H. (eds). London, UK: Academic Press, pp. 141-147.
30. Kröger, A., Biel, S., Simon, J., Gross, R., Unden, G., and Lancaster, C.R.D. (2002) Fumarate respiration of Wolinella succinogenes: enzymology, energetics and coupling mechanism. Biochim Biophys Acta 1553: 23-38.
31. Lorenzen, J.P., Kröger, A., and Unden, G. (1993) Regulation of anaerobic respiratory pathways in Wolinella succinogenes by the presence of electron acceptors. Arch Microbiol 159: 477-483.
32. Mills, P.C., Rowley, G., Spiro, S., Hinton, J.C.D., and Richardson, D.J. (2008) A combination of cytochrome c nitrite reductase (NrfA) and flavorubredoxin (NorV) protects Salmonella enterica serovar Typhimurium against killing by NO in anoxic environments. Microbiology 154: 1218-1228.
33. Nathan, C., and Shiloh, M.U. (2000) Reactive oxygen and nitrogen intermediates in the relationship between mammalian hosts and microbial pathogens. Proc Natl Acad Sci USA 97: 8841-8848.
34. Pittman, M.S., Elvers, K.T., Lee, L., Jones, M.A., Poole, R.K., Park, S.F., and Kelly, D.J. (2007) Growth of Campylobacter jejuni on nitrate and nitrite: electron transport to NapA and NrfA via NrfH and distinct roles for NrfA and the globin Cgb in protection against nitrosative stress. Mol Microbiol 63: 575-590.
35. Poock, S.R., Leach, E.R., Moir, J.W.B., Cole, J.A., and Richardson, D.J. (2002) Respiratory detoxification of nitric oxide by the cytochrome c nitrite reductase of Escherichia coli. J Biol Chem 277: 23664-23669.
36. Poole, R.K. (2005) Nitric oxide and nitrosative stress tolerance in bacteria. Biochem Soc Trans 33: 176-180.
37. Poole, R.K., and Hughes, M.N. (2000) New functions for the ancient globin family: bacterial responses to nitric oxide and nitrosative stress. Mol Microbiol 36: 775-783.
38. r thioredoxin reductase. Eur J Biochem 267: 6126-6133.
39. Qu, W., Zhou, Y., Shao, C., Sun, Y., Zhang, Q., Chen, C., and Jia, J. (2009) Helicobacter pylori proteins response to nitric oxide stress. J Microbiol 47: 486-493.
40. Rider, B.F., and Mellon, B.G. (1946) Colorimetric determination of nitrite. Indust Eng Chem 18: 96-98.
41. Rodrigues, R., Vicente, J.B., Félix, R., Oliveira, S., Teixeira, M., and Rodrigues-Pousada, C. (2006) Desulfovibrio gigas flavodiiron protein affords protection against nitrosative stress in vivo. J Bacteriol 188: 2745-2751.
42. Rudolf, M., Einsle, O., Neese, F., and Kroneck, P.M.H. (2002) Pentahaem cytochrome c nitrite reductase: reaction with hydroxylamine, a potential reaction intermediate and substrate. Biochem Soc Trans 30: 649-653.
43. Saraiva, L.M., Vicente, J.B., and Teixeira, M. (2004) The role of flavodiiron proteins in microbial nitric oxide detoxification. Adv Microb Phys 49: 77-129.
44. Seaver, L.C., and Imlay, J.A. (2004) Are respiratory enzymes the primary sources of intracellular hydrogen peroxide? J Biol Chem 279: 48742-48750.
45. Simon, J. (2002) Enzymology and bioenergetics of respiratory nitrite ammonification. FEMS Microbiol Rev 26: 285-309.
46. Simon, J., Gross, R., Ringel, M., Schmidt, E., and Kröger, A. (1998) Deletion and site-directed mutagenesis of the Wolinella succinogenes fumarate reductase operon. Eur J Biochem 251: 418-426.
47. Simon, J., Gross, R., Einsle, O., Kroneck, P.M.H., Kröger, A., and Klimmek, O. (2000) A NapC/NirT-type cytochrome c (NrfH) is the mediator between the quinone pool and the cytochrome c nitrite reductase of Wolinella succinogenes. Mol Microbiol 35: 686-696.
48. Simon, J., Pisa, R., Stein, T., Eichler, R., Klimmek, O., and Gross, R. (2001) The tetraheme cytochrome c NrfH is required to anchor the cytochrome c nitrite reductase in the membrane of Wolinella succinogenes. Eur J Biochem 268: 5776-5782.
49. Simon, J., Sänger, M., Schuster, S.C., and Gross, R. (2003) Electron transport to periplasmic nitrate reductase (NapA) of Wolinella succinogenes is independent of a NapC protein. Mol Microbiol 49: 69-79.
50. Simon, J., Einsle, O., Kroneck, P.M.H., and Zumft, W.G. (2004) The unprecedented nos gene cluster of Wolinella succinogenes encodes a novel respiratory electron transfer pathway to cytochrome c nitrous oxide reductase. FEBS Lett 569: 7-12.
51. Stach, P., Einsle, O., Schumacher, W., Kurun, E., and Kroneck, P.M.H. (2000) Bacterial cytochrome c nitrite reductase: new structural and functional aspects. J Inorg Biochem 79: 381-385.
52. Tikhonova, T.V., Slutsky, A., Antipov, A.N., Boyko, K.M., Polyakov, K.M., Sorokin, D.Y., etal. (2006) Molecular and catalytic properties of a novel cytochrome c nitrite reductase from nitrate-reducing haloalkaliphilic sulfur-oxidizing bacterium Thioalkalivibrio nitratireducens. Biochim Biophys Acta 1764: 715-723.
53. Wang, G., Alamuri, P., and Maier, R.J. (2006) The diverse oxidant systems of Helicobacter pylori. Mol Microbiol 61: 847-860.
54. Wolfe, M.T., Heo, J., Garavelli, J.S., and Ludden, P.W. (2002) Hydroxylamine reductase activity oft he hybrid cluster protein from Escherichia coli. J Bacteriol 184: 5898-5902.
55. van Wonderen, J.H., Burlat, B., Richardson, D.J., Cheesman, M.R., and Butt, J.N. (2008) The nitric oxide reductase activity of cytochrome c nitrite reductase from Escherichia coli. J Biol Chem 283: 9587-9594.
56. Wood, Z.A., Schröder, E., Harris, J.R., and Poole, L.B. (2003) Structure, mechanism and regulation of peroxiredoxins. Trends Biochem Sci 28: 32-40.
57. Yamasaki, M., Igimi, S., Katayama, Y., Yamamoto, S., and Amano, F. (2004) Identification of an oxidative stress-sensitive protein from Campylobacter jejuni, homologous to rubredoxin oxidoreductase/rubrerythrin. FEMS Microbiol Lett 235: 57-63.
58. 2O reduction by Vibrio succinogenes. Appl Environ Microbiol 39: 81-84.