A truncated haemoglobin implicated in oxygen metabolism by the microaerophilic food-borne pathogen Campylobacter jejuni

Microbiology

Volumn 151, Issue 12, 2005, Pages 4079-4091

  Wainwright, Laura M ^a   Elvers, Karen T ^b   Park, Simon F ^b   Poole, Robert K ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b UNIVERSITY OF SURREY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

HEMOGLOBIN; OXIDOREDUCTASE; PARAQUAT; S NITROSOGLUTATHIONE;

AERATION; ARTICLE; BACTERIAL CELL; BACTERIUM MUTANT; BINDING AFFINITY; CALCULATION; CAMPYLOBACTER JEJUNI; CELL GROWTH; CONTROLLED STUDY; CULTURE MEDIUM; ENZYME KINETICS; GENE MUTATION; GENETIC CODE; NONHUMAN; OXIDATIVE STRESS; OXYGEN CONSUMPTION; OXYGEN SUPPLY; OXYGEN TRANSPORT; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; UPREGULATION; WILD TYPE;

CAMPYLOBACTER JEJUNI; FOOD MICROBIOLOGY; GENE DELETION; HEMOGLOBINS; NITRIC OXIDE; OXYGEN;

BACTERIA (MICROORGANISMS); CAMPYLOBACTER JEJUNI;

EID: 29244484463     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.28266-0     Document Type: Article

References (53)

1. Appleby, C. A. & Bergersen, F. J. (1980). Preparation and experimental use of leghaemoglobin. In Methods of Evaluating Biological Nitrogen Fixation, pp. 315-335. Edited by F. J. Bergerson. Chichester: Wiley.
2. Baillon, M. L., van Vliet, A. H., Ketley, J. M., Constantinidou, C. & Penn, C. W. (1999b). An iron-regulated alkyl hydroperoxide reductase (AhpC) confers aerotolerance and oxidative stress resistance to the microaerophilic pathogen Campylobacter jejuni. J Bacteriol 181, 4798-4804.
3. 2 in and near symbiosomes and beneath intracellular spaces. Protoplasma 191, 9-20.
4. Bergerson, F. J. & Turner, G. L. (1979). Systems utilizing oxygenated leghemoglobin and myoglobin as sources of free dissolved oxygen at low concentrations for experiments with bacteria. Anal Biochem 96, 165-174.
5. 3 mutant has a very high affinity for oxygen. Microbiology 145, 1563-1573.
6. Cooper, C. E. (1999). Nitric oxide and iron proteins. Biochim Biophys Acta 1411, 290-309.
7. 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.
8. Dickinson, J. H., Grant K A. & Park, S. F. (1995). Targeted and random mutagenesis of the Campylobacter coli chromosome with integrational plasmid vectors. Curr Microbiol 31, 92-96.
9. Dikshit, K. L., Spaulding, D., Braun, A. & Webster, D. A. (1989). Oxygen inhibition of globin gene transcription and bacterial haemoglobin synthesis in Vitreoscilla. J Gen Microbiol 135, 2601-2609.
10. D'Mello, R., Hill, S. & Poole, R. K. (1994). Determination of the oxygen affinities of terminal oxidases in Azotobacter vinelandii using the deoxygenation of oxyleghaemoglobin and oxymyoglobin: cytochrome bd is a low affinity oxidase. Microbiology 140, 1395-1402.
11. m values for oxygen are in the submicromolar range. J Bacteriol 177, 867-870.
12. D'Mello, R., Hill, S. & Poole, R. K (1996). The cytochrome bd quinol oxidase in Escherichia coli has an extremely high oxygen affinity and two oxygen-binding haems: implications for regulation of activity in vivo by oxygen inhibition. Microbiology 142, 755-763.
13. Dowd, J. E. & Riggs, D. S. (1965). A comparison of estimates of Michaelis-Menten kinetic constants from various linear transformations. J Biol Chem 240, 863-869.
14. Duncan, C., Dougall, H., Johnston, P., Green, S., Brogan, R., Leifert, C., Smith, L., Golden, M. & Benjamin, N. (1995). Chemical generation of nitric oxide in the mouth from the enterosalivary circulation of dietary nitrate. Nat Med 1, 546-551.
15. Elvers, K. T., Wu, G., Gilberthorpe, N. J., Poole, R. K. & 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.
16. Elvers, K T., Turner, S. M., Penn, C. W., Wainwright, L. M., Poole, R. K. & Park, S. F. (2005). NssR, a member of the Crp-Fnr superfamily from Campylobacter jejuni, regulates a nitrosative stress-responsive regulon that includes both a single-domain and a truncated haemoglobin. Mol Microbiol 57, 735-750.
17. Forte, P., Dykhuizen, R. S., Milne, E., McKenzie, A., Smith, C. C. & Benjamin, N. (1999). Nitric oxide synthesis in patients with infective gastroenteritis. Gut 45, 355-361.
18. Gaynor, E. C., Cawthraw, S., Manning, G., MacKichan, J. K., Falkow, S. & Newell, D. G. (2004). The genome-sequenced variant of Campylobacter jejuni NCTC11168 and the original clonal isolate differ markedly in colonisation, gene expression and virulence associated phenotypes. J Bacteriol 186, 503-517.
19. Hadden, R. D. & Gregson, N. A. (2001). Guillain-Barre syndrome and Campylobacter jejuni infection. Symp Ser Soc Appl Microbiol 145S-154S.
20. Hazeleger, W. C., Wouters, J. A., Rombouts, F. M. & Abee, T. (1998). Physiological activity of Campylobacter jejuni far below the minimal growth temperature. Appl Environ Microbiol 64, 3917-3922.
21. Hickey, T. E., McVeigh, A. L., Scott, D. A., Michielutti, R. E., Bixby, A., Carroll, S. A., Bourgeois, A. L. & Guerry, P. (2000). Campylobacter jejuni cytolethal distending toxin mediates the release of interleukin-8 from intestinal epithelial cells. Infect Immun 68, 6535-6541.
22. Hoffman, P. S., Krieg, N. R. & Smibert, R. M. (1979a). Studies of the microaerophilic nature of Campylobacter fetus subsp. jejuni. I. Physiological aspects of enhanced aerotolerance. Can J Microbiol 25, 1-7.
23. Hoffman, P. S., George, H. A., Krieg, N. R. & Smibert, R. M. (1979b). Studies of the microaerophilic nature of Campylobacter fetus subsp. jejuni. II. Role of exogenous superoxide anions and hydrogen peroxide. Can J Microbiol 25, 8-16.
24. Imlay, J. A. (1995). A metabolic enzyme that rapidly produces superoxide, fumarate reductase of Escherichia coli. J Biol Chem 270, 19767-19777.
25. Inoue, H., Nojima, N. & Okayama, H. (1990). High efficiency transformation of Escherichia coli with plasmids. Gene 96, 23-28.
26. Kalnenieks, U., Galinina, N., Bringer-Meyer, S. & Poole, R. K. (1998). Membrane D-lactate oxidase in Zymomonas mobilis: evidence for a branched respiratory chain. FEMS Microbiol Left 168, 91-97.
27. Kelly, M. J. S., Poole, R. K., Yates, M. G. & Kennedy, C. (1990). Cloning and mutagenesis of genes encoding the cytochrome-bd terminal oxidase complex in Azotobacter vinelandii: mutants deficient in the cytochrome d complex are unable to fix nitrogen in air. J Bacteriol 172, 6010-6019.
28. Ketley, J. M. (1997). Pathogenesis of enteric infection by Campylobacter. Microbiology 143, 5-21.
29. Khosla, C. & Bailey, J. E. (1988). Heterologous expression of a bacterial haemoglobin improves the growth properties of recombinant Escherichia coli. Nature 331, 633-635.
30. Khosla, C. & Bailey, J. E. (1989). Evidence for partial export of Vitreoscilla hemoglobin into the periplasmic space in Escherichia coli. J Mol Biol 210, 79-89.
31. Krieg, N. R. & Hoffman, P. S. (1986). Microaerophily and oxygen toxicity. Annu Rev Microbiol 40, 107-130.
32. Li, H., Duncan, C., Townend, J. & 8 other authors (1997). Nitrate-reducing bacteria on rat tongues. Appl Environ Microbiol 63, 924-930.
33. Li, J., Huang, F. L. & Huang, K.-P. (2001). Glutathiolation of proteins by glutathione disulfide-S-oxide derived from S-nitrosoglutathione. J Biol Chem 276, 3098-3105.
34. Liu, C., He, Y. & Chang, Z. (2004). Truncated hemoglobin O of Mycobacterium tuberculosis: the oligomeric state change and the interaction with membrane components. Biochem Biophys Res Commun 316, 1163-1172.
35. Lundsgaard, J. S., Gronlund, J. & Degn, H. (1978). Error in oxygen measurements in open systems owing to oxygen consumption in the unstirred layer. Biotechnol Bioeng 20, 809-819.
36. Membrillo-Hernández, J., Ioannidis, N. & Poole, R. K. (1996). The flavohaemoglobin (HMP) of Escherichia coli generates superoxide in vitro and causes oxidative stress in vivo. FEBS Lett 382, 141-144.
37. Membrillo-Hernández, J., Coopamah, M. D., Anjum, M. F., Stevanin, T. M., Kelly, A., Hughes, M. N. & Poole, R. K. (1999). The flavohemoglobin of Escherichia coli confers resistance to a nitrosating agent, a "nitric oxide releaser", and paraquat and is essential for transcriptional responses to oxidative stress. J Biol Chem 274, 748-754.
38. Nikov, G., Bhat, V., Wishnok J. F. & Tannenbaum, S. R. (2003). Analysis of nitrated proteins by nitrotyrosine-specific affinity probes and mass spectrometry. Anal Biochem 320, 214-222.
39. Ouellet, H., Ouellet, Y., Richard, C., Labarre, M., Wittenberg, B., Wittenberg, J. & Guertin, M. (2002). Truncated hemoglobin HbN protects Mycobacterium bovis from nitric oxide. Proc Natl Acad Sci U S A 99, 5902-5907.
40. Park K. W., Kim, K. J., Howard, A. J., Stark, B. C. & Webster, D. A. (2002). Vitreoscilla hemoglobin binds to subunit I of cytochrome bo ubiquinol oxidases. J Biol Chem 277, 33334-33337.
41. Parkhill, J., Wren, B. W., Mungall, K. & 18 other authors (2000). The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 403, 665-668.
42. Pathania, R., Navani, N. K., Rajamohan, G. & Dikshit, K. L. (2002). Mycobacterium tuberculosis hemoglobin HbO associates with membranes and stimulates cellular respiration of recombinant Escherichia coli. J Biol Chem 277, 15293-15302.
43. Pirt, S. J. (1975). Chapter 9. In Principles of Microbe and Cell Cultivation. Oxford: Blackwell Scientific Publications.
44. Pitcher, D. G., Saunders, N. A. & Owen, R. J. (1989). Rapid extraction of bacterial genomic DNA with guanidium. thiocyanate. Lett Appl Microbiol 8, 151-156.
45. Poole, R. K. (1976). The influence of growth substrate and capacity for oxidative phosphorylation on respiratory oscillations in synchronous cultures of Escherichia coli. J Gen Microbiol 99, 369-377.
46. Sellars, M. J., Hall, S. J. & Kelly, D. J. (2002). Growth of Campylobacter jejuni supported by respiration of fumarate, nitrate, nitrite, trimethylamine-N-oxide, or dimethyl sulfoxide requires oxygen. J Bacteriol 184, 4187-4196.
47. Skirrow, M. B. & Blaser, M. J. (2000). Clinical aspects of Campylobacter infection. In Campylobacter, pp. 69-88. Edited by I. Nachamkin & M. J. Blaser. Washington, DC: American Society for Microbiology.
48. Smith, A., Hill, S. & Anthony, C. (1990). The purification, characterization and role of the d-type cytochrome oxidase of Klebsiella pneumoniae during nitrogen fixation. J Gen Microbiol 136, 171-180.
49. Stevanin, T. M., Poole, R. K., Demoncheaux, E. A. G. & Read, R. C. (2002). Flavohemoglobin Hmp protects Salmonella enterica serovar typhimurium from nitric oxide-related killing by human macrophages. Infect Immun 70, 4399-4405.
50. 2-dependent gene regulation in facultatively anaerobic bacteria. Arch Microbiol 164, 81-90.
51. Wittenberg, J. B., Bolognesi, M., Wittenberg, B. A. & Guertin, M. (2002). Truncated hemoglobins: a new family of hemoglobins widely distributed in bacteria, unicellular eukaryotes, and plants. J Biol Chem 277, 871-874.
52. Wu, G., Wainwright, L. M. & Poole, R. K. (2003). Microbial globins. Adv Microb Physiol 47, 255-310.
53. Wu, G., Corker, H., Orii, Y. & Poole, R. K. (2004). Escherichia coli Hmp, an "oxygen-binding flavohaemoprotein", produces superoxide anion and self-destructs. Arch Microbiol 182, 193-203.