Tetrathionate stimulated growth of Campylobacter jejuni identifies a new type of bi-functional tetrathionate reductase (TsdA) that is widely distributed in bacteria

Molecular Microbiology

Volumn 88, Issue 1, 2013, Pages 173-188

  Liu, Yang Wei ^a   Denkmann, Kevin ^b   Kosciow, Konrad ^b   Dahl, Christiane ^b   Kelly, David J ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b UNIVERSITY OF BONN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ENZYME; CYSTEINE; CYTOCHROME C; HISTIDINE; OXIDOREDUCTASE; OXYGEN; TETRATHIONATE REDUCTASE; TETRATHIONIC ACID; THIOSULFATE; THIOSULPHATE DEHYDROGENASE; UNCLASSIFIED DRUG;

AMINO ACID SYNTHESIS; ARTICLE; BACTERIAL GROWTH; BINDING AFFINITY; CAMPYLOBACTER JEJUNI; CONTROLLED STUDY; ENERGY METABOLISM; ENZYME ACTIVITY; ENZYME KINETICS; ENZYME PURIFICATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION;

AEROBIOSIS; BIOCATALYSIS; CAMPYLOBACTER JEJUNI; CYTOCHROMES C; ELECTRONS; FORMATES; KINETICS; MODELS, BIOLOGICAL; MUTATION; NADH, NADPH OXIDOREDUCTASES; OXIDATION-REDUCTION; OXIDOREDUCTASES; OXYGEN; RECOMBINANT PROTEINS; SPECTRUM ANALYSIS; TETRATHIONIC ACID; THIOSULFATES;

CAMPYLOBACTER JEJUNI; VERTEBRATA;

EID: 84875618987     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12176     Document Type: Article

References (58)

1. 3 oxidase in Escherichia coli. Biochem Biophys Res Commun 251: 744-747.
2. Atkinson, S.J., Mowat, C.G., Reid, G.A., and Chapman, S.K. (2007) An octaheme c-type cytochrome from Shewanella oneidensis can reduce nitrite and hydroxylamine. FEBS Lett 581: 3805-3808.
3. Bamford, V.A., Bruno, S., Rasmussen, T., Appia-Ayme, C., Cheesman, M.R., Berks, B.C., and Hemmings, A.M. (2002) Structural basis for the oxidation of thiosulfate by a sulfur cycle enzyme. EMBO J 21: 5599-5610.
4. Blachier, F., Davila, A.M., Mimoun, S., Benetti, P.H., Atanasiu, C., Andriamihaja, M., etal. (2010) Luminal sulfide and large intestine mucosa: friend or foe? Amino Acids 39: 335-347.
5. Blaser, M.J., and Engberg, J. (2008) Clinical aspects of Campylobacter jejuni and Campylobacter coli infections. In Campylobacter. Nachamkin, I., Szymanski, G., and Blaser, M.J. (eds). Washington, DC: ASM Press, pp. 99-121.
6. Cheesman, M.R., Little, P.J., and Berks, B.C. (2001) Novel heme ligation in a c-type cytochrome involved in thiosulfate oxidation: EPR and MCD of SoxAX from Rhodovulum sulfidophilum. Biochemistry 40: 10562-10569.
7. Dahl, C., Engels, S., Pott-Sperling, A.S., Schulte, A., Sander, J., Lübbe, Y., etal. (2005) Novel genes of the dsr gene cluster and evidence for close interaction of Dsr proteins during sulfur oxidation in the phototrophic sulfur bacterium Allochromatium vinosum. J Bacteriol 187: 1392-1404.
8. Dambe, T., Quentmeier, A., Rother, D., Friedrich, C., and Scheidig, A.J. (2005) Structure of the cytochrome complex SoxXA of Paracoccus pantotrophus, a heme enzyme initiating chemotrophic sulfur oxidation. J Struct Biol 152: 229-234.
9. Denkmann, K., Grein, F., Zigann, R., Siemen, A., Bergmann, J., Nicolai, A., etal. (2012) Thiosulfate dehydrogenase: a wide-spread unusual acidophilic c-type cytochrome. Environ Microbiol 14: 2673-2688.
10. Emerson, D., Rentz, J.A., Lilburn, T.G., Davis, R.E., Aldrich, H., Chan, C., and Moyer, C.L. (2007) A novel lineage of Proteobacteria involved in formation of marine Fe-oxidizing microbial mat communities. PLoS ONE 2: e667.
11. Friedrich, C.G., Rother, D., Bardischewsky, F., Quentmeier, A., and Fischer, J. (2001) Oxidation of reduced inorganic sulfur compounds by bacteria: emergence of a common mechanism? Appl Environ Microbiol 67: 2873-2882.
12. Fultz, M.L., and Durst, R.A. (1982) Mediator compounds for the electrochemical study of biological redox systems - a compilation. Anal Chim Acta 140: 1-18.
13. Furne, J., Springfield, J., Koenig, T., DeMaster, E., and Levitt, M.D. (2001) Oxidation of hydrogen sulfide and methanethiol to thiosulfate by rat tissues: a specialized function of the colonic mucosa. Biochem Pharmacol 62: 255-259.
14. Gaskin, D.J.H., van Vliet, A.H.M., and Pearson, B.M. (2007) The Campylobacter genetic toolbox: development of tractable and generally applicable genetic techniques for Campylobacter jejuni. Zoonoses Public Health 54: 101.
15. van Gelder, B., and Slater, E.C. (1962) The extinction coefficient of cytochrome c. Biochim Biophys Acta 58: 593-595.
16. Gibson, D.G., Young, L., Chuang, R.Y., Venter, J.C., Hutchison, C.A., and Smith, H.O. (2009) Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat Methods 6: 343-U41.
17. Grein, F., Venceslau, S.S., Schneider, L., Hildebrandt, P., Todorovic, S., Pereira, I.A.C., and Dahl, C. (2010) DsrJ, an essential part of the DsrMKJOP complex in the purple sulfur bacterium Allochromatium vinosum, is an unusual triheme cytochrome c. Biochemistry 49: 8290-8299.
18. Guccione, E., Hitchcock, A., Hall, S.J., Mulholland, F., Shearer, N., van Vliet, A.H., and Kelly, D.J. (2010) Reduction of fumarate, mesaconate and crotonate by Mfr, a novel oxygen-regulated periplasmic reductase in Campylobacter jejuni. Environ Microbiol 12: 576-591.
19. Hensel, M., Hinsley, A.P., Nikolaus, T., Sawers, G., and Berks, B.C. (1999) The genetic basis of tetrathionate respiration in Salmonella typhimurium. Mol Microbiol 32: 275-287.
20. Hensen, D., Sperling, D., Trüper, H.G., Brune, D.C., and Dahl, C. (2006) Thiosulphate oxidation in the phototrophic sulphur bacterium Allochromatium vinosum. Mol Microbiol 62: 794-810.
21. Hermans, D., Van Deun, K., Messens, W., Martel, A., Van Immerseel, F., Haesebrouck, F., etal. (2011) Campylobacter control in poultry by current intervention measures ineffective: urgent need for intensified fundamental research. Vet Microbiol 152: 219-228.
22. Hinojosa-Leon, M., Dubourdieu, M., Sanchez-Crispin, J.A., and Chippaux, M. (1986) Tetrathionate reductase from Salmonella typhimurium: a molybdenum containing enzyme. Biochem Biophys Res Commun 136: 577-581.
23. Hitchcock, A., Hall, S.J., Myers, J.D., Mulholland, F., Jones, M.A., and Kelly, D.J. (2010) Roles of the twin-arginine translocase and associated chaperones in the biogenesis of the electron transport chains of the human pathogen Campylobacter jejuni. Microbiology 156: 2994-3010.
24. Jackson, R.J., Elvers, K.T., Lee, L.J., Gidley, M.D., Wainwright, L.M., Lightfoot, J., etal. (2007) Oxygen reactivity of both respiratory oxidases in Campylobacter jejuni: the cydAB genes encode a cyanide-resistant, low-affinity oxidase that is not of the cytochrome bd type. J Bacteriol 189: 1604-1615.
25. Jacobs, B.C., van Belkum, A., and Endtz, H.P. (2008) Gullain-Barré syndrome and Campylobacter infection. In Campylobacter. Nachamkin, I., Szymanski, G., and Blaser, M.J. (eds). Washington, DC: ASM Press, pp. 245-261.
26. Juhnke, H.D., Hiltscher, H., Nasiri, H.R., Schwalbe, H., and Lancaster, C.R.D. (2009) Production, characterization and determination of the real catalytic properties of the putative 'succinate dehydrogenase' from Wolinella succinogenes. Mol Microbiol 71: 1088-1101.
27. Kelly, D.J. (2008) Complexity and versatility in the physiology and metabolism of Campylobacter jejuni. In Campylobacter. Nachamkin, I., Szymanski, G., and Blaser, M.J. (eds). Washington, DC: ASM Press, pp. 41-61.
28. Kelly, D.P., Chambers, L.A., and Trudinger, P.A. (1969) Cyanolysis and spectrophotometric estimation of trithionate in mixture with thiosulfate and tetrathionate. Anal Chem 41: 898-901.
29. Levitt, M.D., Furne, J., Springfield, J., Suarez, F., and DeMaster, E. (1999a) Detoxification of hydrogen sulfide and methanethiol in the cecal mucosa. J Clin Invest 104: 1107-1114.
30. Levitt, M.D., Furne, J.K., Springfield, J., and Suarez, F.L. (1999b) Colonic hydrogen sulfide and methanethiol are detoxified via a novel reaction that results in thiosulfate. Gastroenterology 116: A762-A763.
31. 2. Biochim Biophys Acta 1202: 82-86.
32. Molbak, K., and Havelaar, A. (2008) Burden of illness of campylobacteriosis and sequelae. In Campylobacter. Nachamkin, I., Szymanski, G., and Blaser, M.J. (eds). Washington, DC: ASM Press, pp. 151-162.
33. Mowat, C.G., Rothery, E., Miles, C.S., McIver, L., Doherty, M.K., Drewette, K., etal. (2004) Octaheme tetrathionate reductase is a respiratory enzyme with novel heme ligation. Nat Struct Mol Biol 11: 1023-1024.
34. Myer, Y.P., Saturno, A.F., Verma, B.C., and Pande, A. (1979) Horse heart cytochrome-c - oxidation-reduction potential and protein structures. J Biol Chem 254: 1202-1207.
35. Myers, J.D., and Kelly, D.J. (2005) A sulphite respiration system in the chemoheterotrophic human pathogen Campylobacter jejuni. Microbiology 151: 233-242.
36. Oltman, L.F., Claasen, V.P., Kastelein, P., Reijinders, W.N.M., and Stouthammer, A.H. (1979) The influence of tungstate on the formation and activities of four reductases of Proteus mirabilis: identification of two new molybdoenzymes, chlorate reductase and tetrathionate reductase. FEBS Lett 106: 43-46.
37. Pande, A., and Myer, Y.P. (1978) Redox potential of horse heart cytochrome-c. Biochem Biophys Res Commun 85: 7-13.
38. 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.
39. Rappaport, F., Hirschberg, I., and Konforti, N. (1956) Modified tetrathionate enrichment medium for certain Salmonellae. Acta Med Orient 15: 84-87.
40. Reijerse, E.J., Sommerhalter, M., Hellwig, P., Quentmeier, A., Rother, D., Laurich, C., etal. (2007) The unusal redox centers of SoxXA, a novel c-type heme-enzyme essential for chemotrophic sulfur-oxidation of Paracoccus pantotrophus. Biochemistry 46: 7804-7810.
41. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
42. Segel, I.H. (1993) Enzyme Kinetics: Behavior and Analysis of Rapid Equilibrium and Steady-State Enzyme Systems. New York: Wiley-Interscience.
43. Sellars, M.J., Hall, S.J., and 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.
44. Smart, J.P., Cliff, M.J., and Kelly, D.J. (2009) A role for tungsten in the biology of Campylobacter jejuni: tungstate stimulates formate dehydrogenase activity and is transported via an ultra-high affinity ABC system distinct from the molybdate transporter. Mol Microbiol 74: 742-757.
45. Tareen, A.M., Dasti, J.I., Zautner, A.E., Gross, U., and Lugert, R. (2011) Sulphite:cytochrome c oxidoreductase deficiency in Campylobacter jejuni reduces motility, host cell adherence and invasion. Microbiology 157: 1776-1785.
46. Thauer, R.K., Jungermann, K., and Decker, K. (1977) Energy conservation in chemotrophic anaerobic bacteria. Bacteriol Rev 41: 100-180.
47. Thiennimitr, P., Winter, S.E., Winter, M.G., Xavier, M.N., Tolstikov, V., Huseby, D.L., etal. (2011) Intestinal inflammation allows Salmonella to use ethanolamine to compete with the microbiota. Proc Natl Acad Sci USA 108: 17480-17485.
48. Thomas, M.T., Shepherd, M., Poole, R.K., van Vliet, A.H.M., Kelly, D.J., and Pearson, B.M. (2011) Two respiratory enzyme systems in Campylobacter jejuni NCTC 11168 contribute to growth on L-lactate. Environ Microbiol 13: 48-61.
49. Thomas, P.E., Ryan, D., and Levin, W. (1976) Improved staining procedure for detection of peroxidase-activity of cytochrome P-450 on sodium dodecyl-sulfate polyacrylamide gels. Anal Biochem 75: 168-176.
50. Trudinger, P.A. (1967) Metabolism of thiosulfate and tetrathionate by heterotrophic bacteria from soil. J Bacteriol 93: 550-559.
51. Tuttle, J.H. (1980) Thiosulfate oxidation and tetrathionate reduction by a marine pseudomonad 16B. Appl Environ Microbiol 39: 1159-1166.
52. Urban, P.J. (1961) Colorimetry of sulfur anions. I. An improved colorimetric method for the determination of thiosulfate. Z Analyt Chem 179: 415-422.
53. Velayudhan, J., and Kelly, D.J. (2002) Analysis of gluconeogenic and anaplerotic enzymes in Campylobacter jejuni: an essential role for phosphoenolpyruvate carboxykinase. Microbiology 148: 685-694.
54. van Vliet, A.H.M., Wood, A.C., Henderson, J., Wooldridge, K., and Ketley, J.M. (1998) Genetic manipulation of enteric Campylobacter species. Methods Microbiol 27: 407-419.
55. Weingarten, R.A., Taveirne, M.E., and Olson, J.W. (2009) The dual functioning fumarate reductase is the sole succinate:quinone reductase in Campylobacter jejuni and is required for full host colonization. J Bacteriol 191: 5293-5300.
56. Whited, G.M., and Tuttle, J.H. (1983) Separation and distribution of thiosulfate-oxidizing enzyme, tetrathionate reductase, and thiosulfate reductase in extracts of marine heterotroph strain 16B. J Bacteriol 156: 600-610.
57. Winter, S.E., Thiennimitr, P., Winter, M.G., Butler, B.P., Huseby, D.L., Crawford, R.W., etal. (2010) Gut inflammation provides a respiratory electron acceptor for Salmonella. Nature 467: 426-429.
58. Zehnder, A.J.B., and Wuhrmann, K. (1976) Titanium(III) citrate as a nontoxic oxidation-reduction buffering system for culture of obligate anaerobes. Science 194: 1165-1166.