The Wolinella succinogenes mcc gene cluster encodes an unconventional respiratory sulphite reduction system

Molecular Microbiology

Volumn 82, Issue 6, 2011, Pages 1515-1530

  Kern, Melanie ^a   Klotz, Martin G ^b   Simon, Jörg ^a  

^a DARMSTADT UNIVERSITY OF TECHNOLOGY   (Germany)

^b UNIVERSITY OF NORTH CAROLINA AT CHARLOTTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME C; FORMIC ACID; FUMARIC ACID; MULTIHAEME CYTOCHROME C A; MULTIHAEME CYTOCHROME C B; MULTIHAEME CYTOCHROME C C; MULTIHAEME CYTOCHROME C D; NITRATE; SULFIDE; SULFITE; THIOSULFATE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIUM MUTANT; CONTROLLED STUDY; GENE CLUSTER; MCC GENE; NONHUMAN; OPEN READING FRAME; PHENOTYPE; PRIORITY JOURNAL; PROTEIN MOTIF; PROTEIN SYNTHESIS; WOLINELLA SUCCINOGENES;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; IRON-SULFUR PROTEINS; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; OXIDATION-REDUCTION; SULFITE DEHYDROGENASE; SULFITES; WOLINELLA;

WOLINELLA SUCCINOGENES;

EID: 83355166271     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2011.07906.x     Document Type: Article

References (76)

1. Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zheng, Z., Miller, W., and Lipman, D.J. (1997) Gapped BLAST and PSI-BLAST - a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
2. Baar, C., Eppinger, M., Raddatz, G., Simon, J., Lanz, C., Klimmek, O., etal. (2003) Complete genome sequence and analysis of Wolinella succinogenes. Proc Natl Acad Sci USA 100: 11690-11695.
3. Beliaev, A.S., Klingeman, D.M., Klappenbach, J.A., Wu, L., Romine, M.F., Tiedje, J.M., etal. (2005) Global transcription analysis of Shewanella oneidensis MR-1 exposed to different terminal electron acceptors. J Bacteriol 187: 7138-7145.
4. Bergmann, D.J., Hooper, A.B., and Klotz, M.G. (2005) Structure and sequence conservation of hao cluster genes of autotrophic ammonia-oxidizing bacteria: evidence for their evolutionary history. Appl Environ Microbiol 71: 5371-5382.
5. 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.
6. Burns, J.L., and DiChristina, T.J. (2009) Anaerobic respiration of elemental sulphur and thiosulfate by Shewanella oneidensis MR-1 requires psrA, a homolog of the phs gene of Salmonella enterica serovar typhimurium LT2. Appl Environ Microbiol 75: 5209-5217.
7. Clarke, T.A., Hemmings, A.M., Burlat, B., Butt, J.N., Cole, J.A., and Richardson, D.J. (2006) Comparison of the structural and kinetic properties of the cytochrome c nitrite reductases from Escherichia coli, Wolinella succinogenes, Sulfurospirillum deleyianum and Desulfovibrio desulfuricans. Biochem Soc Trans 34: 143-145.
8. Clarke, T.A., Cole, J.A., Richardson, D.J., and Hemmings, A.M. (2007) The crystal structure of the pentahaem c-type cytochrome NrfB and characterization of its solution-state interaction with the pentahaem nitrite reductase NrfA. Biochem J 406: 19-30.
9. Cordova, C.D., Schicklberger, F.R., Yu, Y., and Spormann, A.M. (2011) Partial functional replacement of CymA by SirCD in Shewanella oneidensis MR-1. J Bacteriol 193: 2323-2321.
10. Crane, B.R., and Getzoff, E.D. (1996) The relationship between structure and function for the sulfite reductases. Curr Opin Struct Biol 6: 744-756.
11. Dahl, C., and Friedrich, C.G. (2008) Microbial Sulfur Metabolism. Berlin: Springer.
12. Dietrich, W., and Klimmek, O. (2002) The function of methyl-menaquinone-6 and polysulfide reductase membrane anchor (PsrC) in polysulfide respiration of Wolinella succinogenes. Eur J Biochem 269: 1086-1095.
13. Drummond, A., and Rambaut, A. (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7: 214.
14. Einsle, O., Stach, P., Messerschmidt, A., Simon, J., Kröger, A., Huber, R., and Kroneck, P.M.H. (2000) Cytochrome c nitrite reductase from Wolinella succinogenes: structure at 1.6 Å resolution, inhibitor binding, and heme-packing motifs. J Biol Chem 275: 39608-39616.
15. Francis, R.T., and Becker, R.R. (1984) Specific indication of hemoproteins in polyacrylamide gels using a double-staining process. Anal Biochem 136: 509-514.
16. Gross, R., Pisa, R., Sänger, M., Lancaster, C.R.D., and Simon, J. (2004) Characterization of the menaquinone reduction site in the diheme cytochrome b membrane anchor of Wolinella succinogenes Ni/Fe-hydrogenase. J Biol Chem 279: 274-281.
17. Gross, R., Eichler, R., and Simon, J. (2005) Site-directed modifications indicate differences in axial haem c iron ligation between the related NrfH and NapC families of multihaem c-type cytochromes. Biochem J 390: 689-693.
18. Hartshorne, R.S., Kern, M., Meyer, B., Clarke, T.A., Karas, M., Richardson, D.J., and Simon, J. (2007) A dedicated haem lyase is required for the maturation of a novel bacterial cytochrome c with unconventional covalent haem binding. Mol Microbiol 64: 1049-1060.
19. Hartshorne, S., Richardson, D.J., and Simon, J. (2006) Multiple haem lyase genes indicate substrate specificity in cytochrome c biogenesis. Biochem Soc Trans 34: 146-149.
20. Hooper, A.B., Arciero, D.M., Bergmann, D., and Hendrich, M.P. (2005) The oxidation of ammonia as an energy source in bacteria in respiration. In Respiration in Archaea and Bacteria. Zannoni, D. (ed.). Dordrecht: Springer, pp. 121-147.
21. Hsieh, Y.C., Liu, M.Y., Wang, V.C., Chiang, Y.L., Liu, E.H., Wu, W.G., etal. (2010) Structural insights into the enzyme catalysis from comparison of three forms of dissimilatory sulphite reductase from Desulfovibrio gigas. Mol Microbiol 78: 1101-1106.
22. Huang, C.J., and Barrett, E.L. (1990) Identification and cloning of genes involved in anaerobic sulfite reduction by Salmonella typhimurium. J Bacteriol 172: 4100-4102.
23. Johnson, E.F., and Mukhopadhyay, B. (2005) A new type of sulfite reductase, a novel coenzyme F420-dependent enzyme, from the methanarchaeon Methanocaldococcus jannaschii. J Biol Chem 280: 38776-38786.
24. Jormakka, M., Yokoyama, K., Yano, T., Tamakoshi, M., Akimoto, S., Shimamura, T., etal. (2008) Molecular mechanism of energy conservation in polysulfide respiration. Nat Struct Mol Biol 15: 730-737.
25. Kemp, G.L., Clarke, T.A., Marritt, S.J., Lockwood, C., Poock, S.R., Hemmings, A.M., etal. (2010) Kinetic and thermodynamic resolution of the interactions between sulfite and the pentahaem cytochrome NrfA from Escherichia coli. Biochem J 431: 73-80.
26. Kern, M., and Simon, J. (2008) Characterization of the NapGH quinol dehydrogenase complex involved in Wolinella succinogenes nitrate respiration. Mol Microbiol 69: 1137-1152.
27. 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.
28. 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.
29. Kern, M., and Simon, J. (2011) Production of recombinant multiheme cytochromes c in Wolinella succinogenes. Methods Enzymol 486: 429-446.
30. Kern, M., Mager, A., and Simon, J. (2007) Role of individual nap gene cluster products in NapC-independent nitrate respiration of Wolinella succinogenes. Microbiology 153: 3739-3747.
31. Kern, M., Eisel, F., Scheithauer, J., Kranz, R.G., and Simon, J. (2010a) 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.
32. Kern, M., Scheithauer, J., Kranz, R.G., and Simon, J. (2010b) Essential histidine pairs indicate conserved haem binding in epsilonproteobacterial cytochrome c haem lyases. Microbiology 156: 3773-3781.
33. Kern, M., Volz, J., and Simon, J. (2011) 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. Environ Microbiol 13: 2478-2494.
34. King, T.E., and Morris, R.O. (1967) Determination of acid-labile sulfide and sulfhydryl groups. Methods Enzymol 10: 634-641.
35. 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: Springer, pp. 217-232.
36. Klotz, M.G., and Stein, L.Y. (2011) Genomics of ammonia-oxidizing bacteria and insights into their evolution. In Nitrification. Ward, B.B., Klotz, M.G., and Arp, D.J. (eds). Washington, DC: ASM Press, pp. 57-94.
37. Klotz, M.G., Schmid, M.C., Strous, M., Op den Camp, H.J.M., Jetten, M.S.M., and Hooper, A.B. (2008) Evolution of an octaheme cytochrome c protein family that is key to aerobic and anaerobic ammonia oxidation by bacteria. Environ Microbiol 10: 3150-3163.
38. Kostera, J., Youngblut, M.D., Slosarczyk, J.M., and Pacheco, A.A. (2008) Kinetic and product distribution analysis of NO· reductase activity in Nitrosomonas europaea hydroxylamine oxidoreductase. J Biol Inorg Chem 13: 1073-1083.
39. Kranz, R.G., Richard-Fogal, C., Taylor, J.S., and Frawley, E.R. (2009) Cytochrome c biogenesis: mechanisms for covalent modifications and trafficking of heme and for heme-iron redox control. Microbiol Mol Biol Rev 73: 510-528.
40. 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: Academic Press, pp. 141-147.
41. 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.
42. 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.
43. Lukat, P., Rudolf, M., Stach, P., Messerschmidt, A., Kroneck, P.M.H., Simon, J., and Einsle, O. (2008) Binding and reduction of sulfite by cytochrome c nitrite reductase. Biochemistry 47: 2080-2086.
44. 2S plus fumarate and on formate plus sulfur as energy sources. Arch Microbiol 144: 147-150.
45. Mileni, M., MacMillan, F., Tziatzios, C., Zwicker, K., Haas, A.H., Mäntele, W., etal. (2006) Heterologous production in Wolinella succinogenes and characterization of the quinol:fumarate reductase enzymes from Helicobacter pylori and Campylobacter jejuni. Biochem J 395: 191-201.
46. Myers, J.D., and Kelly, D.J. (2005) A sulphite respiration system in the chemoheterotrophic human pathogen Campylobacter jejuni. Microbiology 151: 233-242.
47. Oliveira, T.F., Vonrhein, C., Matias, P.M., Venceslau, S.S., Pereira, I.A.C., and Archer, M. (2008) The crystal structure of Desulfovibrio vulgaris dissimilatory sulfite reductase bound to DsrC provides novel insights into the mechanism of sulfate respiration. J Biol Chem 283: 34141-34149.
48. Oliveira, T.F., Franklin, E., Afonso, J.P., Khan, A.R., Oldham, N.J., Pereira, I.A.C., and Archer, M. (2011) Structural insights into dissimilatory sulfite reductases: structure of desulforubidin from Desulfomicrobium norvegicum. Front Microbiol 2: 71. doi: 10.3389/fmicb.2011.00071.
49. Pachmayer, F. (1960) Vorkommen und Bestimmung von Schwefelverbindungen in Mineralwasser. PhD thesis, Ludwig Maximilians Universität, Munich, Germany.
50. Parey, K., Warkentin, E., Kroneck, P.M.H., and Ermler, U. (2010) Reaction cycle of the dissimilatory sulfite reductase from Archaeoglobus fulgidus. Biochemistry 49: 8912-8921.
51. Pereira, I.A.C., Ramos, A.R., Grein, F., Marques, M.C., da Silva, S.M., and Venceslau, S.S. (2011) A comparative genomic analysis of energy metabolism in sulfate reducing bacteria and archaea. Front Microbiol 2: 69. doi: 10.3389/fmicb.2011.00069.
52. Pereira, I.C., Abreu, I.A., Xavier, A.V., LeGall, J., and Teixeira, M. (1996) Nitrite reductase from Desulfovibrio desulfuricans (ATCC 27774) - a heterooligomer heme protein with sulfite reductase activity. Biochem Biophys Res Commun 224: 611-618.
53. Pfennig, N., and Trüper, H.G. (1981) Isolation of members of the families chromatiaceae and chlorobiaceae. In The Prokaryotes. vol. 1. Starr, M.P. (ed.). Berlin: Springer, pp. 279-289.
54. Pisa, R., Stein, T., Eichler, R., Gross, R., and Simon, J. (2002) The nrfI gene is essential for the attachment of the active site haem group of Wolinella succinogenes cytochrome c nitrite reductase. Mol Microbiol 43: 763-770.
55. Quentin, K.E., and Pachmayr, F. (1964) Bestimmung von Thiosulfat in schwefelhaltigen Mineralwässern. Fresenius J Anal Chem 200: 250-256.
56. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
57. Schiffer, A., Parey, K., Warkentin, E., Diederichs, K., Huber, H., Stetter, K.O., etal. (2008) Structure of the dissimilatory sulfite reductase from the hyperthermophilic archaeon Archaeoglobus fulgidus. J Mol Biol 379: 1063-1074.
58. Schumacher, W., Kroneck, P.M.H., and Pfennig, N. (1992) Comparative systematic study on 'Spirillum' 5175, Campylobacter and Wolinella species. Arch Microbiol 158: 287-293.
59. Shirodkar, S., Reed, S., Romine, M., and Saffarini, D. (2011) The octahaem SirA catalyses dissimilatory sulfite reduction in Shewanella oneidensis MR-1. Environ Microbiol 13: 108-115.
60. Simon, J. (2002) Enzymology and bioenergetics of respiratory nitrite ammonification. FEMS Microbiol Rev 26: 285-309.
61. Simon, J., and Hederstedt, L. (2011) Composition and function of cytochrome c biogenesis System II. FEBS J 278: 4179-4188.
62. Simon, J., and Kern, M. (2008) Quinone-reactive proteins devoid of haem b form widespread membrane-bound electron transport modules in bacterial respiration. Biochem Soc Trans 36: 1011-1016.
63. 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.
64. 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.
65. 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.
66. Simon, J., Eichler, R., Pisa, R., Biel, S., and Gross, R. (2002) Modification of heme c binding motifs in the small subunit (NrfH) of the Wolinella succinogenes cytochrome c nitrite reductase complex. FEBS Lett 522: 83-87.
67. 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.
68. 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.
69. Simon, J., van Spanning, R.J.M., and Richardson, D.J. (2008) The organization of proton motive and non-proton motive redox loops in prokaryotic respiratory systems. Biochim Biophys Acta 1777: 1480-1490.
70. Simon, J., Kern, M., Hermann, B., Einsle, O., and Butt, J.N. (2011) Physiological function and catalytic versatility of bacterial multihaem cytochromes c involved in nitrogen and sulfur cycling. Biochem Soc Trans 39: 1864-1870.
71. 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.
72. Swofford, D.L. (1999) PAUP (Phylogenetic Analysis Using Parsimony)*. Sunderland, MA: Sinauer Associates.
73. Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F., and Higgins, D.G. (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24: 4876-4882.
74. 554 of Nitrosomonas europaea. J Am Chem Soc 128: 4330-4337.
75. Whelan, S., and Goldman, N. (2001) A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol Biol Evol 18: 691-699.
76. Zehnder, A.J.B., and Wuhrmann, K. (1976) Titanium (III) citrate as a nontoxic oxidation-reduction buggering system for the culture of obligate anaerobes. Science 194: 1165-1166.