The presence of multiple c-type cytochromes at the surface of the methanotrophic bacterium Methylococcus capsulatus (Bath) is regulated by copper

Molecular Microbiology

Volumn 70, Issue 1, 2008, Pages 15-26

  Karlsen, O A ^a   Lillehaug, J R ^a   Jensen, H B ^a  

^a UNIVERSITY OF BERGEN   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

COPPER; CYTOCHROME C;

ARTICLE; BACTERIAL CELL; CELL CULTURE; CELL SURFACE; CONTROLLED STUDY; ENERGY TRANSFER; FUNCTIONAL PROTEOMICS; HOMEOSTASIS; MASS SPECTROMETRY; METHYLOCOCCUS CAPSULATUS; NONHUMAN; OXIDATION REDUCTION REACTION; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS;

BACTERIAL OUTER MEMBRANE PROTEINS; COPPER; CYTOCHROME C GROUP; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; GENE EXPRESSION REGULATION, BACTERIAL; HEME; MASS SPECTROMETRY; METHYLOCOCCUS CAPSULATUS; PHENOTYPE; PROTEOMICS; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, PROTEIN;

BACTERIA (MICROORGANISMS); METHYLOCOCCUS CAPSULATUS;

EID: 51649111734     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2008.06380.x     Document Type: Article

References (47)

1. Balasubramanian, R. Rosenzweig, A.C. (2007) Structural and mechanistic insights into methane oxidation by particulate methane monooxygenase. Acc Chem Res 40 : 573 580.
2. Beliaev, A.S., Saffarini, D.A., McLaughlin, J.L. Hunnicutt, D. (2001) MtrC, an outer membrane decahaem c cytochrome required for metal reduction in Shewanella putrefaciens MR-1. Mol Microbiol 39 : 722 730.
3. Bergmann, D.J., Zahn, J.A., Hooper, A.B. DiSpirito, A.A. (1998) Cytochrome P460 genes from the methanotroph Methylococcus capsulatus (Bath). J Bacteriol 180 : 6440 6445.
4. Bergmann, D.J., Zahn, J.A. DiSpirito, A.A. (1999) High-molecular-mass multi-c-heme cytochromes from Methylococcus capsulatus (Bath). J Bacteriol 181 : 991 997.
5. Berven, F.S., Karlsen, O.A., Murrell, J.C. Jensen, H.B. (2003) Multiple polypeptide forms observed in two-dimensional gels of Methylococcus capsulatus (Bath) polypeptides are generated during the separation procedure. Electrophoresis 24 : 757 761.
6. Berven, F.S., Karlsen, O.A., Straume, A.H., Flikka, K., Murrell, J.C., Fjellbirkeland, A., et al. (2006) Analysing the outer membrane subproteome of Methylococcus capsulatus (Bath) using proteomics and novel biocomputing tools. Arch Microbiol 184 : 362 377.
7. Borges-Walmsley, M.I., McKeegan, K.S. Walmsley, A.R. (2003) Structure and function of efflux pumps that confer resistance to drugs. Biochem J 376 : 313 338.
8. Brantner, C.A., Remsen, C.C., Owen, H.A., Buchholz, L.A. Perille Collins, M.L. (2002) Intracellular localization of the particulate methane monooxygenase and methanol dehydrogenase in Methylomicrobium album BG8. Arch Microbiol 178 : 59 64.
9. Brusseau, G.A., Tsien, H.C., Hanson, R.S. Wackett, L.P. (1990) Optimization of trichloroethylene oxidation by methanotrophs and the use of a colorimetric assay to detect soluble methane monooxygenase activity. Biodegradation 1 : 19 29.
10. Bycroft, M., Bateman, A., Clarke, J., Hamill, S.J., Sandford, R., Thomas, R.L. Chothia, C. (1999) The structure of a PKD domain from polycystin-1: implications for polycystic kidney disease. EMBO J 18 : 297 305.
11. Choi, D.W., Kunz, R.C., Boyd, E.S., Semrau, J.D., Antholine, W.E., Han, J.I., et al. (2003) The membrane-associated methane monooxygenase (pMMO) and pMMO-NADH: quinone oxidoreductase complex from Methylococcus capsulatus (Bath). J Bacteriol 185 : 5755 5764.
12. Dorward, D.W. (1993) Detection and quantitation of heme-containing proteins by chemiluminescence. Anal Biochem 209 : 219 223.
13. Feldman, R.A., Wang, E. Hanafusa, H. (1983) Cytoplasmic localization of the transforming protein of Fujinami sarcoma virus: salt-sensitive association with subcellular components. J Virol 45 : 782 791.
14. Gaspard, S., Vazquez, F. Holliger, C. (1998) Localization and solubilization of the Iron(III) reductase of Geobacter sulfurreducens. Appl Environ Microbiol 64 : 3188 3194.
15. Gatti, D., Mitra, B. Rosen, B.P. (2000) Escherichia coli soft metal ion-translocating ATPases. J Biol Chem 275 : 34009 34012.
16. Gennis, R.B. (1987) The cytochromes of Escherichia coli. FEMS Microbiol Rev 46 : 387 399.
17. Gobom, J., Nordhoff, E., Mirgorodskaya, E., Ekman, R. Roepstorff, P. (1999) Sample purification and preparation technique based on nano-scale reversed-phase columns for the sensitive analysis of complex peptide mixtures by matrix-assisted laser desorption/ionization mass spectrometry. J Mass Spectrom 34 : 105 116.
18. Hancock, R.E. Brinkman, F.S. (2002) Function of pseudomonas porins in uptake and efflux. Annu Rev Microbiol 56 : 17 38.
19. Heidelberg, J.F., Seshadri, R., Haveman, S.A., Hemme, C.L., Paulsen, I.T., Kolonay, J.F., et al. (2004) The genome sequence of the anaerobic, sulfate-reducing bacterium Desulfovibrio vulgaris Hildenborough. Nat Biotechnol 22 : 554 559.
20. Ingledew, W.J. (1982) Thiobacillus ferrooxidans - thebioenergetics of an acidophilic chemolithotroph. Biochim Biophys Acta 683 : 89 117.
21. Karlsen, O.A., Berven, F.S., Stafford, G.P., Larsen, O., Murrell, J.C., Jensen, H.B. Fjellbirkeland, A. (2003) The surface-associated and secreted MopE protein of Methylococcus capsulatus (Bath) responds to changes in the concentration of copper in the growth medium. Appl Environ Microbiol 69 : 2386 2388.
22. Karlsen, O.A., Kindingstad, L., Angelskar, S.M., Bruseth, L.J., Straume, D., Puntervoll, P., et al. (2005a) Identification of a copper-repressible C-type heme protein of Methylococcus capsulatus (Bath). A member of a novel group of the bacterial di-heme cytochrome c peroxidase family of proteins. FEBS J 272 : 6324 6335.
23. Karlsen, O.A., Ramsevik, L., Bruseth, L.J., Larsen, O., Brenner, A., Berven, F.S., et al. (2005b) Characterization of a prokaryotic haemerythrin from the methanotrophic bacterium Methylococcus capsulatus (Bath). FEBS J 272 : 2428 2440.
24. Laugesen, S. Roepstorff, P. (2003) Combination of two matrices results in improved performance of MALDI MS for peptide mass mapping and protein analysis. J Am Soc Mass Spectrom 14 : 992 1002.
25. Lovley, D.R. (2006) Bug juice: harvesting electricity with microorganisms. Nat Rev Microbiol 4 : 497 508.
26. Methe, B.A., Nelson, K.E., Eisen, J.A., Paulsen, I.T., Nelson, W., Heidelberg, J.F., et al. (2003) Genome of Geobacter sulfurreducens: metal reduction in subsurface environments. Science 302 : 1967 1969.
27. Mehta, T., Coppi, M.V., Childers, S.E. Lovley, D.R. (2005) Outer membrane c-type cytochromes required for Fe(III) and Mn(IV) oxide reduction in Geobacter sulfurreducens. Appl Environ Microbiol 71 : 8634 8641.
28. Myers, C.R. Myers, J.M. (2003) Cell surface exposure of the outer membrane cytochromes of Shewanella oneidensis MR-1. Lett Appl Microbiol 37 : 254 258.
29. Myers, C.R. Myers, J.M. (2004) The outer membrane cytochromes of Shewanella oneidensis MR-1 are lipoproteins. Lett Appl Microbiol 39 : 466 470.
30. Myers, J.M. Myers, C.R. (2001) Role for outer membrane cytochromes OmcA and OmcB of Shewanella putrefaciens MR-1 in reduction of manganese dioxide. Appl Environ Microbiol 67 : 260 269.
31. Myers, J.M. Myers, C.R. (2002) Genetic complementation of an outer membrane cytochrome omcB mutant of Shewanella putrefaciens MR-1 requires omcB plus downstream DNA. Appl Environ Microbiol 68 : 2781 2793.
32. Navarre, W.W. Schneewind, O. (1999) Surface proteins of gram-positive bacteria and mechanisms of their targeting to the cell wall envelope. Microbiol Mol Biol Rev 63 : 174 229.
33. Neuhoff, V., Arold, N., Taube, D. Ehrhardt, W. (1988) Improved staining of proteins in polyacrylamide gels including isoelectric focusing gels with clear background at nanogram sensitivity using Coomassie Brilliant Blue G-250 and R-250. Electrophoresis 9 : 255 262.
34. Niederman, R.A. (1974) Membranes of Rhodopseudomonas spheroides: interactions of chromatophores with the cell envelope. J Bacteriol 117 : 19 28.
35. Nielsen, A.K., Gerdes, K., Degn, H. Murrell, J.C. (1996) Regulation of bacterial methane oxidation: transcription of the soluble methane mono-oxygenase operon of Methylococcus capsulatus (Bath) is repressed by copper ions. Microbiology 142 (Part 5 1289 1296.
36. Nielsen, A.K., Gerdes, K. Murrell, J.C. (1997) Copper-dependent reciprocal transcriptional regulation of methane monooxygenase genes in Methylococcus capsulatus and Methylosinus trichosporium. Mol Microbiol 25 : 399 409.
37. Odenbreit, S. (2005) Adherence properties of Helicobacter pylori: impact on pathogenesis and adaptation to the host. Int J Med Microbiol 295 : 317 324.
38. Reguera, G., McCarthy, K.D., Mehta, T., Nicoll, J.S., Tuominen, M.T. Lovley, D.R. (2005) Extracellular electron transfer via microbial nanowires. Nature 435 : 1098 1101.
39. Scott, J.R. Barnett, H.-C. (2006) Surface proteins of gram-positive bacteria and how they get there. Annu Rev Microbiol 60 : 397 424.
40. Shevchenko, A., Wilm, M., Vorm, O. Mann, M. (1996) Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal Chem 68 : 850 858.
41. Shi, L., Squier, T.C., Zachara, J.M. Fredrickson, J.K. (2007) Respiration of metal (hydr)oxides by Shewanella and Geobacter: a key role for multihaem c-type cytochromes. Mol Microbiol 65 : 12 20.
42. Stanley, S.H., Prior, S.D.J. Dalton, H. (1983) Copper stress underlies the fundamental change in intracellular location of methane mono-oxygenase in methane-oxidizing organisms: studies in batch and continuous cultures. Biotechnol Lett 5 : 487 492.
43. Stevens, J.M., Daltrop, O., Allen, J.W. Ferguson, S.J. (2004) C-type cytochrome formation: chemical and biological enigmas. Acc Chem Res 37 : 999 1007.
44. Thomas, P.E., Ryan, D. Levin, W. (1976) An improved staining procedure for the detection of the peroxidase activity of cytochrome P-450 on sodium dodecyl sulfate polyacrylamide gels. Anal Biochem 75 : 168 176.
45. Vargas, C., McEwan, A.G. Downie, J.A. (1993) Detection of c-type cytochromes using enhanced chemiluminescence. Anal Biochem 209 : 323 326.
46. Ward, N., Larsen, O., Sakwa, J., Bruseth, L., Khouri, H., Durkin, A.S., et al. (2004) Genomic insights into methanotrophy: the complete genome sequence of Methylococcus capsulatus (Bath). PLoS Biol 2 : e303.
47. Whittenbury, R., Phillips, K.C. Wilkinson, J.F. (1970) Enrichment, isolation and some properties of methane-utilizing bacteria. J Gen Microbiol 61 : 205 218.