1887

Abstract

The nucleotide sequence of an open reading frame () downstream of the copper-repressible CorA-encoding gene of the methanotrophic bacterium BG8 was obtained by restriction enzyme digestion and inverse PCR. The amino acid sequence deduced from this gene showed significant sequence similarity to the surface-associated di-haem cytochrome peroxidase (SACCP) previously isolated from (Bath), including both -type haem-binding motifs. Homology analysis placed this protein, phylogenetically, within the subfamily containing the SACCP of the bacterial di-haem cytochrome peroxidase (BCCP) family of proteins. Immunospecific recognition confirmed synthesis of the CorB as a protein non-covalently associated with the outer membrane and exposed to the periplasm. c expression is regulated by the availability of copper ions during growth and the protein is most abundant in when grown at a low copper-to-biomass ratio, indicating an important physiological role of CorB under these growth conditions. was co-transcribed with the gene encoding CorA, constituting a copper-responding operon, which appears to be under the control of a -dependent promoter. CorB is the second isolated member of the recently described subfamily of the BCCP family of proteins. So far, these proteins have only been described in methanotrophic bacteria.

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2010-09-01
2024-04-20
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References

  1. Allen J. W., Barker P. D., Daltrop O., Stevens J. M., Tomlinson E. J., Sinha N., Sambongi Y., Ferguson S. J. 2005; Why isn't ‘standard’ heme good enough for c-type and d1-type cytochromes?. Dalton Trans3410–3418
    [Google Scholar]
  2. Barrios H., Valderrama B., Morett E. 1999; Compilation and analysis of σ54-dependent promoter sequences. Nucleic Acids Res 27:4305–4313
    [Google Scholar]
  3. Bendtsen J. D., Nielsen H., von Heijne G., Brunak S. 2004; Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340:783–795
    [Google Scholar]
  4. Berson O., Lidstrom M. E. 1997; Cloning and characterization of corA, a gene encoding a copper-repressible polypeptide in the type I methanotroph, Methylomicrobium albus BG8. FEMS Microbiol Lett 148:169–174
    [Google Scholar]
  5. Brodsky L. I., Ivanov V. V., Kalaydzidis Y. L., Leontovich A. M., Nikolaev V. K., Feranchuk S. I., Drachev V. A. 1995; Genebee-Net–internet-based server for analyzing biopolymers structure. Biochemistry (Mosc 60:923–928
    [Google Scholar]
  6. Chistoserdov A. Y., Chistoserdova L. V., McIntire W. S., Lidstrom M. E. 1994; Genetic organization of the mau gene cluster in Methylobacterium extorquens AM1: complete nucleotide sequence and generation and characteristics of mau mutants. J Bacteriol 176:4052–4065
    [Google Scholar]
  7. Collado-Vides J., Magasanik B., Gralla J. D. 1991; Control site location and transcriptional regulation in Escherichia coli. Microbiol Rev 55:371–394
    [Google Scholar]
  8. Csaki R., Bodrossy L., Klem J., Murrell J. C., Kovacs K. L. 2003; Genes involved in the copper-dependent regulation of soluble methane monooxygenase of Methylococcus capsulatus (Bath): cloning, sequencing and mutational analysis. Microbiology 149:1785–1795
    [Google Scholar]
  9. Dorward D. W. 1993; Detection and quantitation of heme-containing proteins by chemiluminescence. Anal Biochem 209:219–223
    [Google Scholar]
  10. Ferguson S. J. 2001; Keilin's cytochromes: how bacteria use them, vary them and make them. Biochem Soc Trans 29:629–640
    [Google Scholar]
  11. Fjellbirkeland A., Kleivdal H., Joergensen C., Thestrup H., Jensen H. B. 1997; Outer membrane proteins of Methylococcus capsulatus (Bath. Arch Microbiol 168:128–135
    [Google Scholar]
  12. Fjellbirkeland A., Kruger P. G., Bemanian V., Hogh B. T., Murrell J. C., Jensen H. B. 2001; The C-terminal part of the surface-associated protein MopE of the methanotroph Methylococcus capsulatus (Bath) is secreted into the growth medium. Arch Microbiol 176:197–203
    [Google Scholar]
  13. Fulop V., Ridout C. J., Greenwood C., Hajdu J. 1995; Crystal structure of the di-haem cytochrome c peroxidase from Pseudomonas aeruginosa. Structure 3:1225–1233
    [Google Scholar]
  14. Gardy J. L., Laird M. R., Chen F., Rey S., Walsh C. J., Ester M., Brinkman F. S. 2005; PSORTb v.2.0: expanded prediction of bacterial protein subcellular localization and insights gained from comparative proteome analysis. Bioinformatics 21:617–623
    [Google Scholar]
  15. Gattiker A., Gasteiger E., Bairoch A. 2002; ScanProsite: a reference implementation of a PROSITE scanning tool. Appl Bioinformatics 1:107–108
    [Google Scholar]
  16. Goodhew C. F., Wilson I. B., Hunter D. J., Pettigrew G. W. 1990; The cellular location and specificity of bacterial cytochrome c peroxidases. Biochem J 271:707–712
    [Google Scholar]
  17. Hancock R. E., Carey A. M. 1979; Outer membrane of Pseudomonas aeruginosa: heat-2-mercaptoethanol-modifiable proteins. J Bacteriol 140:902–910
    [Google Scholar]
  18. Helland R., Fjellbirkeland A., Karlsen O. A., Ve T., Lillehaug J. R., Jensen H. B. 2008; An oxidized tryptophan facilitates copper binding in Methylococcus capsulatus-secreted protein MopE. J Biol Chem 283:13897–13904
    [Google Scholar]
  19. 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
    [Google Scholar]
  20. Karlsen O. A., Kindingstad L., Angelskar S. M., Bruseth L. J., Straume D., Puntervoll P., Fjellbirkeland A., Lillehaug J. R., Jensen H. B. 2005; 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
    [Google Scholar]
  21. Karlsen O. A., Lillehaug J. R., Jensen H. B. 2008; The presence of multiple c-type cytochromes at the surface of the methanotrophic bacterium Methylococcus capsulatus (Bath) is regulated by copper. Mol Microbiol 70:15–26
    [Google Scholar]
  22. Laemmli U. K. 1970; Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685
    [Google Scholar]
  23. Li X., Feng M., Wang Y., Tachikawa H., Davidson V. L. 2006; Evidence for redox cooperativity between c-type hemes of MauG which is likely coupled to oxygen activation during tryptophan tryptophylquinone biosynthesis. Biochemistry 45:821–828
    [Google Scholar]
  24. Li X., Fu R., Liu A., Davidson V. L. 2008; Kinetic and physical evidence that the diheme enzyme MauG tightly binds to a biosynthetic precursor of methylamine dehydrogenase with incompletely formed tryptophan tryptophylquinone. Biochemistry 47:2908–2912
    [Google Scholar]
  25. Lloyd J. S., De Marco P., Dalton H., Murrell J. C. 1999; Heterologous expression of soluble methane monooxygenase genes in methanotrophs containing only particulate methane monooxygenase. Arch Microbiol 171:364–370
    [Google Scholar]
  26. Nakamura T., Hoaki T., Hanada S., Maruyama A., Kamagata Y., Fuse H. 2007; Soluble and particulate methane monooxygenase gene clusters in the marine methanotroph Methylomicrobium sp. strain NI. FEMS Microbiol Lett 277:157–164
    [Google Scholar]
  27. 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
    [Google Scholar]
  28. Otten M. F., van der Oost J., Reijnders W. N., Westerhoff H. V., Ludwig B., Van Spanning R. J. 2001; Cytochromes c550, c552, and c1 in the electron transport network of Paracoccus denitrificans: redundant or subtly different in function?. J Bacteriol 183:7017–7026
    [Google Scholar]
  29. Pearson A. R., De La Mora-Rey T., Graichen M. E., Wang Y., Jones L. H., Marimanikkupam S., Agger S. A., Grimsrud P. A., Davidson V. L., Wilmot C. M. 2004; Further insights into quinone cofactor biogenesis: probing the role of MauG in methylamine dehydrogenase tryptophan tryptophylquinone formation. Biochemistry 43:5494–5502
    [Google Scholar]
  30. Ronnberg M., Ellfolk N. 1979; Heme-linked properties of Pseudomonas cytochrome c peroxidase. Evidence for non-equivalence of the hemes. Biochim Biophys Acta 581:325–333
    [Google Scholar]
  31. Shimizu H., Schuller D. J., Lanzilotta W. N., Sundaramoorthy M., Arciero D. M., Hooper A. B., Poulos T. L. 2001; Crystal structure of Nitrosomonas europaea cytochrome c peroxidase and the structural basis for ligand switching in bacterial di-heme peroxidases. Biochemistry 40:13483–13490
    [Google Scholar]
  32. Thompson J. D., Gibson T. J., Plewniak F., Jeanmougin F., Higgins D. G. 1997; The clustal_x windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882
    [Google Scholar]
  33. Vargas C., McEwan A. G., Downie J. A. 1993; Detection of c-type cytochromes using enhanced chemiluminescence. Anal Biochem 209:323–326
    [Google Scholar]
  34. Wang Y., Graichen M. E., Liu A., Pearson A. R., Wilmot C. M., Davidson V. L. 2003; MauG, a novel diheme protein required for tryptophan tryptophylquinone biogenesis. Biochemistry 42:7318–7325
    [Google Scholar]
  35. Ward N., Larsen O., Sakwa J., Bruseth L., Khouri H., Durkin A. S., Dimitrov G., Jiang L., Scanlan D. other authors 2004; Genomic insights into methanotrophy: the complete genome sequence of Methylococcus capsulatus (Bath. PLoS Biol 2:e303
    [Google Scholar]
  36. Whittenbury R., Phillips K. C., Wilkinson J. F. 1970; Enrichment, isolation and some properties of methane-utilizing bacteria. J Gen Microbiol 61:205–218
    [Google Scholar]
  37. Wilmot C. M., Davidson V. L. 2009; Uncovering novel biochemistry in the mechanism of tryptophan tryptophylquinone cofactor biosynthesis. Curr Opin Chem Biol 13:469–474
    [Google Scholar]
  38. Zahn J. A., Arciero D. M., Hooper A. B., Coats J. R., DiSpirito A. A. 1997; Cytochrome c peroxidase from Methylococcus capsulatus Bath. Arch Microbiol 168:362–372
    [Google Scholar]
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