1887

Abstract

The soluble methane monooxygenase (sMMO) is a key enzyme for methane oxidation, and is found in only some methanotrophs, including 5. sMMO expression is regulated at the level of transcription from a promoter by a copper-switch, and is only expressed when the copper-to-biomass ratio during growth is low. Extensive phylogenetic and genetic analyses of sMMOs and other soluble di-iron monooxygenases reveal that these enzymes have only been acquired relatively recently through horizontal gene transfer. In this study, further evidence of horizontal gene transfer was obtained, through cloning and sequencing of the genes encoding the sMMO enzyme complex plus the regulatory genes and , and identification of a duplicate copy of the gene in . encodes the subunit of the hydroxylase of the sMMO enzyme, which constitutes the active site ( Prior & Dalton, 1985 ). The genes were characterized at the molecular and biochemical levels. Although both copies were transcribed, only copy 1 was essential for sMMO activity. Construction of an sMMO mutant by marker-exchange mutagenesis gave some possible insights into the role of the water-soluble pigment in siderophore-mediated iron acquisition. Finally, the amenability of to genetic manipulation was demonstrated by complementing the sMMO mutant by heterologous expression of sMMO genes from OB3b and (Bath), and it was shown that could be used as an alternative model organism for molecular analysis of MMO regulation.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.29031-0
2006-10-01
2019-11-17
Loading full text...

Full text loading...

/deliver/fulltext/micro/152/10/2931.html?itemId=/content/journal/micro/10.1099/mic.0.29031-0&mimeType=html&fmt=ahah

References

  1. Anthony, C. ( 1982; ). The Biochemistry of the Methylotrophs, pp. 1–41. New York: Academic Press.
  2. Arp, D. J., Sayavedra-Soto, L. A. & Hommes, N. G. ( 2002; ). Molecular biology and biochemistry of ammonia oxidation by Nitrosomonas europaea. Arch Microbiol 178, 250–255.[CrossRef]
    [Google Scholar]
  3. Barrios, H., Valderrama, B. & Morett, E. ( 1999; ). Compilation and analysis of σ 54-dependent promoter sequences. Nucleic Acids Res 27, 4305–4313.[CrossRef]
    [Google Scholar]
  4. Brusseau, G., Tsien, H., Hanson, R. & Wackett, L. ( 1990; ). Optimization of trichloroethylene oxidation by methanotrophs and the use of a colorimetric assay to detect soluble methane monooxygenase activity. Biodegradation 1, 19–29.[CrossRef]
    [Google Scholar]
  5. Cardy, D. L. N., Laidler, V., Salmond, G. P. C. & Murrell, J. C. ( 1991a; ). Molecular analysis of the methane monooxygenase (mmo) gene-cluster of Methylosinus trichosporium OB3b. Mol Microbiol 5, 335–342.[CrossRef]
    [Google Scholar]
  6. Cardy, D. L. N., Laidler, V., Salmond, G. P. C. & Murrell, J. C. ( 1991b; ). The methane monooxygenase gene cluster of Methylosinus trichosporium – cloning and sequencing of the mmoC gene. Arch Microbiol 156, 477–483.
    [Google Scholar]
  7. Colby, J. & Dalton, H. ( 1976; ). Some properties of a soluble methane mono-oxygenase from Methylococcus capsulatus strain Bath. Biochem J 157, 495–497.
    [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.[CrossRef]
    [Google Scholar]
  9. Dedysh, S. N., Liesack, W., Khmelenina, V. N., Suzina, N. E., Trotsenko, Y. A., Semrau, J. D., Bares, A. M., Panikov, N. S. & Tiedje, J. M. ( 2000; ). Methylocella palustris gen. nov., sp nov., a new methane- oxidizing acidophilic bacterium from peat bogs, representing a novel subtype of serine-pathway methanotrophs. Int J Syst Evol Microbiol 50, 955–969.[CrossRef]
    [Google Scholar]
  10. Dedysh, S. N., Berestovskaya, Y. Y., Vasylieva, L. V., Belova, S. E., Khmelenina, V. N., Suzina, N. E., Trotsenko, Y. A., Liesack, W. & Zavarzin, G. A. ( 2004; ). Methylocella tundrae sp. nov., a novel methanotrophic bacterium from acidic tundra peatlands. Int J Syst Evol Microbiol 54, 151–156.[CrossRef]
    [Google Scholar]
  11. Dennis, J. J. & Zylstra, G. J. ( 1998; ). Plasposons: modular self-cloning minitransposon derivatives for rapid genetic analysis of gram-negative bacterial genomes. Appl Environ Microbiol 64, 2710–2715.
    [Google Scholar]
  12. Dunfield, P. F., Khmelenina, V. N., Suzina, N. E., Trotsenko, Y. A. & Dedysh, S. N. ( 2003; ). Methylocella silvestris sp nov., a novel methanotroph isolated from an acidic forest cambisol. Int J Syst Evol Microbiol 53, 1231–1239.[CrossRef]
    [Google Scholar]
  13. Elango, N., Radhakrishnan, R., Froland, W. A., Wallar, B. J., Earhart, C. A., Lipscomb, J. D. & Ohlendorf, D. H. ( 1997; ). Crystal structure of the hydroxylase component of methane monooxygenase from Methylosinus trichosporium OB3b. Protein Sci 6, 556–568.
    [Google Scholar]
  14. Fox, B. G., Froland, W. A., Dege, J. E. & Lipscomb, J. D. ( 1989; ). Methane monooxygenase from Methylosinus trichosporium OB3b. Purification and properties of a three-component system with high specific activity from a type II methanotroph. J Biol Chem 264, 10023–10033.
    [Google Scholar]
  15. Gilbert, B., McDonald, I. R., Finch, R., Stafford, G. P., Nielsen, A. K. & Murrell, J. C. ( 2000; ). Molecular analysis of the pmo (particulate methane monooxygenase) operons from two type II methanotrophs. Appl Environ Microbiol 66, 966–975.[CrossRef]
    [Google Scholar]
  16. Green, J. & Dalton, H. ( 1985; ). Protein-B of soluble methane monooxygenase from Methylococcus capsulatus (Bath) – a novel regulatory protein of enzyme activity. J Biol Chem 260, 5795–5801.
    [Google Scholar]
  17. Herrero, M., de Lorenzo, V. & Timmis, K. N. ( 1990; ). Transposon vectors containing non-antibiotic resistance selection markers for cloning and stable chromosomal insertion of foreign genes in gram-negative bacteria. J Bacteriol 172, 6557–6567.
    [Google Scholar]
  18. Hutchens, E., Radajewski, S., Dumont, M. G., McDonald, I. R. & Murrell, J. C. ( 2004; ). Analysis of methanotrophic bacteria in Movile Cave by stable isotope probing. Environ Microbiol 6, 111–120.
    [Google Scholar]
  19. Kim, H. J., Graham, D. W., DiSpirito, A. A., Alterman, M. A., Galeva, N., Larive, C. K., Asunskis, D. & Sherwood, P. M. ( 2004; ). Methanobactin, a copper-acquisition compound from methane-oxidizing bacteria. Science 305, 1612–1615.[CrossRef]
    [Google Scholar]
  20. Leahy, J. G., Batchelor, P. J. & Morcomb, S. M. ( 2003; ). Evolution of the soluble diiron monooxygenases. FEMS Microbiol Rev 27, 449–479.[CrossRef]
    [Google Scholar]
  21. Lidstrom, M. E. & Wopat, A. E. ( 1984; ). Plasmids in methanotrophic bacteria: isolation, characterization and DNA hybridization analysis. Arch Microbiol 140, 27–33.[CrossRef]
    [Google Scholar]
  22. 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.[CrossRef]
    [Google Scholar]
  23. Lund, J., Woodland, M. P. & Dalton, H. ( 1985; ). Electron transfer reactions in the soluble methane monooxygenase of Methylococcus capsulatus (Bath). Eur J Biochem 147, 297–305.[CrossRef]
    [Google Scholar]
  24. Marmur, J. ( 1961; ). A procedure for the isolation of deoxyribonucleic acid from microorganisms. J Mol Biol 3, 208–218.[CrossRef]
    [Google Scholar]
  25. Martin, H. ( 1994; ). Molecular genetics of methane oxidation in Methylosinus trichosporium OB3b. PhD thesis, University of Warwick.
  26. Martin, H. & Murrell, J. C. ( 1995; ). Methane monooxygenase mutants of Methylosinus trichosporium constructed by marker-exchange mutagenesis. FEMS Microbiol Lett 127, 243–248.[CrossRef]
    [Google Scholar]
  27. McDonald, I. R., Uchiyama, H., Kambe, S., Yagi, O. & Murrell, J. C. ( 1997; ). The soluble methane monooxygenase gene cluster of the trichloroethylene-degrading methanotroph Methylocystis sp. strain M. Appl Environ Microbiol 63, 1898–1904.
    [Google Scholar]
  28. Murrell, J. C., McDonald, I. R. & Gilbert, B. ( 2000; ). Regulation of expression of methane monooxygenases by copper ions. Trends Microbiol 8, 221–225.[CrossRef]
    [Google Scholar]
  29. Nguyen, H. H. T., Elliott, S. J., Yip, J. H. K. & Chan, S. I. ( 1998; ). The particulate methane monooxygenase from Methylococcus capsulatus (Bath) is a novel copper-containing three-subunit enzyme – Isolation and characterization. J Biol Chem 273, 7957–7966.[CrossRef]
    [Google Scholar]
  30. Nielsen, A. K., Gerdes, K., Degn, H. & Murrell, J. C. ( 1996; ). Regulation of bacterial methane oxidation: transcription of the soluble methane monooxygenase operon of Methylococcus capsulatus (Bath) is repressed by copper ions. Microbiology 142, 1289–1296.[CrossRef]
    [Google Scholar]
  31. 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.[CrossRef]
    [Google Scholar]
  32. Pilkington, S. J. & Dalton, H. ( 1991; ). Purification and characterization of the soluble methane monooxygenase from Methylosinus sporium 5 demonstrates the highly conserved nature of this enzyme in methanotrophs. FEMS Microbiol Lett 78, 103–108.[CrossRef]
    [Google Scholar]
  33. Prior, S. D. & Dalton, H. ( 1985; ). Acetylene as a suicide substrate and active site probe for methane monooxygenase from Methylococcus capsulatus (Bath). FEMS Microbiol Lett 29, 105–109.[CrossRef]
    [Google Scholar]
  34. Rosenzweig, A. C., Frederick, C. A., Lippard, S. J. & Nordlund, P. ( 1993; ). Crystal structure of a bacterial nonheme iron hydroxylase that catalyzes the biological oxidation of methane. Nature 366, 537–543.[CrossRef]
    [Google Scholar]
  35. Sambrook, J., Fritsch, E. F. & Maniatis, T. ( 1989; ). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  36. Schafer, A., Tauch, A., Jager, W., Kalinowski, J., Thierbach, G. & Puhler, A. ( 1994; ). Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum. Gene 145, 69–73.[CrossRef]
    [Google Scholar]
  37. Schäfer, H., McDonald, I. R., Nightingale, P. D. & Murrell, J. C. ( 2005; ). Evidence for presence of CmuA methyltransferase pathway in novel marine methyl halide-oxidizing isolates. Environ Microbiol 7, 839–852.[CrossRef]
    [Google Scholar]
  38. Schalk, I. J., Yue, W. W. & Buchanan, S. K. ( 2004; ). Recognition of iron-free siderophores by TonB-dependent iron transporters. Mol Microbiol 54, 14–22.[CrossRef]
    [Google Scholar]
  39. Schottel, J. L., Sninsky, J. J. & Cohen, S. N. ( 1984; ). Effects of alterations in the translation control region on bacterial gene expression: use of cat gene constructs transcribed from the lac promoter as a model system. Gene 28, 177–193.[CrossRef]
    [Google Scholar]
  40. Semrau, J. D., Chistoserdov, A., Lebron, J. & 7 other authors ( 1995; ). Particulate methane monooxygenase genes in methanotrophs. J Bacteriol 177, 3071–3079.
    [Google Scholar]
  41. Shigematsu, T., Hanada, S., Eguchi, M., Kamagata, Y., Kanagawa, T. & Kurane, R. ( 1999; ). Soluble methane monooxygenase gene clusters from trichloroethylene-degrading Methylomonas sp strains and detection of methanotrophs during in-situ bioremediation. Appl Environ Microbiol 65, 5198–5206.
    [Google Scholar]
  42. Shine, J. & Dalgarno, L. ( 1974; ). The 3′-terminal sequence of Escherichia coli 16S ribosomal RNA: complementarity to nonsense triplets and ribosome binding sites. Proc Natl Acad Sci U S A 71, 1342–1346.[CrossRef]
    [Google Scholar]
  43. Shingler, V. ( 1996; ). Signal sensing by σ 54-dependent regulators: derepression as a control mechanism. Mol Microbiol 19, 409–416.[CrossRef]
    [Google Scholar]
  44. Sluis, M. K., Sayavedra-Soto, L. A. & Arp, D. J. ( 2002; ). Molecular analysis of the soluble butane monooxygenase from ‘Pseudomonas butanovora’. Microbiology 148, 3617–3629.
    [Google Scholar]
  45. Smith, T. J. & Dalton, H. ( 2004; ). Biocatalysis by methane monooxygenase and its implications for the petroleum industry. Studies in Surface Science and Catalysis 151, 177–192.
    [Google Scholar]
  46. Stafford, G. P., Scanlan, J., McDonald, I. R. & Murrell, J. C. ( 2003; ). rpoN, mmoR and mmoG, genes involved in regulating the expression of soluble methane monooxygenase in Methylosinus trichosporium OB3b. Microbiology 149, 1771–1784.[CrossRef]
    [Google Scholar]
  47. Stainthorpe, A. C., Murrell, J. C., Salmond, G. P., Dalton, H. & Lees, V. ( 1989; ). Molecular analysis of methane monooxygenase from Methylococcus capsulatus (Bath). Arch Microbiol 152, 154–159.[CrossRef]
    [Google Scholar]
  48. Stainthorpe, A. C., Lees, V., Salmond, G. P. C., Dalton, H. & Murrell, J. C. ( 1990; ). The methane monooxygenase gene cluster of Methylococcus capsulatus (Bath). Gene 91, 27–34.[CrossRef]
    [Google Scholar]
  49. Stanley, S. H., Prior, S. D., Leak, D. J. & Dalton, H. ( 1983; ). Copper stress underlies the fundamental change in intracellular location of methane monooxygenase in methane oxidizing organisms: studies in batch and continuous cultures. Biotechnology Lett 5, 487–492.[CrossRef]
    [Google Scholar]
  50. Stolyar, S., Costello, A. M., Peeples, T. L. & Lidstrom, M. E. ( 1999; ). Role of multiple gene copies in particulate methane monooxygenase activity in the methane-oxidizing bacterium Methylococcus capsulatus Bath. Microbiology 145, 1235–1244.[CrossRef]
    [Google Scholar]
  51. Theisen, A. R., Ali, M. H., Radajewski, S., Dumont, M. G., Dunfield, P. F., McDonald, I. R., Dedysh, S. N., Miguez, C. B. & Murrell, J. C. ( 2005; ). Regulation of methane oxidation in the facultative methanotroph Methylocella silvestris BL2. Mol Microbiol 58, 682–692.[CrossRef]
    [Google Scholar]
  52. Vieira, J. & Messing, J. ( 1982; ). The pUC plasmids, an M13mp7-derived system for insertion mutagenesis and sequencing with synthetic universal primers. Gene 19, 259–268.[CrossRef]
    [Google Scholar]
  53. Ward, N., Larsen, O., Sakwa, J. & 35 other authors ( 2004; ). Genomic insights into methanotrophy: the complete genome sequence of Methylococcus capsulatus (Bath). PLoS Biol 2, e303.[CrossRef]
    [Google Scholar]
  54. Whittenbury, R., Phillips, K. C. & Wilkinson, J. F. ( 1970; ). Enrichment, isolation and some properties of methane-utilizing bacteria. J Gen Microbiol 61, 205–218.[CrossRef]
    [Google Scholar]
  55. Woodland, M. P. & Dalton, H. ( 1984; ). Purification of component A of the soluble methane monooxygenase of Methylococcus capsulatus (Bath) by high-pressure gel permeation chromatography. Anal Biochem 139, 459–462.[CrossRef]
    [Google Scholar]
  56. Zahn, J. A. & DiSpirito, A. A. ( 1996; ). Membrane-associated methane monooxygenase from Methylococcus capsulatus (Bath). J Bacteriol 178, 1018–1029.
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.29031-0
Loading
/content/journal/micro/10.1099/mic.0.29031-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error