1887

Abstract

Methane is oxidized to methanol by the enzyme methane mono-oxygenase (MMO) in methanotrophic bacteria. In previous work, this multicomponent enzyme system has been extensively characterized at the biochemical and molecular level. Copper ions have been shown to irreversibly inhibit MMO activity and , but the effect of copper ions on transcription of the genes encoding the soluble (cytoplasmic) MMO (sMMO) has not previously been investigated. To examine more closely the regulation of bacterial methane oxidation and to determine the role of copper in this process, we have investigated transcriptional regulation of the sMMO gene cluster in the methanotrophic bacterium (Bath). Using Northern blot analysis and primer extension experiments, it was shown that the six ORFs of the sMMO gene cluster are organized as an operon and the transcripts produced upon expression of this operon have been identified. The synthesis of these transcripts was under control of a single copper-regulated promoter, which is as yet not precisely defined.

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1996-05-01
2024-04-19
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References

  1. Anthony C. Bacterial oxidation of methane and methanol. Adv Microb Physiol 1986; 27:113–210
    [Google Scholar]
  2. Bolivar F., Rodrigues R.L., Greene P.J., Betlach M.C., Heyneker H.L., Boyer H.W., Crosa J.H., Falkow S. Construction and characterization of new cloning vehicles II A multipurpose cloning system. Gene 1977; 2:95–113
    [Google Scholar]
  3. Brusseau G.A., Tsien H., -C, Hanson R.S., Wackett L.P. Optimization of trichloroethylene oxidation by methanotrophs and the use of a colorimetric assay to detect soluble methane monooxygenase activity. Biodégradation 1990; 1:19–29
    [Google Scholar]
  4. Cardy D.L.N., Laidler V., Salmond G.P., G & Murrell J.C. Molecular analysis of the methane monooxygenase (MMO) gene cluster of Methylosinus trichosporium OB3b. Mol Microbiol 1991a; 5:335–342
    [Google Scholar]
  5. Cardy D.L.N., Laidler V., Salmond G.P.C., Murrell J.C. The methane monooxygenase gene cluster of Methylosinus trichosporium: cloning and sequencing of the mmoC gene. Arch Microbiol 1991b; 156:477–483
    [Google Scholar]
  6. Chan S.I., Nguyen H.-H.T., Shiemke A.K., Lidstrom M.E. Biochemical and biophysical studies towards characterization of the membrane-associated methane monooxygenase. In Microbial Growth on Cl Compounds 1993 Edited by Murrell J.C., Kelly D.P. Andover: Intercept Press; pp 93–107
    [Google Scholar]
  7. Colby J., Dalton H. Resolution of the methane monooxygenase of Methylococcus capsulatus (Bath) into three components. Biochem J 1978; 171:461–468
    [Google Scholar]
  8. Colby J., Dalton H. Characterization of the second prosthetic group of the flavoenzyme NADH-acceptor reductase (component C) of the methane monooxygenase from Methylococcus capsulatus (Bath). Biochem J 1979; 157:495–497
    [Google Scholar]
  9. Dalton H., Whittenbury R. The acetylene reduction technique as an assay for the nitrogenase activity in the methane-oxidizing bacterium Methylococcus capsulatus strain Bath. Arch Microbiol 1976; 109:147–151
    [Google Scholar]
  10. Dalton H., Prior S.D., Leak D.J., Stanley S. Regulation and control of methane monooxygenase. In Microbial Growth on Cx Compounds. Proceedings of the Ath International Symposium 1984 Edited by Crawford R.L., Hanson R.S. Washington, DC: American Society for Microbiology; pp 75–82
    [Google Scholar]
  11. Dalton H., Wilkins P., Jiang Y. Structure and mechanism of action of the hydroxylase of soluble methane monooxygenase. In Microbial Growth on C1 Compounds 1993 Edited by Murrell J.C., Kelly D.P. Andover: Intercept Press; pp 65–80
    [Google Scholar]
  12. Deretic V., Gill J.F., Chakrabarty A.M. Alginate biosynthesis: a model system for gene regulation and function in Pseudomonas. Biotechnology 1987; 5:469–477
    [Google Scholar]
  13. Dixon R. The xylABC promoter from the Pseudomonas putida TOL plasmid is activated by nitrogen regulatory genes in Escherichia coli. Mol Gen Genet 1986; 203:129–136
    [Google Scholar]
  14. Fox B.G., Froland W.A., Dege J.E., Lipscomb J.D. 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 1989; 264:10023–10033
    [Google Scholar]
  15. Fox B.G., Froland W.A., Jollie D.R., Lipscomb J.D. Methane monooxygenase from Methylosinus trichosporium OB3b. Methods Enzymol 1990; 188:191–202
    [Google Scholar]
  16. Fox B.G., Lin Y., Dege J.E., Lipscomb J.D. Complex formation between the protein components of methane monooxygenase from Methylosinus trichosporium OB3b, identification of sites of component interaction. J Biol Chem 1991; 266:540–550
    [Google Scholar]
  17. Green J., Dalton H. Protein B of the soluble methane monooxygenase from Methylococcus capsulatus (Bath): a novel regulatory protein of enzyme activity. J Biol Chem 1985; 260:15795–15801
    [Google Scholar]
  18. Green J., Prior S.D., Dalton H. Copper ions as inhibitors of protein C of soluble methane monooxygenase Methylococcus capsulatus (Bath). Eur J Biochem 1985; 153:137–144
    [Google Scholar]
  19. Koh S.-G., Bowman J.P., Sayler G.S. Soluble methane monooxygenase production and trichlorethylene degradation by a type I methanotroph, Methjlomonas methanica 68-1. Appl Environ Microbiol 1993; 59:960–967
    [Google Scholar]
  20. Lipscomb J.D. Biochemistry of the soluble methane monooxygenase. Annu Rev Microbiol 1994; 48:371–399
    [Google Scholar]
  21. Liu K.E., Lippard S.J. Redox properties of the hydroxylase component of methane monooxygenase from Methylococcus capsulatus (Bath): effects of protein B, reductase and substrate. J Biol Chem 1991; 266:12836–12839
    [Google Scholar]
  22. De Lorenzo V., Wee S., Herrero M., Nielands J.B. Operator sequences of the aerobactin operon of plasmid ColV-K30 binding the ferric uptake regulation (fur) repressor. J Bacteriol 1987; 169:2624–2630
    [Google Scholar]
  23. Lund J., Dalton H. Further characterization of the FAD and Fe2S2 redox centres of component C, the NADH: acceptor reductase of the soluble methane monooxygenase of Methylococcus capsulatus (Bath). Eur J Biochem 1985; 147:291–296
    [Google Scholar]
  24. Lund J., Woodland M.P., Dalton H. Electron transfer reactions in the soluble methane monooxygenase of Methylococcus capsulatus (Bath). Eur J Biochem 1985; 147:297–305
    [Google Scholar]
  25. Maniatis T., Fritsch E.F., Sambrook J. Molecular Cloning: a Eaboratory Manual 1982 Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  26. Miller J. Experiments in Molecular Genetics 1972 Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  27. Murrell J.C. Genetics and molecular biology of methano-trophs. FEMS Microbiol Rev 1992; 88:233–248
    [Google Scholar]
  28. Murrell J.C. Molecular genetics of methane oxidation. Biodégradation 1994; 5:145–159
    [Google Scholar]
  29. Nakajima T., Uchiyama H., Yagi O., Nakahara T. Purification and properties of a soluble methane monooxygenase from Methylocystis sp M. Biosci Biotech Biochem 1992; 56:736–740
    [Google Scholar]
  30. Nguyen H.-H., T., Shiemke A.K., Jacobs S.J., Hales B.J., Lidstrom M.E., Chan S.I. The nature of the copper ions in the membranes containing the particulate methane monooxygenase from Methylococcus capsulatus (Bath). J Biol Chem 1994; 269:14995–15005
    [Google Scholar]
  31. Pilkington S., J. & Dalton H. Purification and characterization of the soluble methane monooxygenase from Methylosinus sporium 5 demonstrates the highly conserved nature of this enzyme in methanotrophs. FEMS Microbiol Eett 1991; 78:103–108
    [Google Scholar]
  32. Prior S.D., Dalton H. The effect of copper ions on membrane content and methane monooxygenase activity in methanol-grown cells of Methylococcus capsulatus (Bath). J Gen Microbiol 1985; 131:155–163
    [Google Scholar]
  33. Sanger F., Nicklen S., Coulsen A.R. DNA sequencing with chain terminating inhibitors. Proc Natl Acad Sci USA 1977; 74:5463–5467
    [Google Scholar]
  34. Scott D., Brannan J., Higgins I.J. The effect of growth conditions on intracytoplasmic membranes and methane monooxygenase activities in Methylosinus trichosporium OB3b. J Gen Microbiol 1981a; 125:63–72
    [Google Scholar]
  35. Scott D., Best D.J., Higgins I.J. Intracytoplasmic membranes in oxygen-limited chemostat cultures of Methylosinus trichosporium OB3b: biocatalystic implication of physiologically balanced growth. Biotechnol Eett 1981b; 3:641–644
    [Google Scholar]
  36. Silver S., Walderhaug M. Gene regulation of plasmid-and chromosome-determined inorganic ion transport in bacteria. Microbiol Rev 1992; 56:195–228
    [Google Scholar]
  37. Stainthorpe A.C., Murrell J.G., Salmond G.P.G., Dalton H., Lees V. Molecular analysis of methane monooxygenase from Methylococcus capsulatus (Bath). Arch Microbiol 1989; 152:154–159
    [Google Scholar]
  38. Stainthorpe A.G., Lees V., Salmond G.P.G., Dalton H., Murrell J.G. The methane monooxygenase gene cluster of Methylococcus capsulatus (Bath). Gene 1990; 91:27–34
    [Google Scholar]
  39. Stanley S.H., Prior S.D., Leak D.J., Dalton H. Copper stress underlies the fundamental change in intracellular location of methane monooxygenase in methane-oxidizing organisms: studies in batch and continuous cultures. Biotechnol Eett 1983; 5:487–492
    [Google Scholar]
  40. Stirling D.I., Dalton H. Properties of the methane monooxygenase from extracts of Methylosinus trichosporium OB3b and evidence for its similarity to the enzyme from Methylococcus capsulatus (Bath). Eur J Biochem 1979; 96:205–212
    [Google Scholar]
  41. Tsien H., -G, Brusseau G.A., Hanson R.S., Wacket L.P. Biodégradation of trichlorethylene by Methylosinus trichosporium OB3b. Appi Environ Microbiol 1989; 55:3155–3161
    [Google Scholar]
  42. Woodland M.P., 8. Dalton H. Purification and characterization of Component A of the methane monooxygenase from Methylococcus capsulatus (Bath). J Biol Chem 1989; 259:53–59
    [Google Scholar]
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