1887

Abstract

The key enzyme in methane metabolism is methane monooxygenase (MMO), which catalyses the oxidation of methane to methanol. Some methanotrophs, including (Bath), possess two distinct MMOs. The level of copper in the environment regulates the biosynthesis of the MMO enzymes in these methanotrophs. Under low-copper conditions, soluble MMO (sMMO) is expressed and regulation takes place at the level of transcription. The structural genes of sMMO were previously identified as , and . Putative transcriptional start sites, containing a - and a -dependent motif, were identified in the 5′ region of . The promoter region of was mapped using truncated 5′ end regions fused to a promoterless green fluorescent protein gene. A 9·5 kb region, adjacent to the sMMO structural gene cluster, was analysed. Downstream (3′) from the last gene of the operon, , four ORFs were found, , , and . shows significant identity to the large subunit of the bacterial chaperonin gene, . In the opposite orientation, two genes, and , showed significant identity to two-component sensor–regulator system genes. Next to , a gene encoding a putative -dependent transcriptional activator, was identified. The and genes were mutated by marker-exchange mutagenesis and the effects of these mutations on the expression of sMMO was investigated. sMMO transcription was impaired in both mutants. These results indicate that and are essential for the expression of sMMO in (Bath).

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.26061-0
2003-07-01
2020-10-01
Loading full text...

Full text loading...

/deliver/fulltext/micro/149/7/mic1491785.html?itemId=/content/journal/micro/10.1099/mic.0.26061-0&mimeType=html&fmt=ahah

References

  1. Anantharaman V., Koonin V. E., Aravind L.. 2001; Regulatory potential, phylogenetic distribution and evolution of ancient, intracellular small-molecule-binding domains. J Mol Biol307:1271–1292
    [Google Scholar]
  2. Aravind L., Ponting P. C.. 1997; The GAF Domain: an evolutionary link between diverse phototransducing proteins. Trends Biochem Sci22:458–459
    [Google Scholar]
  3. Bauer E. C., Elsen S., Bird H. T.. 1999; Mechanisms for redox control of gene expression. Annu Rev Microbiol53:495–523
    [Google Scholar]
  4. Bilwes A. M., Alex L. A., Crane B. R., Simon M. I.. 1999; Structure of CheA, a signal-transducing histidine kinase. Cell96:131–141
    [Google Scholar]
  5. Bourret R. B., Hess J. F., Borkovich A. B., Pakula A. A., Simon M. I.. 1989; Protein phosphorylation in chemotaxis and two-component regulatory systems of bacteria. J Biol Chem264:7085–7088
    [Google Scholar]
  6. Braig K.. 1998; Chaperonins. Curr Opin Struct Biol8:159–165
    [Google Scholar]
  7. Buck M., Gallegos M.-T., Studholme D. J., Guo Y., Gralla J. D.. 2000; The bacterial enhancer-dependent σ 54 ( σ N) transcription factor. J Bacteriol182:4129–4136
    [Google Scholar]
  8. Burrows K., Cornish A., Scott D., Higgins I.. 1984; Substrate specificities of the soluble and particulate methane monooxygenase of Methylosinus trichosporium OB3b. J Gen Microbiol130:3327–3333
    [Google Scholar]
  9. Collado-Vides J., Magasanik B., Gralla D. J.. 1991; Control site location and transcriptional regulation in Escherichia coli . Microbiol Rev55:371–394
    [Google Scholar]
  10. Dennis J. J., Zylstra G. J.. 1998; Plasposons: modular self-cloning mini-transposon derivatives for rapid genetic analysis of gram-negative bacterial genomes. Appl Environ Microbiol64:2710–2715
    [Google Scholar]
  11. Forstner U., Wittman G. T. W.. 1979; Metal Pollution in the Aquatic Environment New York: Springer;
    [Google Scholar]
  12. 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 the two type II methanotrophs. Appl Environ Microbiol66:966–975
    [Google Scholar]
  13. Green J., Prior S. D., Dalton H.. 1985; Copper ions as inhibitors of protein C of soluble methane monooxygenase of Methylococcus capsulatus (Bath). Eur J Biochem153:137–144
    [Google Scholar]
  14. Hanahan D.. 1983; Studies on transformation of Escherichia coli with plasmid. J Mol Biol166:557–558
    [Google Scholar]
  15. Hanson S. R., Hanson E. T.. 1996; Methanotrophic bacteria. Microbiol Rev60:439–471
    [Google Scholar]
  16. 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 Bacteriol172:6557–6567
    [Google Scholar]
  17. Humberto B., Valderama B., Morett E.. 1999; Compilation and analysis of σ 54-dependent promoter sequences. Nucleic Acid Res27:4305–4313
    [Google Scholar]
  18. Jahng D., Wood T. K.. 1996; Metal ions and chloramphenicol inhibition of soluble methane monooxygenase from Methylosinus trichosporium OB3b. Appl Microbiol Biotechnol45:744–749
    [Google Scholar]
  19. Koch K. A., Pena M. M. O., Thiele D. J.. 1997; Copper-binding motifs in catalysis, transport, detoxification and signalling. Chem Biol4:549–560
    [Google Scholar]
  20. Kovach E. M., Elzer H. P., Hill S. D., Robertson T. G., Farris A. M., Roop M. R., Peterson M. K.. 1995; Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene166:175–176
    [Google Scholar]
  21. Lemos J. A. C., Chen Y. M., Burne R. A.. 2001; Genetic and physiological analysis of the groE operon and role of the HrcA repressor in stress regulation and acid tolerance in Streptococcus mutans . J Bacteriol183:6074–6084
    [Google Scholar]
  22. Lipscomb J. D.. 1994; Biochemistry of soluble methane monooxygenase. Annu Rev Microbiol48:371–399
    [Google Scholar]
  23. Miller W. G., Leveau J. H., Lindow S. E.. 2000; Improved gfp and inaZ broad-host-range promoter-probe vectors. Mol Plant Microbe Interact 13:1243–1250
    [Google Scholar]
  24. Murrell J. C., Gilbert B., McDonald R. I.. 2000; Molecular biology and regulation of methane monooxygenase. Arch Microbiol173:325–332
    [Google Scholar]
  25. Nielsen A. K.. 1996; Transcriptional regulation of soluble and particulate methane monooxygenase genes in the methanotrophic bacteria Methylococcus capsulatus (Bath) and Methylosinus trichosporium OB3b PhD thesis, Odense University; Denmark:
    [Google Scholar]
  26. 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 Microbiol25:399–409
    [Google Scholar]
  27. Phelps A. P., Agarwal K. S., Speitel E. G., Georgiou G.. 1992; Methylosinus trichosporium OB3b mutants having constitutive expression of soluble methane monooxygenase in the presence of high levels of copper. Appl Environ Microbiol58:3701–3708
    [Google Scholar]
  28. Ponting P. C., Aravind L.. 1997; PAS: a multifunctional domain family comes to light. Curr Biol7:R674–R677
    [Google Scholar]
  29. Ranson A. N., White E. H., Saibil R. H.. 1998; Chaperonins. Biochem J333:233–242
    [Google Scholar]
  30. Reitzer L., Schneider B. L.. 2001; Metabolic context and possible physiological themes of σ 54 dependent genes in Escherichia coli . Microbiol Mol Biol Rev65:422–444
    [Google Scholar]
  31. Robinson L. V., Buckler D. R., Stock M. A.. 2000; A tale of two components: novel kinase and a regulatory switch. Nat Struct Biol7:626–633
    [Google Scholar]
  32. Sambrook J., Fritsch E. F., Maniatis T.. 1989; Molecular Cloning: a Laboratory Manual , 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  33. Schäfer A., Tauch A., Jäger W., Lalinowski J., Thierbach G., Pühler A.. 1994; Small mobilisable multi-purpose cloning vector derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum . Gene145:69–73
    [Google Scholar]
  34. Segal R., Ron E. Z.. 1996; Regulation and organization of the groE and dnaK operons in eubacteria. FEMS Microbiol Lett15:1–10
    [Google Scholar]
  35. Semrau J. D., Chistoserdov A., Lebron J.. 7 other authors 1995; Particulate methane monooxygenase genes in methanotrophs. J Bacteriol177:3071–3079
    [Google Scholar]
  36. 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 Microbiol65:5198–5206
    [Google Scholar]
  37. Siegle A. D., Campbell L., Hu C. J.. 2000; Green fluorescent protein as a reporter of transcription activity in a prokaryotic system. Methods Enzymol305:499–513
    [Google Scholar]
  38. Sonnhammer E. L. L., von Heijne G., Krogh A.. others 1998; A hidden Markov model for predicting transmembrane helices in protein sequences. In Proceedings of the Sixth International Conference on Intelligent Systems for Molecular Biology pp 175–182 Edited by Glasgow I. N.. Menlo Park, CA: AAAI Press;
    [Google Scholar]
  39. 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. Microbiology149:1771–1784
    [Google Scholar]
  40. Stainthorpe A. C., Murrell J. C., Salmond G. P. C., Dalton H., Lees V.. 1989; Molecular analysis of methane monooxygenase from Methylococcus capsulatus (Bath). Arch Microbiol152:154–159
    [Google Scholar]
  41. Stainthorpe A. C., Lees V., Salmond G. P. C., Dalton H., Murrell J. C.. 1990; The methane monooxygenase gene cluster from Methylococcus capsulatus (Bath). Gene91:27–34
    [Google Scholar]
  42. 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. Biotechnol Lett5:487–492
    [Google Scholar]
  43. Stock M. A., Robinson L. V., Goudreau N. P.. 2000; Two-component signal transduction. Annu Rev Biochem69:183–215
    [Google Scholar]
  44. 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. Microbiology145:1235–1244
    [Google Scholar]
  45. Stolyar S., Franke M., Lidstrom M. E.. 2001; Expression of individual copies of Methylococcus capsulatus Bath particulate methane monooxygenase genes. J Bacteriol183:1810–1812
    [Google Scholar]
  46. Taylor L. B., Zhulin B. I., Johnson S. M.. 1999; Aerotaxis and other energy-sensing behaviour in bacteria. Annu Rev Microbiol53:103–128
    [Google Scholar]
  47. Thompson J. D., Gibson T. J., Plewniak F., Jeanmougin F., Higgins D. G.. 1997; The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res24:4876–4882
    [Google Scholar]
  48. West H. A., Stock M. A.. 2001; Histidine kinases and response regulator proteins in two-component signaling systems. Trends Biochem Sci26:369–376
    [Google Scholar]
  49. Whittenbury R., Dalton H.. 1981; The methylotrophic bacteria. In The Prokaryotes: a Handbook on Habitats, Isolation, and Identification of Bacteria pp 894–902 Edited by Starr M. P. Berlin, Heidelberg: Springer;
    [Google Scholar]
  50. Whittenbury R., Philips K. C., Wilkinson J. F.. 1970; Enrichment, isolation and some properties of methane utilizing bacteria. J Gen Microbiol61:205–218
    [Google Scholar]
  51. Zahn J. A., Dispirito A. A.. 1996; Membrane-associated methane monooxygenase from Methylococcus capsulatus (Bath). J Bacteriol178:1018–1029
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.26061-0
Loading
/content/journal/micro/10.1099/mic.0.26061-0
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