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Volume 143, Issue 8

Association of newly discovered IS elements with the dichloromethane utilization genes of methylotrophic bacteria Free

Abstract

Summary: Dichloromethane (DCM) dehalogenases enable facultative methylotrophic bacteria to utilize DCM as sole carbon and energy source. DCM-degrading aerobic methylotrophic bacteria expressing a type A DCM dehalogenase were previously shown to share a conserved 4.2 kb HI DNA fragment containing the dehalogenase structural gene, , and , the gene encoding a putative regulatory protein. Sequence analysis of a 10 kb DNA fragment including this region led to the identification of three types of insertion sequences identified as IS , IS and IS, and also two ORFs, and , of unknown function. Two identical copies of element IS flank the conserved 4.2 kb fragment as a direct repeat. The occurrence of these newly identified IS elements was shown to be limited to DCM-utilizing methylotrophs containing a type A DCM dehalogenase. The organization of the corresponding regions in 12 DCM-utilizing strains was examined by hybridization analysis using IS-specific probes. Six different groups could be defined on the basis of the occurrence, position and copy number of IS sequences. All groups shared a conserved 5.6 kb core region with and as well as IS One group of strains including sp. DM1 contained two copies of this conserved core region. The high degree of sequence conservation observed within the genomic region responsible for DCM utilization and the occurrence of clusters of insertion sequences in the vicinity of the genes suggest that a transposon is involved in the horizontal transfer of the DCM-utilization character among methylotrophic bacteria.

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  • Accepted:
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  • Published Online:
Keyword(s): dehalogenase , dichloromethane , IS element and methylotrophic bacteria
© Society for General Microbiology 1997
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1997-08-01
2024-04-20
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References

  1. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. 1990; Basic local alignment search tool. J Mol Biol 215:403–410
     [Google Scholar]
  2. Ausubel F. M., Brent R., Kingston R. E., Moore D. D., Seidman J. G., Smith J. A., Struhl K. 1997 Current Protocols in Molecular Biology New York: Greene Publishing Associates & Wiley;
     [Google Scholar]
  3. Bader R., Leisinger T. 1994; Isolation and characterization of the Methylophilus sp. strain DM11 gene encoding dichloromethane dehalogenase/glutathione S-transferase. J Bacteriol 176:3466–3473
     [Google Scholar]
  4. Brunner W. B., Staub D., Leisinger T. 1980; Bacterial degradation of dichloromethane. Appl Environ Microbiol 40:950–958
     [Google Scholar]
  5. Chandler M., Fayet O. 1993; Translational frameshifting in the control of transposition in bacteria. Mol Microbiol 7:497–503
     [Google Scholar]
  6. Chen C. W., Yu T.-W., Chung H.-M., Chou C.-F. 1992; Discovery and characterization of a new transposable element, Tn4811, in Streptomyces lividans 66. . J Bacteriol 174:7762–7769
     [Google Scholar]
  7. Coque J. J. R., Enguita F. J., Martin J. F., Liras P. 1995; A two-protein component 7α-cephem-methyloxylase encoded by two genes of the cephamycin C cluster converts cephalosporin C to 7-methoxycephalosporin C. J Bacteriol 177:2230–2235
     [Google Scholar]
  8. Coucheron D. H. 1993; A family of IS1031 elements in the genome of Acetobacter xylinum: nucleotide sequences and strain distribution. Mol Microbiol 9:211–218
     [Google Scholar]
  9. Daube G., Simon P., Kaeckenbeeck A. 1993; IS1151, an IS-like element of Clostridium perfringens. . Nucleic Acids Res 21:352
     [Google Scholar]
  10. De Meirsman C., Van Soom C., Verreth C., Van Gool A., Vanderleyden J. 1990; Nucleotide sequence analysis of IS427 and its target sites in Agrobacterium tumefaciens T37. Plasmid 24:227–234
     [Google Scholar]
  11. Doronina N. V., Braus-Stromeyer S. A., Leisinger T., Trotsenko Y. A. 1995; Isolation and characterization of a new facultatively methylotrophic bacterium: description of Methylorhabdus multivorans, gen.nov., sp.nov. Syst Appl Microbiol 18:92–98
     [Google Scholar]
  12. Doronina N. V., Sokolov A. P., Trotsenko Y. A. 1996; Isolation and initial characterization of aerobic chloromethane-utilizing bacteria. FEMS Microbiol Lett 142:179–183
     [Google Scholar]
  13. Eisen J. A., Benito M.-I., Walbot V. 1994; Sequence similarity of putative transposases links the maize Mutator autonomous element and a group of bacterial insertion sequences. Nucleic Acids Res 22:2634–2636
     [Google Scholar]
  14. Engler-Blum G., Meier M., Frank J., Müller G. A. 1993; Reduction of background problems in nonradioactive Northern and Southern blot analyses enables higher sensitivity than 32P-based hybridizations. Anal Biochem 210:235–244
     [Google Scholar]
  15. Farabaugh P. J. 1996; Programmed translational frameshifting. Microbiol Rev 60:103–134
     [Google Scholar]
  16. Ferrante A. A., Lessie T. G. 1991; Nucleotide sequence of IS402 from Pseudomonas cepacia. . Gene 102:143–144
     [Google Scholar]
  17. Galas D. J., Chandler M. 1989; Bacterial insertion sequences. . In Mobile DNA pp. 109–162 . Edited by Berg D. E., Howe M. M. Washington, DC: American Society of Microbiology;
     [Google Scholar]
  18. Gälli R. 1986 Optimierung des mikrobiellen Abbaus von Dichlormethan in einem Wirbelschicht-Bioreaktor Dissertation, ETH Zürich.
    [Google Scholar]
  19. Gälli R., Leisinger T. 1985; Specialized bacterial strains for the removal of dichloromethane from industrial waste. Conserv Recycl 8:91–100
     [Google Scholar]
  20. Gälli R., Leisinger T. 1988; Plasmid analysis and cloning of the dichloromethane-utilization genes of Methylobacterium sp. DM4. J Gen Microbiol 134:943–952
     [Google Scholar]
  21. Green P. N. 1992; The genus Methylobacterium. . In The Procaryotes vol. 3 , 2nd edn, pp. 2342–2349 . Edited by Balows A., Trüper H. G., Dworkin M., Harder W., Schleifer K.-H. New York: Springer;
     [Google Scholar]
  22. Guédon G., Bourgoin F., Pébay M., Roussel Y., Colmin C., Simonet J. M., Decaris B. 1995; Characterization and distribution of two insertion sequences, IS1191 and iso-IS981, in Streptococcus thermophilus: does intergeneric transfer of insertion sequences occur in lactic acid bacteria co-cultures?. Mol Microbiol 16:69–78
     [Google Scholar]
  23. Guerrero C., Bernasconi C., Burki D., Bodmer T., Telenti A. 1995; A novel insertion element from Mycobacterium avium, IS1245, is a specific target for analysis of strain relatedness. J Clin Microbiol 33:304–307
     [Google Scholar]
  24. Guilhot C., Gicquel B., Davies J., Martin C. 1992; Isolation and analysis of IS6120, a new insertion sequence from Mycobacterium smegmatis. . Mol Microbiol 6:107–113
     [Google Scholar]
  25. Haugland R. A., Sangodkar U. M. X., Chakrabarty A. M. 1990; Repeated sequences including RS1100 from Pseudomonas cepacia AC1100 function as IS elements. Mol Gen Genet 220:222–228
     [Google Scholar]
  26. Inoue H., Nojima, H & Okayama H. 1990; High efficiency transformation of Escherichia coli with plasmids. Gene 96:23–28
     [Google Scholar]
  27. Iversen T. G., Standal R., Pedersen T., Coucheron D. H. 1994; IS1032 from Acetobacter xylinum, a new mobile insertion sequence. Plasmid 32:46–54
     [Google Scholar]
  28. Kaneko T., Sato S., Kotani H. and 21 other authors 1996; Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. PCC6803. 2. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res 3:109–136
     [Google Scholar]
  29. Kleckner N. 1981; Transposable elements in prokaryotes. Annu Rev Genet 15:341–404
     [Google Scholar]
  30. Kohler-Staub D., Hartmans S., Gälli R., Suter F., Leisinger T. 1986; Evidence for identical dichloromethane dehalogenases in different methylotrophic bacteria. J Gen Microbiol 132:2837–2843
     [Google Scholar]
  31. Laberge S., Middleton A. T., Wheatcroft R. 1995; Characterization, nucleotide sequence and conserved genomic locations of insertion sequence ISRm5 in Rhizobium meliloti. . J Bacteriol 177:3133–3142
     [Google Scholar]
  32. La Roche S., Leisinger T. 1990; Sequence analysis and expression of the bacterial dichloromethane dehalogenase structural gene, a member of the glutathione S-transferase supergene family. J Bacteriol 172:164–171
     [Google Scholar]
  33. La Roche S., Leisinger T. 1991; Identification of dcmR, the regulatory gene governing expression of dichloromethane dehalogenase in Methylobacterium sp. strain DM4. J Bacteriol 173:6714–6721
     [Google Scholar]
  34. Leisinger T., Bader R., Hermann R., Schmid-Appert M., Vuilleumier S. 1994; Microbes, enzymes and genes involved in dichloromethane utilization. Biodegradation 5:237–248
     [Google Scholar]
  35. Mazel D., Bernard C., Schwarz R., Castets A. M., Houmard J., Tandeau de Marsac N. 1991; Characterization of two insertion sequences, IS701 and IS702, from cyanobacterium Calothrix species PCC7601. Mol Microbiol 5:2165–2170
     [Google Scholar]
  36. Miller J. H. 1972 Experiments in Molecular Genetics Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
     [Google Scholar]
  37. Pearson W. R. 1996; Effective protein sequence comparison. Methods Enzymol 266:227–258
     [Google Scholar]
  38. van der Ploeg J., Willemsen M., van Hall G., Janssen D. B. 1995; Adaptation of Xanthobacter autotrophicus GJ10 to bromoacetate due to activation and mobilization of the haloacetate dehalogenase gene by insertion element IS1247. . J Bacteriol 177:1348–1356
     [Google Scholar]
  39. Rezsöhazy R., Hallet B., Delcour J., Mahillon J. 1993; The IS4 family of insertion sequences: evidence for a conserved transposase motif. Mol Microbiol 9:1283–1295
     [Google Scholar]
  40. 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]
  41. Schmid-Appert M. 1996 Untersuchungen zur Regulation des Dichlormethan-Dehalogenase Gens aus Methylobacterium sp. Stamm DM4 und Struktur der angrenzenden DNA-Region Dissertation, ETH Zürich.
    [Google Scholar]
  42. Scholtz R., Wackett L. P., Egli C., Cook A. M., Leisinger T. 1988; Dichloromethane dehalogenase with improved catalytic activity isolated from a fast-growing dichloromethane-utilizing bacterium. J Bacteriol 170:5698–5704
     [Google Scholar]
  43. Schuurman R., Keulen W. 1991; Modified protocol for DNA sequence analysis using Sequenase® 2.0. BioTechniques 10:185
     [Google Scholar]
  44. Simon R., Priefer U., Pühler A. 1983; Vector plasmids for in vitro and in vivo manipulation of Gram-negative bacteria. . In Molecular Genetics of the Bacteria–Plant Interaction pp. 98–106 . Edited by Pühler A. Berlin: Springer;
     [Google Scholar]
  45. Soto M. J., Zorzano A., Olivares J., Toro N. 1992; Sequence of ISRm4 from Rhizobium meliloti strain GR4. Gene 120:125–126
     [Google Scholar]
  46. Stucki G., Gälli R., Ebersold H.-R., Leisinger T. 1981; Dehalogenation of dichloromethane by cell extracts of Hyphomicrobium DM2. Arch Microbiol 130:366–371
     [Google Scholar]
  47. Thomas A. W., Slater J. H., Weightman A. J. 1992; The dehalogenase gene dehI from Pseudomonas putida PP3 is carried on an unusual mobile genetic element designated DEH. . J Bacteriol 174:1932–1940
     [Google Scholar]
  48. Van der Meer J. R., Zehnder A. J. B., de Vos W. M. 1991; Identification of a novel composite transposable element, Tn5280, carrying chlorobenzene dioxygenase genes of Pseudomonas sp. strain P51. J Bacteriol 173:7077–7083
     [Google Scholar]
  49. Van der Meer J. R., de Vos W. M., Harayama S., Zehnder A. J. B. 1992; Molecular mechanisms of genetic adaptation to xenobiotic compounds. Microbiol Rev 56:677–694
     [Google Scholar]
  50. Wood M. S., Byrne A., Lessie T. G. 1991; IS406 and IS407, two gene-activating insertion sequences from Pseudomonas cepacia. . Gene 105:101–105
     [Google Scholar]
  51. Wyndham R. C., Cashore A. E., Nakatsu C. H., Peel M. C. 1994; Catabolic transposons. Biodegradation 5:323–342
     [Google Scholar]
  52. Yates J. R., Cunningham R. P., Holmes D. S. 1988; IST2: an insertion sequence from Thiobacillus ferrooxidans. . Proc Natl Acad Sci USA 85:7284–7287
     [Google Scholar]
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Association of newly discovered IS elements with the dichloromethane utilization genes of methylotrophic bacteria
Microbiology 143, 2557 (1997); https://doi.org/10.1099/00221287-143-8-2557
/content/journal/micro/10.1099/00221287-143-8-2557
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