1887

Abstract

Horizontal dissemination of the genes responsible for resistance to toxic pollutants may play a key role in the adaptation of bacterial populations to environmental contaminants. However, the frequency and extent of gene dissemination in natural environments is not known. A natural horizontal spread of two distinct mercury resistance operon variants, which occurred amongst diverse and related species over wide geographical areas, is reported. One variant encodes a mercuric reductase with a single N-terminal domain, whilst the other encodes a reductase with a duplicated N-terminal domain. The strains containing the former operon types are sensitive to organomercurials, and are most common in the terrestrial mercury-resistant populations studied in this work. The strains containing the latter operon types are resistant to organomercurials, and dominate in a Minamata Bay mercury-resistant population, previously described in the literature. At least three distinct transposons (related to a class II vancomycin-resistance transposon, Tn , from a clinical strain) and conjugative plasmids are implicated as mediators of the spread of these operons.

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1998-03-01
2024-10-03
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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. Arthur M., Molinas C., Depardieu T., Courvalin P. 1993; Characterization of Tnl546, a Tn3-related transposon conferring glycopeptide resistance by synthesis of depsipeptide peptido- glycan precursors in Enterococcus faecium BM 4147.. J Bacteriol 175:117–127
    [Google Scholar]
  3. Ash C., Farrow J.A.E., Dorsch M., Stackebrandt E., Collins M.D. 1991; Comparative analysis of Bacillus antbracis, Bacillus cereus, and related species on the basis of reverse transcriptase sequencing of 16S rRNA.. Int J Syst Bacteriol 41:343–346
    [Google Scholar]
  4. Begley T.P., Walts A.E., Walsh C.T. 1986; Mechanistic studies of a protonolytic organomercurial cleaving enzyme: bacterial organomercurial lyase.. Biochemistry 25:7192–7200
    [Google Scholar]
  5. Belliveau B.H., Trevors J.T. 1990; Mercury resistance determined by a self-transmissible plasmid in Bacillus cereus 5.. Bio Metals 3:188–196
    [Google Scholar]
  6. Birnboim H.C., Doly J. 1979; A rapid alkaline extraction procedure for screening recombinant plasmid DNA.. Nucleic Acids Res 7:1513–1523
    [Google Scholar]
  7. Bogdanova E.S., Mindlin S.Z. 1989; Two structural types of mercury reductases and possible ways of their evolution.. FEBS Lett 247:333–336
    [Google Scholar]
  8. Bogdanova E.S., Mindlin S.Z. 1991; Occurrence of two structural types of mercury reductases among Gram-positive bacteria.. FEMS Microbiol Lett 78:277–280
    [Google Scholar]
  9. Bogdanova E.S., Mindlin S.Z., Kalyaeva E.S., Nikiforov V.G. 1988; The diversity of mercury reductases among mercury- resistant bacteria.. FEBS Lett 234:280–282
    [Google Scholar]
  10. Bogdanova E.S., Mindlin S.Z., Pakrova E., Kocur M., Rouch D.A. 1992; Mercuric reductase in environmental Gram-positive bacteria sensitive to mercury.. FEMS Microbiol Lett 97:95–100
    [Google Scholar]
  11. Brown N.L., Lund P.L., Ni’Bhrian N. 1989; Mercury resistance in bacteria.. In The Genetics of Bacterial Diversity pp. 175–195 Hopwood D.A., Chater K.F. Edited by London & New York: Academic Press;
    [Google Scholar]
  12. de Bruijn F.J. 1992; Use of repetitive (repetitive extragenic palindromic and enterobacterial repetitive intergeneric consensus) sequences and the polymerase chain reaction to fingerprint the genomes of Rhizobium meliloti isolates and other soil bacteria.. Appl Environ Microbiol 58:2180–2187
    [Google Scholar]
  13. Cano R.J., Borucki M.K., Higby-Schweitzer M., Poinar H.N., Poinar G.O. Jr Pollard K.J. 1994; Bacillus DNA in fossil bees: an ancient symbiosis?. Appl Environ Microbiol 60:2164–2167
    [Google Scholar]
  14. Claus D., Berkely R.C.W. 1986; Genus Bacillus Cohn 1872, 174 AL.. In Bergey’s Manual of Systematic Bacteriology 2 pp. 1105–1139 Sneath P.H.A., Mair N.C., Sharpe M.E., Holt J.G. Edited by Baltimore: Williams & Wilkins;
    [Google Scholar]
  15. Dornbush A.C., Pelcak E.J. 1948; Assay of aureomycin level in body fluid.. Ann NY Acad Sci 51:218–220
    [Google Scholar]
  16. Gadd G.M. 1990; Metal tolerance.. In Microbiology of Extreme Environments pp. 179–210 Edwards C. Edited by Milton Keynes: Open University Press;
    [Google Scholar]
  17. Gilbert M.P., Summers A.O. 1988; The distribution and divergence of DNA sequences related to Tn21 and Tn502 mer operons.. Plasmid 20:127–136
    [Google Scholar]
  18. Gilichinsky D.A., Vorobyova E.A., Erochina L.G., Fyodorov-Davydov D.G., Chaikovskaya N.R. 1992; Long-term pres-ervation of microbial ecosystems in permafrost.. Adv Space Res 12:(4)255–(4)263
    [Google Scholar]
  19. Grinsted J., De La Cruz F., Schmitt R. 1990; The Tn22 subgroup of bacterial transposable elements.. Plasmid 24:163–189
    [Google Scholar]
  20. Hobman J.L., Brown N.L. 1997; Bacterial mercury resistance genes.. In Metal Zons in Biological Systems 34 pp. 527–567 Sigel H., Sigel A. Edited by New York: Marcel Dekker;
    [Google Scholar]
  21. Hobman J.L., Kholodii Ya G., Nikiforov V.G., Ritchie D.A., Strike P., Yurieva O.V. 1994; The sequence of the mer operon of pMER 327/419 and transposon ends of pMER.327/419, 330 and 05.. Gene 146:73–78
    [Google Scholar]
  22. Johansen T., Carlson C.R., Kolsto A.-B. 1996; Variable numbers of rRNA gene operons in Bacillus cereus strains.. FEMS Microbiol Lett 136:325–328
    [Google Scholar]
  23. Kholodii Ya G., Gorlenko Zh M., Lomovskaya O.L., Mindlin S.Z., Yurieva O.V., Nikiforov V.G. 1993a; Molecular characterization of an aberrant mercury resistance transposable element from an environmental Acinetobacter strain.. Plasmid 30:303–308
    [Google Scholar]
  24. Kholodii Ya G., Yurieva O.V., Lomovskaya O.L., Gorlenko Zh M., Mindlin S.Z., Nikiforov V.G. 1993b; Tn5053, a mercury resistance transposon with integron’s ends.. J Mol Biol 230:1103–1107
    [Google Scholar]
  25. Kholodii Ya G., Mindlin S.Z., Bass I.A., Yurieva O.V., Minakhina S.V., Nikiforov V.G. 1995; Four genes, two ends, and a res region are involved in transposition of Tn5053: a paradigm for a novel family of transposons carrying either a mer operon or an integron.. Mol Microbiol 6:1189–1200
    [Google Scholar]
  26. Kholodii Ya G., Yurieva O.V., Gorlenko Zh M., Mindlin S.Z., Bass I.A., Lomovskaya O.L., Kopteva A.V., Nikiforov V.G. 1997; Tn5042 : a chimeric mercury resistance transposon closely related to the toluene degradative transposon Tn4652.. Microbiology 143:2549–2556
    [Google Scholar]
  27. Laddaga R.A., Chu L., Misra T.K., Silver S. 1987; Nucleotide sequence and expression of the mercurial resistance operon from Staphylococcus aureus plasmid pI258.. Proc Natl Acad Sci USA 84:5106–5110
    [Google Scholar]
  28. Liebert C.A., Wireman J., Smith T., Summers A.O. 1997; Phylogeny of mercury resistance (mer) operons of Gram-negative bacteria isolated from the fecal flora of primates.. Appl Environ Microbiol 63:1066–1076
    [Google Scholar]
  29. Mahler I., Levinson H.S., Wang Y., Halvorson H.O. 1986; Cadmium- and mercury-resistant Bacillus strains from a salt marsh and from Boston Harbor.. Appl Environ Microbiol 52:1293–1298
    [Google Scholar]
  30. Maidak B.L., Larsen N., McGaughey M.J, Overbek R., Olson G.J., Fogell K., Blandy J., Woese C.R. 1994; The Ribosomal Database Project.. Nucleic Acids Res 22:3485–3487
    [Google Scholar]
  31. Milkman R., McKane M. 1995; DNA sequence variation and recombination in E. coli. . In The Population Genetics of Bacteria(Society for General Microbiology Symposium) 52 pp. 127–142 Baumberg S., Young J.P.W., Wellington E.M.H., Saunders J.R. Edited by Cambridge: Cambridge University Press;
    [Google Scholar]
  32. Misra T.K. 1992; Bacterial resistances to inorganic mercury salts and organomercurials.. Plasmid 25:4–16
    [Google Scholar]
  33. Nakahara H., Ishikawa T., Sarai Y., Kondo I., Mitsuhashi S. 1977; Frequency of heavy-metal resistance in bacteria from inpatients in Japan.. Nature 266:165–167
    [Google Scholar]
  34. Nakamura K., Silver S. 1994; Molecular analysis of mercury- resistant Bacillus isolates from sediment of Minamata Bay, Japan.. Appl Environ Microbiol 60:4596–4599
    [Google Scholar]
  35. Ochman H., Wilson A.C. 1987; Evolution in bacteria: evidence for a universal substitution rate in cellular genomes.. J Mol Evol 26:74–84
    [Google Scholar]
  36. Olson B.H., Lester J.N., Cayless S.M., Ford S. 1989; Distribution of mercury resistance determinants in bacterial communities of river sediments.. Wat Res 23:1209–1217
    [Google Scholar]
  37. Osborn A.M., Bruce K.D., Strike P., Ritchie D.A. 1995; Sequence conservation between regulatory mercury resistance genes in bacteria from mercury polluted and pristine environments.. Syst Appl Microbiol 18:1–6
    [Google Scholar]
  38. Osborn A.M., Bruce K.D., Ritchie D.A., Strike P. 1996; Themercury resistance operon of the IncJ plasmid pMERPH exhibits structural and regulatory divergence from other Gram-negative mer operons.. Microbiology 142:337–345
    [Google Scholar]
  39. Osborn A.M., Bruce K.D., Strike P., Ritchie D.A. 1997; Distribution, diversity and evolution of the bacterial mercury resistance (mer) operon.. FEMS Microbiol Rev 19:239–262
    [Google Scholar]
  40. Reniero D., Galli E., Barbieri P. 1995; Cloning and comparison of mercury- and organomercurial-resistance determinants from a Pseudomonas stutzeri plasmid.. Gene 166:77–82
    [Google Scholar]
  41. Roberts M.S., Cohan F.M. 1995; Recombination and migration rates in natural populations of Bacillus subtilis and Bacillus mojavensis.. Evolution 49:1081–1094
    [Google Scholar]
  42. Robinson J.B., Tuovinen O.H. 1984; Mechanisms of mi-crobial resistance and detoxification of mercury and organo- mercury compounds: physiological, biochemical and genetic analyses.. Microbiol Rev 48:95–124
    [Google Scholar]
  43. 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]
  44. Sanger F., Nicklen S., Coulson A.R. 1977; DNA sequencing with chain-terminating inhibitors.. Proc Natl Acad Sci USA 74:5463–5467
    [Google Scholar]
  45. Sedlmeier R., Altenbuchner J. 1992; Cloning and DNA sequence analysis of the mercury resistance genes of Streptomyces lividans.. Mol Gen Genet 236:76–85
    [Google Scholar]
  46. Shiratori T., Inoue C., Sugawara K., Kusano T., Kitigawa Y. 1989; Cloning and expression of Thiobacillus ferrooxidans mercury ion resistance genes in Escherichia coli.. J Bacteriol 171:3458–3464
    [Google Scholar]
  47. Siemieniak D.R., Slightom J.L., Chung S.T. 1990; Nucleotide sequence of Streptomyces fradiae transposable element Tn4556: a class II transposon related to Tn3.. Gene 86:1–9
    [Google Scholar]
  48. Silver S., Phung L.T. 1996; Bacterial heavy metal resistance: new surprises.. Annu Rev Microbiol 50:753–789
    [Google Scholar]
  49. Summers A.O. 1986; Organization, expression and evolution of genes for mercury resistance.. Annu Review Microbiol 40:607–634
    [Google Scholar]
  50. VandePeer Y., De Wachter R. 1994; TREECON for Windows: a software package for the construction and drawing of evolutionary trees for the Microsoft Windows environment.. Comput Appl Biosci 10:569–570
    [Google Scholar]
  51. Wang Y., Mahler I., Levinson H.S., Hallorson H.O. 1987; Cloning and expression in Escherichia coli of chromosomal mercury resistance genes from a Bacillus sp.. J Bacteriol 169:4848–4851
    [Google Scholar]
  52. Wang Y., Moore M., Levinson H.S., Silver S., Walsh C., Mahler I. 1989; Nucleotide sequence of a chromosomal mercury resistance determinant from a Bacillus sp. with broad-spectrum mercury resistance.. J Bacteriol 171:83–92
    [Google Scholar]
  53. Witte W., Green L., Silver S. 1986; Resistance to mercury and to cadmium in chromosomally resistant Staphylococcus aureus.. Antimicrob Agents Chemother 29:663–669
    [Google Scholar]
  54. Yurieva O., Nikiforov V. 1996; Catalytic center quest: comparison of transposases belonging to the Tn3 family reveals an invariant triad of acidic amino acid residues.. Biochem Mol Biol Int 38:15–20
    [Google Scholar]
  55. Yurieva O.V., Kholodii G.Ya., Minakhin L.S., Gorlenko Zh M., Kalyaeva E.S., Mindlin S.Z., Nikiforov V.G. 1997; Inter-continental spread of promiscuous mercury resistance operons in environmental bacteria.. Mol Microbiol 24:321–329
    [Google Scholar]
  56. Zharkikh A.A., Rzhetsky Yu A., Morosov P.S., Sitnikova T.L., Krushkal J.S. 1991; VOSTORG : a package of microcomputer programs for sequence analysis and construction on phylogenetic trees.. Gene 101:251–254
    [Google Scholar]
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