Skip to main content
Log in

Plasmids in tributyltin-resistant bacteria from fresh and estuarine waters

  • Published:
Journal of Industrial Microbiology

Summary

Twenty-six tributyltin (TBT)-resistant bacterial strains isolated from sediments were examined for the presence of plasmids. Plasmids of the size reported to carry metal resistance genes were not found in 15 of the strains, indicating that resistance does not have to be plasmid-mediated. Attempts to cure plasmid-containing strains using acridine organge, ethidium bromide, novobiocin or sodium dodecylsulfate, or by growth at elevated temperature were not successful, nor were plasmids transferred from TBT-resistant strains into TBT-sensitive organisms by electroporation. In a broth mating experiment however, plasmid pUM505, a conjugative plasmid known to encode chromium resistance inPseudomonas aeruginosa PAO1, was introduced into TBT-sensitiveBeijerinckia sp. MC-27 isolated from freshwater sediment. The TBT tolerance of theBeijerinckia sp. increased 100-fold, from 8.4 μM TBT inBeijerinckia sp. MC-27 to 840 μM TBT inBeijerinckia sp. MC-27 (pUM505) on solid medium. The plasmid was transferred at a frequency of approximately 6×10−4. TBT-resistant transconjugants grew faster in media containing TBT and lost their enhanced TBT tolerance and the plasmid upon serial transfer in medium without TBT. Spontaneous mutants of the donorP. aeruginosa lost both TBT resistance and the plasmid. Therefore, TBT resistance in bacteria can be plasmid-mediated. To our knowledge, this is the first report that resistance to a tin compound can be plasmid-mediated.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Anderson, D.G. and L.L. McKay. 1983. Simple and rapid method for isolating large plasmid DNA from lactic streptococci. Appl. Environ. Microbiol. 46: 549–552.

    PubMed  Google Scholar 

  2. Avery, S.V., M.E. Miller, G.M. Gadd, G.A. Codd and J.J. Cooney. 1991. Toxicity of organotins toward cyanobacterial photosynthesis and nitrogen fixation. FEMS Microbiol. Lett. 84: 205–210.

    Google Scholar 

  3. Belliveau, B.H., T.S. Wong and J.J. Trevors. 1987. Lead, tin and multiple antibiotic resistantPseudomonas isolated from polluted sediment. Tox. Assess. 2: 377–386.

    Google Scholar 

  4. Birnboim, H.C. and J. Doly. 1979. A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucl. Acids Res. 7: 1513–1523.

    PubMed  Google Scholar 

  5. Cervantes, C. and H. Ohtake. 1988. Plasmid-determined resistance to chromate inPseudomonas aeruginosa. FEMS Microbiol. Lett. 56: 173–176.

    Google Scholar 

  6. Cervantes, C., H. Ohtake, L. Chu, T.K. Misra and S. Silver. 1990. Cloning, nucleotide sequence and expression of the chromate resistance determinant ofPseudomonas aeruginosa plasmid pUM505. J. Bacteriol. 172: 287–291.

    PubMed  Google Scholar 

  7. Champ, M.A. and W.L. Pugh. 1987. Tributyltin antifouling paints: introduction and overview. Oceans 87 Proc., Vol. 4, pp. 1296–1308, IEEE Service Center, Piscataway, NJ.

    Google Scholar 

  8. Cooney, J.J. 1988. Microbial transformations of tin and tin compounds. J. Ind. Microbiol. 3: 195–204.

    Google Scholar 

  9. Cooney, J.J. 1995. Organotin compounds and aquatic bacteria. Helgoland Meeresuch. 49: (in press).

  10. Cooney, J.J., L. deRome, O. Laurence and G.M. Gadd. 1989. Effects of organotin and organolead compounds on yeasts. J. Ind. Microbiol. 4: 279–288.

    Google Scholar 

  11. Cooney, J.J. and S. Wuertz. 1989. Toxic effects of tin compounds on microorganisms. J. Ind. Microbiol. 4: 375–402.

    Google Scholar 

  12. Crosa, J.H. and S. Falkow. 1981. Plasmids. In: Manual of Methods for General Microbiology (Gerhard, P., ed.), pp. 266–283, Amer. Soc. Microbiol., Washington, DC.

    Google Scholar 

  13. Fukagawa, T. and S. Suzuki. 1993. Cloning of gene responsible for tributyltin chloride (TBTCl) resistance in TBTCl-resistant marine bacterium,Alteromonas sp. M-1. Biochem. Biophys. Res. Commun. 194: 733–740.

    PubMed  Google Scholar 

  14. Gibbs, P.E., G.W. Bryan and P.L. Pascoe. 1991. TBT-induced imposex in the dogwhelk,Nucella lapillus: geographical uniformity of the response and effects. Mar. Environ. Res. 32: 79–87.

    Google Scholar 

  15. Krone, C.A., D.W. Brown, D.G. Burrows, S. Chan and U. Varanasi. 1989. Butyltins in sediment from marinas and waterways in Puget Sound, Washington State. USA Mar. Pollut. Bull. 20: 528–531.

    Google Scholar 

  16. Lee, R.F. 1991. Metabolism of tributyltin by marine animals and possible linkages to effects. Mar. Environ. Res. 32: 29–35.

    Google Scholar 

  17. Lee, S. and S. Rasheed. 1990. A simple procedure for maximum yield of high-quality plasmid DNA. Biotechniques 9: 676–679.

    PubMed  Google Scholar 

  18. Mackie, G.L., W.N. Gibbons, B.W. Muncaster and I.M. Gray. 1989. The zebra mussel,Dreissena polymorpha: a synthesis of European experiences and a preview for North America. Environment Ontario, Queen's Printer for Ontario, 75 pp.

  19. Maguire, R.J. and R.K. Tkacz. 1985. Concentration of tributyltin in the surface microlayer of natural waters. Water Pollut. Res. J. Canada 22: 227–233.

    Google Scholar 

  20. Misra, T.K. 1992. Bacterial resistances to inorganic mercury salts and organomercurials. Plasmid 27: 4–16.

    PubMed  Google Scholar 

  21. Oehlmann, J., E. Stroben and P. Fiorini. 1991. The morphological expression of imposex inNucella lapillus (Linnaeus) (Gastropoda: Muricidae). J. Moll. Stud. 57: 375–390.

    Google Scholar 

  22. Olson, J.E. 1990. An improved method for the rapid isolation of plasmid DNA from wild-type Gram-negative bacteria for plasmid restriction profile analysis. Lett. Appl. Microbiol. 10: 209–212.

    PubMed  Google Scholar 

  23. O'Rorke, C. (in preparation). Isolation and characterization of a plasmid associated with phenanthrene biotransformation by a coryneform bacterium, CO6. M.S. Thesis, Univ. Massachusetts, Boston, MA.

  24. Pettibone, G.W. and J.J. Cooney. 1986. Effect of organotins on fecal pollution indicator organisms. Appl. Environ. Microbiol. 52: 562–566.

    PubMed  Google Scholar 

  25. Sambrook, J., E.F. Fritsch and J. Maniatis. 1989. Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.

    Google Scholar 

  26. Silver, S. 1992. Plasmid-determined metal resistance mechanisms: range and overview. Plasmid 21: 1–3.

    Google Scholar 

  27. Smith, C. 1990. Bacterial transport of naphthalene in the environment. Masters Thesis, Univ. Massachusetts, Boston.

    Google Scholar 

  28. Speyer, J.F. 1990. A simple and effective electroporation apparatus. Biotechniques 8: 28–30.

    PubMed  Google Scholar 

  29. Spooner, N., P.E. Gibbs, G.W. Bryan and L.J. Goad. 1991. The effect of tributyltin upon steroid titres in the female dogwhelk,Nucella lapillus, and the development of imposex. Mar. Environ. Res. 32: 37–49.

    Google Scholar 

  30. Summers, A.O. and G.A. Jacoby. 1978. Plasmid-determined resistance to boron and chromium compounds inPseudomonas aeruginosa. Antimicrob. Agents Chemother. 13: 637–640.

    PubMed  Google Scholar 

  31. Suzuki, S., T. Fukagawa and K. Takama. 1992. Occurrence of tributyltin-tolerant bacteria in tributyltin- or cadmium-containing seawater. Appl. Environ. Microbiol. 58: 3410–3412.

    PubMed  Google Scholar 

  32. U.S. Public Law 100-330 102 Stat. 605. Organotin antifouling paint control act of 1988, June 16, 1988.

  33. Wade, T.L., B. Garcia-Romero and J.M. Brooks. 1990. Butyltins in sediments and bivalves from U.S. coastal areas. Chemosphere 20: 647–662.

    Google Scholar 

  34. Walter, M.V., A. Porteous and R.J. Seidler. 1987. Measuring genetic stability in bacteria of potential use in genetic engineering. Appl. Environ. Microbiol. 53: 105–109.

    PubMed  Google Scholar 

  35. Wuertz, S., M.M. Doolittle, M.E. Miller, J.F. Brennan and J.J. Cooney. 1991. Butyltins in estuarine sediments two years after tributyltin use was restricted. Chemosphere 22: 1113–1120.

    Google Scholar 

  36. Wuertz, S., C.E. Miller, R.M. Pfister and J.J. Cooney. 1991. Tributyltin-resistant bacteria from estuarine and freshwater sediments. Appl. Environ. Microbiol. 57: 2783–2789.

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Miller, C.E., Wuertz, S., Cooney, J.J. et al. Plasmids in tributyltin-resistant bacteria from fresh and estuarine waters. Journal of Industrial Microbiology 14, 337–342 (1995). https://doi.org/10.1007/BF01569948

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01569948

Key words

Navigation