Journal of Industrial Microbiology

, Volume 14, Issue 2, pp 142–153 | Cite as

Theczc operon ofAlcaligenes eutrophus CH34: from resistance mechanism to the removal of heavy metals

  • Ludo Diels
  • Qinghan Dong
  • Daniël van der Lelie
  • Wilfried Baeyens
  • Max Mergeay
Article

Summary

The plasmid-borneczc operon ensures for resistance to Cd2+, Zn2+ and Co2+ ions through a tricomponent export pathway and is associated to various conjugative plasmids ofA. eutrophus strains isolated from metal-contaminated industrial areas. Theczc region of pMOL30 was reassessed especially for the segments located upstream and downstream the structural genesczc CBA. In cultures grown with high concentrations of heavy metals,czc-mediated efflux of cations is followed by a process of metal bioprecipitation. These observations led to the development of bioreactors designed for the removal of heavy metals from polluted effluents.

Key words

Soil bacteria Alcaligenes Plasmid Cadmium Metal resistance Cation efflux Gene fusion Bioprecipitation Bioreactor 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Aiking, H., K. Kok, H. van Heerikhuizen and J. van't Riet. 1982. Adaptation to cadmium byKlebsiella aerogenes growing in continuous sulfide. Appl. Environ. Microbiol. 44: 938–944.Google Scholar
  2. 2.
    Arroyo, J., M.C. Hurley, M. Wolf, M.S. McClain, B.I. Eisenstein and N.C. Engleberg. 1994. Shuttle mutagenesis ofLegionella pneumophila: identification of a gene associated with host cell cytopathicity. Infect. Immun. 62: 4075–4080.PubMedGoogle Scholar
  3. 3.
    Baev, N., G. Endre, G. Petrovics, Z. Banfalvi and A. Kondorosi. 1991. Six nodulation genes ofnod box locus 4 inRhizobium meliloti are involved in nodulation signal productionnodM codes ford-glucosamine synthetize. Mol. Gen. Genet. 228: 113–124.PubMedGoogle Scholar
  4. 4.
    Ballinger, D.G., N. Xue and K.D. Harschman. 1993. ADrosophila photoreceptor cell specific protein. Calphotin, binds calcium and contains a leucine zipper. Proc. Natl Acad. Sci. USA 90: 1536–1540.PubMedGoogle Scholar
  5. 5.
    Collard, J.M., A. Provoost, S. Taghavi and M. Mergeay. 1993. A new type ofAlaligenes eutrophus CH34 zinc resistance generated by mutations affecting regulation of thecnr cobalt-nickel resistance system. J. Bacteriol. 175: 779–784.PubMedGoogle Scholar
  6. 6.
    Conklin, D.S., J.A. McMaster, M.R. Culbertson and C. Kung. 1992.Cotl, a gene involved in cobalt accumulation inSaccharomyces cerevisiae. Mol. Cell. Biol. 12: 3678–3688.PubMedGoogle Scholar
  7. 7.
    Crouzet, J., S. Levy-Schil, B. Cameron, L. Cauchois, S. Rigault, M.C. Rongez, F. Blanch, L. Debussche and D. Thibaut. 1991. Nucleotide sequence and genetic analysis of a 13-1-kilobase-pairPseudomonas denitrificans DNA fragment containing fivecob gene and identification of structural genes encoding Cob(I) alamin adenosyl transferase cobytic acid synthase and bifunctional cobinamide kinase—cobinamide phosphate guanylytransferase. J. Bacteriol. 173: 6074–6187.PubMedGoogle Scholar
  8. 8.
    Diels, L., M. Faelen, M. Mergeay and D. Nies. 1985. Mercury transposons from plasmids governing multiple resistance to heavy metals inAlcaligenes eutrophus CH34. Arch. Int. Physiol. Biochim. 93: B27-B28.Google Scholar
  9. 9.
    Diels, L., A. Sadouk and M. Mergeay. 1989. Large plasmids governing multiple resistances to heavy metals: a genetic approach. Toxic. Environ. Chem. 23: 19Google Scholar
  10. 10.
    Diels, L. and M. Mergeay. 1990. DNA probe-mediated detection of resistant bacteria from soils highly polluted by heavy metals. Appl. Environ. Microbiol. 56: 1485–1491.Google Scholar
  11. 11.
    Diels, L., S. Van Roy, M. Mergeay, W Doyen, S. Taghavi and R. Leysen. 1993a. Immobilization of bacteria in composite membranes and development of tubular membrane reactors for heavy metal recuperation. In: Effective Membrane Processes: New Perspectives (R. Paterson, ed.), pp. 275–293. Mechanical Engineering Publications Limited. London, UK.Google Scholar
  12. 12.
    Diels, L., S. Van Roy, S. Taghavi, W. Doyen, R. Leysen and M. Mergeay. 1993b. The use ofAlcaligenes eutrophus immobilized in a tubular membrane reactor for heavy metal recuperation. In: Biohydrometallurgical Technologies, Vol. II (A.E. Torma, M.L. Apel and C.L. Brierley, eds), pp. 133–144, The Minerals, Metals & Materials Society. Warrendale, PA, USA.Google Scholar
  13. 13.
    Diels, L. 1990. Accumulation and precipitation of Cd and Zn ions byAlcaligenes eutrophus strains. In: Biohydrometallurgy 89 (J. Salby, R.G.I. McCready and P.Z. Wichlacz, eds), pp. 369–377, Proceedings of the International Symposium of Jackson Hole (Wyoming), August 13–18, 1989.Google Scholar
  14. 14.
    Dong, Q. and M. Mergeay. 1994. Czc/Cnr efflux: 3 component-export pathway with 12 transmembrane helix exporter. Mol. Microbiol. 14: 185–187.PubMedGoogle Scholar
  15. 15.
    Duong, F., A. Lazdunski, B. Cami and M. Murgier. 1992. Sequence of a cluster of gene controlling synthesis and secretion of alkaline protease inPseudomonas aeruginosa: relationship to other secretory pathways. Gene 121: 47–54.PubMedGoogle Scholar
  16. 16.
    Ehrlich, H.L. 1981. Microbial formation and decomposition of carbonates. In: Geomicrobiology, pp. 101–123, Marcel Dekker, New York.Google Scholar
  17. 17.
    Fath, M.J. and R. Kolter. 1993. ABC transporters: bacterial exporters. Microbiol. Rev. 57: 995–1017.PubMedGoogle Scholar
  18. 18.
    Felmlee, T., S. Pellett, E.Y. Lee and R.A. Welch. 1985.Escherichia coli hemolysin is released extracellularly without cleavage of a signal peptide. J. Bacteriol. 163: 88–93.PubMedGoogle Scholar
  19. 19.
    Glassr, P., H. Sakamoto, J. Bellalou, A. Ullmann and A. Danchin. 1988. Secretion of cyclolysin, the calmodulin-sensitive adenylate cyclase-haemolysin bifunctional protein ofBordetella pertussis. EMBO J. 7: 3997–4004.PubMedGoogle Scholar
  20. 20.
    Higgins, C.F. 1992. ABC transporter: from micro-organisms to man. Annu. Rev. Cell Biol. 8: 7–113.Google Scholar
  21. 21.
    Hrycyna, C.A., S.K. Sapperstein, S. Clarke and S. Michaelis. 1991. TheSaccharomyces cerevisiae STE14 gene encodes a methyltransferase that mediates C-terminal methylation of a-factor and RAS proteins. EMBO J. 10: 1699–1709.PubMedGoogle Scholar
  22. 22.
    Ji, G. and S. Silver. 1944. Review: bacterial resistance mechanisms for heavy metals of environmental concern. J. Ind. Microbiol. (this issue).Google Scholar
  23. 23.
    Kamizono, A., M. Nishizawa, Y. Ternishi, K. Murata and A. Kimura. 1989. Identification of a gene conferring resistance to zinc and cadmium ions in the yeastSaccharomyces cerevisiae. Mol. Gen. Genet. 219: 161–167.PubMedGoogle Scholar
  24. 24.
    Klein, J.R., B. Henrich and R. Plapp. 1991. Molecular analysis and nucleotide sequence of theenvCD operon ofEscherichia coli. Mol. Gen. Genet. 230: 230–240.PubMedGoogle Scholar
  25. 25.
    Létoffé, S., P. Delepelaire and C. Wandersman. 1990. Protease secretion byErwinia chrysanthemi: the specific secretion functions are analogous to those ofEscherichia coli α-haemolysin. EMBO J. 9: 1375–1382.PubMedGoogle Scholar
  26. 26.
    Liesegang, H., K. Lemke, R. Siddiqui and H.G. Schlegel. 1993. Characterization of the inducible nickel and cobalt resistance determinantcnr from pMOL28 ofAlcaligenes eutrophus CH34. J. Bacteriol. 175: 767–778.PubMedGoogle Scholar
  27. 27.
    Ma, D., D.N. Cook, M. Alberti, N.G. Pon, H. Nikaido and J.E. Hearst. 1993. Characterization ofacrA andacrE genes ofEscherichia coli. J. Bacteriol. 175: 6299–6313.PubMedGoogle Scholar
  28. 28.
    Macaskie, L.E. 1990. An immobilized cell bioprocess for the removal of heavy metals from aqueous flow. J. Chem. Tech. Biotechnol. 49: 357–379.Google Scholar
  29. 29.
    Mergeay, M., C. Houba and J. Gerits. 1978. Extrachromosomal inheritance controlling resistance to cadmium, cobalt and zinc ions: evidence from curing in aPseudomonas. Arch. Int. Physiol. Biochim. 86: 440–441.PubMedGoogle Scholar
  30. 30.
    Mergeay, M., D. Nies, H.G. Schlegel, J. Gerits and F. Van Gijsegem. 1985.Alcaligenes eutrophus CH34, a facultative chemolithotroph displaying plasmid bound resistance to heavy metals. J. Bacteriol. 162: 328–334.PubMedGoogle Scholar
  31. 31.
    Mergeay, M. 1991. Towards an understanding of the genetics of bacterial metal resistance. Trends Biotech. 9: 17–24.Google Scholar
  32. 32.
    Nies, A., D. Nies and S. Silver. 1990. Nucleotide sequence and expression of a plasmid-encoded chromate resistance determinant fromAlcaligenes eutrophus. J. Biol. Chem. 265: 5648–5653.PubMedGoogle Scholar
  33. 33.
    Nies, D. 1992. CzcR and CzcD, gene products affecting regulation of resistance to cobalt, zinc, and cadmiumczc system inAlcaligenes eutrophus. J. Bacteriol. 174: 8102–8110.PubMedGoogle Scholar
  34. 34.
    Nies, D., M. Mergeay, B. Friedrich and H.G. Schlegel. 1987. Cloning of plasmid genes encoding resistance to cobalt, zinc and cadmium fromAlcaligenes eutrophus CH34. J. Bacteriol. 167: 4865–4868.Google Scholar
  35. 35.
    Nies, A., D. Nies and S. Silver. 1989a. Cloning and expression of plasmid genes encoding resistance to chromate and cobalt inAlcaligenes eutrophus. J. Bacteriol. 171: 5065–5070.PubMedGoogle Scholar
  36. 36.
    Nies, D.H., A. Nies, L. Chu and S. Silver. 1989b. Expression and nucleotide sequence of a plasmid determined divalent cation efflux system fromAlcaligenes eutrophus. Proc. Natl Acad. Sci. USA 86: 7351–7355.PubMedGoogle Scholar
  37. 37.
    Nies, D. and S. Silver. 1989c. Plasmid-determined inducible efflux is responsible for resistance to cadmium, zinc and cobalt inAlcaligenes eutrophus. J. Bacterial. 171: 896–900.Google Scholar
  38. 38.
    Nies, D. and S. Silver. 1994. Ion efflux systems involved in bacterial metal resistances. J. Ind. Microbiol. (this issue).Google Scholar
  39. 39.
    Nikaido, H. 1994. Prevention of drug access to bacterial targets: permeability barriers and active efflux. Science 264: 382–388.PubMedGoogle Scholar
  40. 40.
    Poole, K., D.E. Henrichs and S. Heshat. 1993a. Cloning and sequence analysis of an EnvCD homologue inPseudomonas aeruginosa: regulation by iron and possible involvement in the secretion of the siderophore pyoverdine. Mol. Microbiol. 10: 529–544.PubMedGoogle Scholar
  41. 41.
    Poole, K., K. Krebes, C. McNally and S. Neshat. 1993b. Multiple antibiotic resistance inPseudomonas aeruginosa: evidence for involvement of an efflux operon. J. Bacteriol. 175: 7363–7372.PubMedGoogle Scholar
  42. 42.
    Saier, M.H. Jr, R. Tam, A. Reizer and J. Reizer. 1994. Two novel families of bacterial membrane proteins concerned with nodulation, cell division and transport. Mol. Microbiol. 11: 841–847.PubMedGoogle Scholar
  43. 43.
    Schultze-Lam, S., G. Harauz and T.J. Beveridge. 1992. Participation of cyanobacterial S layer in fine-rain mineral formation. J. Bacterial. 174: 7971–7981.Google Scholar
  44. 44.
    Sensfuss, C. and H.G. Schlegel. 1988. Plasmid pMOL28 encoded resistance to nickel is due to specific efflux. FEMS Microbiol. Lett. 55: 295–298.Google Scholar
  45. 45.
    Siddiqui, R.A., K. Benthin and H.G. Schlegel. 1989. Cloning of pMOL28 encoded nickel resistance genes and expression of the genes inAlcaligenes eutrophus andPseudomonas spp. J. Bacteriol. 171: 5071–5078.PubMedGoogle Scholar
  46. 46.
    Silver, S. and M. Walderhaug. 1992. Gene regulation of plasmid-and chromosome-determined inorganic ion transport in bacteria. Microbiol. Rev. 56: 195–228.PubMedGoogle Scholar
  47. 47.
    Smith, T.F. and M.S. Waterman. 1981. Identification of common molecular subsequences. J. Mol. Biol. 147: 195–197.PubMedGoogle Scholar
  48. 48.
    Shaw, J.J., L.G. Settles and C.I. Kado. 1988. Transposon Tn4431 mutagenesis ofXanthomonas campestris pv.campestris: characterization of a non pathogenic mutant and cloning of a locus of pathogenicity. Molecular Plant-Microbe Interactions 1: 39–45.Google Scholar
  49. 49.
    van der Lelie, D., P. Corbisier, W. Baeyens, S. Wuertz, L. Diels and M. Mergeay. 1994. The use of biosensors for environmental monitoring. Res. Microbiol. 145: 67–74.PubMedGoogle Scholar
  50. 50.
    Von Heijne, G. 1986. A new method predicting signal sequence cleavage sites. Nucl. Acids Res. 14: 4683–4690.PubMedGoogle Scholar
  51. 51.
    Wandersman, C. and P. Deleplaire. 1990. TolC anEscherichia coli outer membrane protein required for hemolysin secretion. Proc. Natl Acad. Sci. USA 87: 4776–4780.PubMedGoogle Scholar

Copyright information

© Society for Industrial Microbiology 1995

Authors and Affiliations

  • Ludo Diels
    • 1
  • Qinghan Dong
    • 1
  • Daniël van der Lelie
    • 1
  • Wilfried Baeyens
    • 1
  • Max Mergeay
    • 1
  1. 1.Flemish Institute for Technological Research (VITO)MolBelgium

Personalised recommendations