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Copper toxicity and uptake in microorganisms

Journal of Industrial Microbiology volume 6, pages 77–84 (1990)Cite this article

Summary

Copper is a required trace element for growth of microorganisms since it is a cofactor for numerous enzymes. Also, proteins containing copper are important electron transfer carriers. However, at elevated concentrations, copper can be highly toxic to microorganisms. This review examines copper toxicity and uptake in microorganisms, with an emphasis on copper-resistance mechanisms.

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References

  1. Adaskaveg, J.E. and R.B. Hine, 1985. Copper tolerance and zinc sensitivity of Mexican strains ofXanthomonas campestris pv.vesicatoria, causal agent of bacterial spot of pepper. Plant Disease 69: 993–996.

    Google Scholar 

  2. Babich, H. and O. Stotzky. 1980. Environmental factors that influence the toxicity of heavy metal and gaseous pollutants to microorganisms. CRC Crit. Rev. Bicrobiol 8: 99–145.

    Google Scholar 

  3. Baker, D.E., 1974. Copper: soil, water, plant relationships. Fed. Proc. 33: 1188–1193.

    Google Scholar 

  4. Baldry, M.G.C. and A.C.R. Dean. 1981. Environmental change and copper uptake byBacillus subtilis subsp.niger and byPseudomonas fluorescens. Biotechnol. Lett. 3, 137–142.

    Google Scholar 

  5. Bauda, P., P. Garsot and J.C. Block. 1987. Cadmium uptake byPseudomonas fluorescens cells. Tox. Assess. 2: 63–78.

    Google Scholar 

  6. Belliveau, B.H., M.E. Starodub, C.M. Cotter and J.T. Trevors. 1987. Metal resistance and accumulation in bacteria. Biotech. Adv. 5: 101–127.

    Google Scholar 

  7. Bender, C.L. and D.A. Cooksey. 1986. Indigenous plasmids inPseudomonas syringae pv.tomato and conjugative transfer and role in copper resistance. J. Bacteriol. 165: 534–541.

    Google Scholar 

  8. Beswick, P.H., G.H. Hall, A.J. Hook, K. Little, D.C.H. McBrien and K.A.K. Lot. 1976. Copper toxicity: evidence for the conversion of cupric to cuprous copper in vivo under anaerobic conditions. Chem. Biol. Interact. 15: 347.

    Google Scholar 

  9. Bird, N.P., J.G. Chambers, R.W. Leech, and D. Cummins. 1985. A note on the use of metal species in microbiological tests involving growth media. J. Appl. Bacteriol. 59: 353–355.

    Google Scholar 

  10. Bitton, G. and V. Freihofer. 1978. Influence of extracellular polysaccharides on the toxicity of copper and cadmium towardKlebsiella aerogenes. Microb. Ecol. 4: 119–125.

    Google Scholar 

  11. Bovallius, A. and B. Zacharias. 1971. Variations in the metal content of some commercial media and their effect on microbial growth. Appl. Microbiol. 22: 260–262.

    Google Scholar 

  12. Brierely, C.L., D.P. Kelly, K.J. Seal and D.J. Best 1985. Materials and biotechnology. In: Biotechnology Principles and Applications (Higgins, I.J., D.J. Best and J. Jones, eds.), Blackwell Scientific Publications, Great Britain.

    Google Scholar 

  13. Calomiris, J.J., J.L. Armstrong and R.J. Seidler. 1984. Association of metal tolerance with multiple antibiotic resistance of bacteria isolated from drinking water. Appl. Environ. Microbiol. 47: 1238–1242.

    Google Scholar 

  14. Cobley, J.G. and B.A. Haddock. 1975. The respiratory chain ofThiobacillus ferrooxidans: the reduction of cytochromes by Fe2+ and the preliminary characterization of rusticyanin, a novel “blue” copper protein. FEBS Lett. 60: 29–33.

    Google Scholar 

  15. Cooksey, D.A. 1987. Characterization of a copper resistance plasmid conserved in copper-resistance strains ofPseudomonas syringae pv.tomato. Appl. Environ. Microbiol. 53: 454–456.

    Google Scholar 

  16. Cotter, C. and J.T. Trevors. 1988. Copper adsorption byEscherichia coli. System. Appl. Microbiol 13: 313–317.

    Google Scholar 

  17. Cotter, C.M., J.T. Trevors and G.M. Gadd. 1987. Decreased cupric ion uptake as the mechanism for cupric ion resistance inEscherichia coli. FEMS Microbiol. Letts. 48: 299–303.

    Google Scholar 

  18. Cox, D.P. 1979. The distribution of copper in common rocks and ore deposits. In: Copper in the Environment (Nriagu, J.O., ed.), pp. 19–42.

  19. Davis, G.K. 1974. High-level copper feeding of swine and poultry and the ecology. Fed. Proc. 33: 1194–1196.

    Google Scholar 

  20. De Rome. L. and G.M. Gadd 1987. Copper adsorption byRhizopus arrhizus, Cladosporium resinae andPenicillium italicum. Appl. Microbiol. Biotechnol. 26: 84–90.

    Google Scholar 

  21. De Rome, L. and G.M. Gadd. 1987. Measurement of copper uptake inSaccharomyces cerevisiae using a Cu2+-selective electrode. FEMS Microbiol. Lett. 43: 283–287.

    Google Scholar 

  22. DiJoseph, C.G., M.E. Bayer and A. Kaji. 1973. Host cell growth in the presence of the thermosensitive drug resistance factor, Rts 1. J. Bacteriol. 115: 399–410.

    Google Scholar 

  23. DiJoseph, C.G. and A. Kaji. 1974. The thermosensitive lesion in the replication of the drug resistance factor, Rts 1 Proc. Natl. Acad. Sci. U.S.A. 71: 2515–2519.

    Google Scholar 

  24. Domek, M.J., M.W. LeChevallier, S.C. Cameron and G.A. McFeters. 1984. Evidence for the role of copper in the injury process of coliform bacteria in drinking water. Appl. Environ. Microbiol. 48: 289–293.

    Google Scholar 

  25. Duxbury, T. 1981. Toxicity of heavy metals to soil bacteria. FEMS Microbiol. Lett. 11: 217–220.

    Google Scholar 

  26. Elek, S.D. and L. Hignery. 1970. Resistogram typin—a new epidemiological tool: application toEscherichia coli. J. Med. Microbiol. 3: 103–110.

    Google Scholar 

  27. Erardi, F.X., M.L. Failla and J.O. Falkinham III. 1987. Plasmid-encoded copper resistance and precipitation byMycobacterium scrofulaceum. Appl. Environ. Microbiol. 53: 1951–1954.

    Google Scholar 

  28. Fessenden, R.J. and J.S. Fessenden. 1976. Chemical Principles for the Life Sciences, pp 43–50, 71–77, 211–212, 221–225. Allyn and Bacon Inc., MA, U.S.A.

    Google Scholar 

  29. Flemming, C.A. 1987. Copper Chemistry and Toxicity in Freshwater Sediment. M.Sc. Thesis. University of Guelph, Guelph, Ontario. 176 pp.

    Google Scholar 

  30. Foster, T.J., 1983. Plasmid-determined resistance to antimicrobial drugs and toxic metal ions in bacteria. Microbiol Rev. 47: 361–409.

    Google Scholar 

  31. Gadd, G.M. and A.J. Griffiths. 1978. Microorganisms and heavy metal toxicity. Microb. Ecol. 4: 303–317.

    Google Scholar 

  32. Gadd, G.M. and J.L. Mowll. 1985. Copper uptake by yeastlike cells, hyphae and chlamydospores ofAureobasidium pullulans. Exp. Mycol. 9: 230–240.

    Google Scholar 

  33. Gadd, G.M. and C. White. 1985. Copper uptake byPenicillium ochrochloron: influence of pH on toxicity and demonstration of energy-dependent copper influx using protoplasts. J. Gen. Microbiol. 131: 1875–1879.

    Google Scholar 

  34. Gadd, G.M., C. White and J.L. Mowll. 1987. Heavy metal uptake by intact cells and protoplasts ofAureobasidium pullulans. FEMS Microbiol. Ecol. 45: 261–267

    Google Scholar 

  35. Goodson, M. and R.J. Rowbury. 1986. Copper sensitivity in an envelope mutant ofEscherichia coli and its suppression by Col V, 1-K94. Appl. Microbiol. 3: 35–39.

    Google Scholar 

  36. Harnett, N.M. and C.L. Gyles, 1984. Resistance to drugs and heavy metals, colicin production and biochemical characteristics off selected bovine and procineEscherichia coli strains. Appl. Environ. Microbiol. 48: 930–935.

    Google Scholar 

  37. Heukeklekian, H. and I. Gellman. 1955. Studies of biochemical oxidation by direct methods. IV. Effect of toxic metal ions on oxidation. Sew. Ind. Wastes 27: 70–84.

    Google Scholar 

  38. Ishaq, M. and A. Kaji. 1980. Mechanism of T4 phage restriction by plasmid Rts1: cleavage of T4 phage DNA by Rts1 specific enzyme. J. Biol. Chem. 255: 4040–4047.

    Google Scholar 

  39. Ishihara, M., Y. Kamio and Y. Terawaki. 1978. Cupric ion resistance as a new genetic marker of a temperature sensitive R plasmid, Rts1 inEscherichia coli. Biochem. Biophys. Res. Comm. 82: 74–80.

    Google Scholar 

  40. Itoh, Y., Y. Kamio, Y. Furuta and Y. Terawaki. 1982. Cloning of the replication and incompatibility regions of a plasmid derived from Rts1. Plasmid 8: 232–243.

    Google Scholar 

  41. Kamio, Y. and Y. Terawaki. 1977. A temperature sensitive protein in outer membrane ofEscherichia coli K12 harbouring a temperature sensitive R plasmid, Rts1. Biochem. Biophys. Res. Comm. 77: 939–946.

    Google Scholar 

  42. Koditschek, L.K. and P. Guyre. 1974. Antimicrobial resistant coliforms in New York Bight. Mar. Pollut. Bull. 5: 71–74.

    Google Scholar 

  43. Kovalenko, T.V. and G.I. Karavaiko. 1981. Effect of temperature on the resistance ofThiobacillus ferrooxidans to divalent copper ions. Mikrobiologie 50: 913–918.

    Google Scholar 

  44. Lerch, K. 1980. Copper metallothionein, a copper binding protein fromNeurospora crassa. Nature (Lond.) 284: 368–370.

    Google Scholar 

  45. Lutkenhaus, J.F. 1977. Role of a major outer membrane protein inEscherichia coli. J. Bacteriol. 131: 631–637.

    Google Scholar 

  46. MacLeod, R.A., S.C. Kuo and R. Gelinas. 1967. Metabolic injury to bacteria II: Metabolic injury induced by distilled water or Cu(II) in the plating dilutent. J. Bacteriol. 93: 961–969.

    Google Scholar 

  47. Malaney, G.W., W.D. Sheets and R. Quillin. 1959. Toxic effects of metallic ions on sewage microorganisms. Sew. Ind. Wastes 31: 1309–1315.

    Google Scholar 

  48. Maniatis, T., E.F. Fritsch and J. Sambrook. 1982. Molecular Cloning: a Laboratory Manual, Cold Spring Harbor Laboratory, New York.

    Google Scholar 

  49. Marco, G.M. and R.E. Stall. 1983. Control of bacterial spot of pepper initiated by strains ofXanthomonas compestris pv.vesicatoria that differ in sensitivity to copper Plant Disease 67: 779–781.

    Google Scholar 

  50. Matsumoto, H., Y. Kamio, R. Kobayashi and Y. Terawaki. 1978. R plasmid Rts1-mediated production of extracellular deoxyribonuclease inEscherichia coli. J. Bacteriol. 133: 387–389.

    Google Scholar 

  51. McDermott, G.N., W.A. Moore, M.A. Post and M.B. Ettinger. 1963. Effects of copper on aerobic biological sewage treatment. J. Wat. Pollut. Control Fed. 35: 226–241.

    Google Scholar 

  52. Naiki, N. 1957. Studies on the adaptation of yeast to copper XVIII. Copper-binding sulfur substances of the copper-resistant substrain. Mem. Coll. Sci. Univ. Kyoto 24: 243–248.

    Google Scholar 

  53. Naiki, N. and S. Yamagata. 1976. Isolation and some properties of copper-binding proteins found in a copperresistant strain of yeast. Plant Cell Physiol. 17: 1281–1295.

    Google Scholar 

  54. Norberg, A.B. and H. Persson. 1984. Accumulation of heavy metal ions byZoogloea ramigera. Biotech. Bioeng. 26: 239–246.

    Google Scholar 

  55. Okawa, N., H. Yoshimoto and A. Kaji. 1985. Identification of an Rts1 DNA fragment conferring temperature-dependent instability to vector plasmids. Plasmid 13: 88–98.

    Google Scholar 

  56. Olafson, R.W., S. Laya and R.G. Sim. 1980. Physiological parameters of prokaryotic metallothionein induction. Biochem. Biophys. Res. Comm. 95: 1495–1503.

    Google Scholar 

  57. Puget, K. and A.M. Michelson. 1974. Isolation of new copper-containing superoxide dismutase bacteriocuprein. Biochem. Biophys. Res. Commun. 58: 830–838.

    Google Scholar 

  58. Ramamoorthy, S. and D.J. Kushner, 1975. Binding of mercuric and other heavy metal ions by microbial growth media. Microb. Ecol. 2: 162–176.

    Google Scholar 

  59. Rickard, D.T. 1970. The Chemistry of Copper in Natural Aqueous Solutions, Almqvist and Wiksell, Stockholm.

    Google Scholar 

  60. robinson, K., S.R. Draper and A.L. Gelman. 1971. Biodegradation of pig waste: breakdown of soluble nitrogen compounds and the effect of copper. Environ. Pollut. 2: 49–56.

    Google Scholar 

  61. Rosen, B.P. 1986. Recent advances in bacterial ion transport. Ann. Rev. Microbiol. 40: 263–286.

    Google Scholar 

  62. Rossouw, F.T. and R.J. Rowbury. 1984. Effects of the resistance plasmid R124 on the level of the OmpF outer membrane protein and on the response ofEscherichia coli to environmental agents. J. Appl. Bacteriol. 56: 63–79.

    Google Scholar 

  63. Rouch, D., J. Camakaris, B.T.O. Lee and R.K.J. Luke. 1985. Inducible plasmid-mediated copper resistance inEscherichia coli. J. Gen. Microbiol. 131: 939–943.

    Google Scholar 

  64. Rudd, T., R.M. Sterritt and J.N. Lester. 1984. Formation and conditional stability constants of complexes formed between heavy metals and bacterial extracellular polymers. Water Res. 18: 379–384.

    Google Scholar 

  65. Silver, S. 1978. Transport of cations and ions. In: Bacterial Transport. Rosen, B.P. (ed.), pp. 221–324, Marcel Dekker, Inc. New York.

    Google Scholar 

  66. Silverberg, B.A., P.M. Stokes and L.B. Ferstenberg. 1976. Intranuclear complexes in a copper-tolerant green alga. J. Cell Biol. 69: 210–214.

    Google Scholar 

  67. Stall, R.E., D.C. Loschke and R.W. Rice. 1984. Conjugational transfer of copper resistance and avirulence to pepper within strains ofXanthomonas campestris pv.vesicatoria. Phytophathology 74: 797.

    Google Scholar 

  68. Steemann-Nielsen, E. and S. Wium-Andersen. 1970. Copper ions as poison in the sea and freshwater. Mar. Biol. 6: 93–97.

    Google Scholar 

  69. Summers, A.O. and S. Silver. 1978. Microbiol transformations of metals. Ann. Rev. Microbiol. 32: 637–672.

    Google Scholar 

  70. Temple, K.L. and N.W. LeRoux. 1964. Syngenesis of sulfide ores: sulfatereducing bacteria and copper toxicity. Econ. Giol. 59: 271–278.

    Google Scholar 

  71. Terawaki, Y. and R. Rownd 1972. Replication of the R factor Rts1 inProteus mirabilis. J. Bacteriol 109: 492–498.

    Google Scholar 

  72. Terawaki, Y., H. Takayasu and T. Akiba. 1967. Thermosensitive replication of a kanamycin resistance factor. J. Bacteriol. 94: 687–690.

    Google Scholar 

  73. Tetaz, T.J. and R.K.J. Luke. 1983. Plasmid-controlled resistance to copper inEscherichia coli. J. Bacteriol. 154: 1263–1268.

    Google Scholar 

  74. Tonge, G.M., D.E.F. Harrison and I.J. Higgins. 1977. Purification and properties of the methane mono-oxygenase enzyme system fromMethylosinus trichosporum OB3b. Biochem. J. 161: 333–334.

    Google Scholar 

  75. Trevors, J.T. 1987. Copper resistance in bacteria. Microbiol. Sci. 4: 29–31.

    Google Scholar 

  76. Trevors, J.T., K.M. Oddie and B.H. Belliveau. 1985. Metal resistance in bacteria. FEMS Microbiol. Rev. 32: 39–54.

    Google Scholar 

  77. Van Houwelingen, T., G.W. Canters and G. Stobbelaar. 1985. Isolation and characterization of a blue copper protein fromThiobacillus versutus Eur. J. Biochem. 153: 75–80.

    Google Scholar 

  78. Varma, M.M., W.A. Thomas and C. Prasad. 1976. Resistance to inorganic salts and antibiotics among sewage-borneEnterobacteriaceae andAchromobacteriaceae. J. Appl. Bacteriol. 41: 347–349.

    Google Scholar 

  79. Wakatsuki, T., H. Imahara, T. Kitamura and H. Tanaka. 1979. On the absorption of copper into yeast cells. Agric. Biol. Chem. 43: 1687–1692.

    Google Scholar 

  80. Weathers, P.J., R.D. Cheetham, J. Blanchard, J. Niedzielski and T.C. Crusberg. 1987. Biotraps for heavy metal removal and recovery from electroplating wastewaters. Soc. Ind. Microbiol. News 37: 9–11.

    Google Scholar 

  81. Weed, L.L. and D. Longfellow. 1954. Morphological and biochemical changes induced by copper in a population ofEscherichia coli. J. Bacteriol. 67: 27–33.

    Google Scholar 

  82. White, C. and G.M. Gadd 1986. Uptake and cellular distribution of copper, cobalt and cadmium in strains ofSaccharomyces cerevisiae cultured on elevated concentrations of these metals. FEMS Microbiol. Ecol. 38: 277–283.

    Google Scholar 

  83. Yamamoto, T., T. Yokota and A. Kaji. 1977. Requirement of cyclic adenosine 3′, 5′-monophosphate for the thermosensitive effects of Rts1 in a cyclic adenosine 3′5′-monophosphate-less mutant ofEscherichia coli. J. Bacteriol. 132: 80–89

    Google Scholar 

  84. Yates, J.R., J.H. Lobos and D.S. Holmes. 1986. The use of genetic probes to detect microorganisms in biomining operations. J. Ind. Microbiol. 1: 129–135.

    Google Scholar 

  85. Zevenhuizen, L.P.T.M., J. Dolfing, E.J. Eshius and I.J. Scholten-Koerselman. 1979. Inhibitory effects of copper on bacteria related to free ion concentration. Microb. Ecol. 5: 139–146.

    Google Scholar 

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  1. Department of Environmental Biology, University of Guelph, N1G 2WI, Guelph, Ontario, Canada

    J. T. Trevors & C. M. Cotter

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Trevors, J.T., Cotter, C.M. Copper toxicity and uptake in microorganisms. Journal of Industrial Microbiology 6, 77–84 (1990). https://doi.org/10.1007/BF01576426

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Key words

  • Copper
  • Cofactor
  • Copper-resistance mechanisms
  • Toxicity
  • Microorganisms