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Copper-resistant bacteria from industrial effluents and their role in remediation of heavy metals in wastewater

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Abstract

Six copper-resistant bacterial strains were isolated from wastewater of tanneries of Kasur and Rohi Nala. Two strains tolerated copper at 380 mg/L, four up to 400 mg/L. Three strains were identified as members of the genusSalmonella; one strain was identified asStreptococcus pyrogenes, one asVagococcus fluvialis and the last was identified asEscherichia coli. The pH and temperature optimum for two of them were 7.0 and 30 °C, respectively; four strains had corresponding optima at 7.5 and 37 °C, respectively. All bacterial isola-tes showed resistance against Ag+ (280–350 mg/L), Co2+ (200–420), CrVI (280–400), Cd2+ (250–350), Hg2+ (110–200), Mn2+ (300–380), Pb2+ (300–400), Sn2+ (480–520) and Zn2+ (300–450). Largesized plasmids (>20 kb), were detected in all of the strains. After the isolates were cured of plasmids with ethidium bromide, the efficiency of curing was estimated in the range of 60–90%. Reference strain ofE. coli was transformed with the plasmids of the bacterial isolates which grew in Luria-Bertani medium containing 100 mg/L Cu2+. The capability to adsorb and afterwards accumulate Cu2+ inside their cells was assayed by atomic absorption spectrophotometer; all bacterial cells had the ability to adsorb 50–80 % of the Cu2+ and accumulate 30–45 % Cu2+ inside them after 1 d of incubation.

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References

  • Aiking H., Grover H., Vantriet J.: Detoxification of mercury, cadmium and lead inKlebsiella aerogenes NCTC 418 growing in continuous culture.Appl. Environ. Microbiol. 50, 1262–1267 (1985).

    PubMed  CAS  Google Scholar 

  • Aviles M., Codina J.C., Perez-Garcia A., Cazorla F., Romero P., De Vincente A.: Occurrence of resistance to antibiotics and metals and of plasmids in bacterial strains isolated from marine environment, pp. 475–478 in R.W. Morris, W.O.K. Grabow, A.P. Dufour (Eds):Health Related Water Microbiology, Vol. 27. Pergamon Press, Oxford (UK) 1993.

    Google Scholar 

  • Anisimova L.A., Boronin A.M.: Resistance to metal determined by plasmid of Gram-negative bacteria.Mol. Gen. Microbiol. 12, 3–9 (1994).

    Google Scholar 

  • Bender J., Lee R.F., Philips P.: Uptake and transformation of metals and metalloids by microbial mats and their use in bioremediation.Industr. Microbiol. 14, 113–118 (1995).

    Article  CAS  Google Scholar 

  • Beach I.R., Palmiter R.D.: Amplification ofMT-1 gene in cadmium resistant mouse cells.Proc. Nat. Acad. Sci. USA 78, 2100–2114 (1981).

    Article  Google Scholar 

  • Benson H.J.:Microbiological Applications, Complete Version. Laboratory Manual in General Microbiology. W.C. Brown Publishers, Dubuque (USA) 1994.

    Google Scholar 

  • Brown T.A., Smith D.G.: The effect of silver nitrate on the growth and ultrastructure, of yeastCryptococcus albidus.Microbios Lett. 3, 155–162 (1976).

    CAS  Google Scholar 

  • Capasso C., Nazzaro F., Marulli F., Capasso A., La Cara F., Parisi E.: Identification of high-molecular weight cadmium-binding protein in copper-resistantBacillus acidocaldarius cells.Res. Microbiol. 147, 287–296 (1996).

    Article  PubMed  CAS  Google Scholar 

  • Cervantes C., Silver S.: Metal resistant system inPseudomonas.Rev. Latinoam. Microbiol. 38, 45–64 (1996).

    PubMed  CAS  Google Scholar 

  • Cheesbrough M.:Medical Laboratory Manual for Tropical Countries, Vol. 2, Microbiology. ELBS University Press, Cambridge (UK) 1993.

    Google Scholar 

  • Collee J. G., Marr W.: Culture containers and culture media, pp. 100–120 in J.G. Collee, J.P. Duguid, A.G. Fraser, B.P. Marmion (Eds):Mackie and MacCartney Practical Medical Microbiology, Vol. 2. Churchill Livingstone, Medical Division of Longman Group, Edinburgh-London-Melbourne-New York 1998.

    Google Scholar 

  • Cooksey D.A.: Copper up take and resistance in bacteria.Mol. Microbiol. 7, 1–5 (1993).

    Article  PubMed  CAS  Google Scholar 

  • Cooksey D.A.: Molecular mechanisms of copper resistance and accumulation in bacteria.FEMS. Microbiol. Rev. 14, 381–386 (1994).

    Article  PubMed  CAS  Google Scholar 

  • Crosa J.H., Tolmasky M.E., Actis L.A., Falkow S.: Plasmids, pp. 365–386 in P. Gerhardt, R.G.S. Murray, W.A. Wood, N.R. Kreig (Eds).Methods for General and Molecular Biology. American Society for Microbiology, Washington (DC) 1994.

    Google Scholar 

  • Collard J.M., Corbisier P., Diels L., Dong Q., Jeanthon C., Mergeay M., Taghavi S., Van Der Lelie, D., Wilmotte A., Wuertz S.M.: Plasmids for heavy metal resistance inAlcaligenes eutrophus CH34 mechanisms and applications.FEMS Microbiol. Rev. 14, 405–414 (1994).

    Article  PubMed  CAS  Google Scholar 

  • Fitch M.W., Graham D.W., Arnold R.G., Agarwal S.K., Phelps P.: Phenotypic characterization of copper resistant mutants ofMethylosinus trichosporium.Appl. Environ. Microbiol. 59, 2771–2776 (1993).

    PubMed  CAS  Google Scholar 

  • Fong S.T., Camakaris J., Lee B.T.: Molecular genetics of a chromosomal locus involved in copper tolerance inEscherichia coli K12.Mol. Microbiol. 15, 1127–1137 (1995).

    Article  PubMed  CAS  Google Scholar 

  • Foster T.J.: Plasmid determined resistance to antimicrobial drugs and external ions in bacteria.Microbiol. Rev. 47, 361–409 (1983).

    PubMed  CAS  Google Scholar 

  • Fostner U., Wittman G.T.W.:Metal Pollution in the Aquatic Environment. Springer-Verlag, New York 1997.

    Google Scholar 

  • Francis A.J.: Microbial dissolution and stabilization of toxic metals and radionuclides in mixed wastes.Experientia 46, 840–851 (1990).

    Article  CAS  Google Scholar 

  • Gadd G.M.: Heavy metal accumulation by bacteria and other microorganisms.Appl. Environ. Microbiol. 46, 834–840 (1990).

    CAS  Google Scholar 

  • Ge Z., Hiratsuka K., Taylor D.E.: Nucleotide sequence and mutational analysis indicate that twoHelicobacter pylori gene encode aP-type ATPase and cation-binding protein associated with copper transport.Mol. Microbiol. 15, 97–106 (1995).

    Article  PubMed  CAS  Google Scholar 

  • Gómez M.A., Gonzalez-López J., Calvo C.: Antibiotic resistance patterns of coliforms isolated from six protected wetlands in the southeast of Spain.Folia Microbiol. 45, 555–560 (2000).

    Google Scholar 

  • Gordon A.S., Harword V.J., Sayar S.: Growth, copper tolerant cells and extracellular protein production in copper stressed chemostat cultures ofVibrio alginolyticus.Appl. Environ. Microbiol. 59, 60–66 (1993).

    PubMed  CAS  Google Scholar 

  • Grindle M.: Isolation and characterization of vinclozolin resistant mutants ofNeurospora crassa.Trans. Brit. Mycol. Soc. 82, 635–643 (1984).

    CAS  Google Scholar 

  • Gupta S.D., Lee B.T., Camakaris J., Wu H.C.: Identification ofcutC andcutF (nlpE) genes involved in copper tolerance inEscherichia coli.J. Bacteriol. 177, 4207–4215 (1995).

    PubMed  CAS  Google Scholar 

  • Haq R.U., Rehman A., Shakoori A.R.: Effect of dichromate on population and growth of various protozoa isolated from industrial effluents.Folia Microbiol. 45, 275–280 (2000).

    CAS  Google Scholar 

  • Haq R., Shakoori A.R.: Identification and characterization of plasmid born genes ofThiobacillus ferrooxidans and their implication in improvement of metal recovery operations.Pakistan J. Zool. 29, 1–6 (1997).

    CAS  Google Scholar 

  • Hefnawy M.A., Razak A.A.: Alteration of cell-wall composition ofFusarium oxysporum, by copper stress.Folia Microbiol. 43, 453–458 (1998).

    CAS  Google Scholar 

  • Higham D.P., Sadler P.J., Scawen M.D.: Cadmium resistantPseudomonas putida synthesizes novel cadmium proteins.Science 225, 1043–1046 (1984).

    Article  PubMed  CAS  Google Scholar 

  • Hildebrand C.E., Griffith J.K., Tobey R.A., Walkers R.A., Enger M.D.: Molecular mechanisms of Cd detoxification in Cd-resistant cultured cells, role of metallothioneins and other inducible factors.Rev. Toxicol. Environ. Sci. 9, 279–303 (1982).

    CAS  Google Scholar 

  • Holmes D.S.: Improved rapid techniques for screening recombinant DNA plasmid inE. coli.Biotechniques 2, 68–69 (1984).

    CAS  Google Scholar 

  • Hong Y.C., Azad H.R., Cooksey D.A.: A chromosomal locus required for copper resistance, competitive fitness and cytochromec biogenesis inPseudomonas fluorescens.Proc. Nat. Acad. Sci. USA 93, 7315–7320 (1996).

    Article  Google Scholar 

  • Inniss W.E., Ingraham J.L.: Microbial life at low temperature, mechanisms and molecular aspects, pp. 73–104 in D.J. Kushner (Ed.):Microbial Life in Extreme Environment. Academic Press, New York 1978.

    Google Scholar 

  • Jt G., Silver S.: Bacterial resistance mechanisms for heavy metals of environment concern.J. Industr. Microbiol. 14, 61–75 (1995).

    Article  Google Scholar 

  • Kim B.K., De Macario, E.C., Nolling J., Daniels L.: Isolation and characterization of copper resistant methanogen from a copper mining soil sample.Appl. Environ. Microbiol. 62, 2629–2635 (1996).

    PubMed  CAS  Google Scholar 

  • Kozdroj J.: Microbial responses to single or successive soil contamination with Cd2+ or Cu2+.Soil Biol. Biochem. 27, 1459–1465 (1995).

    Article  CAS  Google Scholar 

  • Laddaga R.A., Silver S.: Cadmium uptake inE. coli K-12.J. Bacteriol. 162, 1100–1105 (1986).

    Google Scholar 

  • Lakshami V.V., Sridhar P., Khan T.B., Polasa H.: Mixed-ligand complexes of platinumII as curing agents for pBP322 and pBR329 (Co/EI) plasmids inEscherichia coli.J. Gen. Microbiol. 134, 1977–1981 (1988).

    Google Scholar 

  • Ledin M., Pedersen K., Allard B.: Effect of pH and ionic strength on the adsorption of Cs, Sr, Eu, Zn, Cd and Hg byPseudomonas putida.Water Air Soil Pollut. 93, 367–381 (1997).

    CAS  Google Scholar 

  • Lin C., Olson B.H.: Occurrence ofcop-like copper-resistance gene among bacteria isolated from a water distribution system.Can. J. Microbiol. 41, 642–646 (1995).

    Article  CAS  Google Scholar 

  • Maniatis T., Fritsch E.F., Sambrook J.:Molecular Cloning. A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor 1989.

    Google Scholar 

  • Mergeay M.: Towards an understanding of the genetics of bacterial metal resistance.Trends Biotech. 9, 17–24 (1991).

    Article  CAS  Google Scholar 

  • Morley G.F., Gadd G.M.: Sorption of toxic metals by fungi and clay minerals.Mycol. Res. 99, 1429–1438 (1995).

    CAS  Google Scholar 

  • Mullen M.D., Wolf D.C., Ferris F.G., Beveridge T.J., Flemming C.A., Baylay G.W.: Bacterial sorption of heavy metals.Appl. Environ. Microbiol. 55, 3143–3149 (1989).

    PubMed  CAS  Google Scholar 

  • Neito J.J., Ventosa A., Montero C.G., Ruiz-Berraquero F.: Toxicity of heavy metals to archaebacterial halococci.Syst. Appl. Microbiol. 11, 116–120 (1989).

    Google Scholar 

  • Nies D.H., Silver S.: Ion efflux system involved in bacterial metal resistance.J. Industr. Microbiol. 14, 186–199 (1995).

    Article  CAS  Google Scholar 

  • Ohman D.E.:Experiments in Gene Manipulation. Prentice Hall, New York 1988.

    Google Scholar 

  • Olukoya D.K., Smith S.I., Ilori M.O.: Isolation and characterization of heavy metal resistant bacteria from Lagos Lagoon.Folia Microbiol. 42, 441–444 (1997).

    CAS  Google Scholar 

  • Patterson D., Gillespie D.: Effect of elevated temperature on protein synthesis inE. coli.J. Bacteriol. 112, 117–118 (1972).

    Google Scholar 

  • Phelps P.A., Agarwal S.K., Speitel G.E., Georgiou G., Speitel G.E. Jr.: Phenotypic characterization of copper resistant mutants ofMethylosinus trichosporium.Appl. Environ. Microbiol. 58, 3701–3708 (1993).

    Google Scholar 

  • Rani D.B., Mahadevan A.: Patterns of heavy metal resistance in marinePseudomonas MRI.Indian J. Exp. Biol. 31, 682–686 (1993).

    PubMed  CAS  Google Scholar 

  • Robinson J.B., Tuovinen O.H.: Mechanisms of microbial resistance and detoxification of mercury and organomercury compounds: physiological, biochemical and genetic analysis.Microbiol. Rev. 48, 95–124 (1984).

    PubMed  CAS  Google Scholar 

  • Shakoori A.R., Tahseen S., Haq R.U.: Chromium-tolerant bacteria isolated from industrial efluents and their use in detoxication of hexavalent chromium.Folia Microbiol. 44, 50–54 (1999).

    Article  CAS  Google Scholar 

  • Silver S.: Exploiting heavy metal resistance systems in bioremediation.Res. Microbiol. 145, 61–66 (1994).

    Article  PubMed  CAS  Google Scholar 

  • Silver S.: Bacterial resistance to toxic metal ions.Gene 179, 9–19 (1996).

    Article  PubMed  CAS  Google Scholar 

  • Silver S.: Gene for all metals: a bacterial view of the periodic table.J. Industr. Microbiol. Biotechnol. 20, 1–12 (1998).

    Article  CAS  Google Scholar 

  • Silver S., Ji G.: Newer systems for bacterial resistance to toxic heavy metals.Environ. Health Perspect. 102, 107–113 (1994).

    Article  PubMed  CAS  Google Scholar 

  • Silver S., Phung L.T.: Bacterial heavy metal resistance—new surprises.Ann. Rev. Microbiol. 50, 753–789 (1996).

    Article  CAS  Google Scholar 

  • Simkiss K., Watkins B.: Differences in zinc uptake between snails (Helix aspersa) from metal and bacterial polluted sites.Funct. Ecol. 5, 787–794 (1991).

    Article  Google Scholar 

  • Sundin G.W., Bender C.L.: Ecological and genetic analysis of copper and streptomycin resistance inPseudomonas syringae.Appl. Environ. Microbiol. 59, 1018–1024 (1996).

    Google Scholar 

  • Thiele D.J.:Metal Detoxification in Eukaryotic Cells. Crisp Data Base of National Institute of Health, Washington (DC) 1995.

    Google Scholar 

  • Traianovska S., Britz M.L., Bhave M.: Detection of heavy metal ion resistance genes in Gram-positive and Gram-negative bacteria isolated from lead contaminated site.Biodegradation 8, 113–124 (1997).

    Article  Google Scholar 

  • Tsekova K.V., Marinov P.G., Tzekova A.N.: Copper accumulation byAspergillus awamori.Folia Microbiol. 45, 217–220 (2000a)

    CAS  Google Scholar 

  • Tsekova K., Dentchev D., Todorova D.: Effect of cadmium and copper on the production of citric acid byAspergillus niger.Folia Microbiol. 45, 331–334 (2000b).

    Article  CAS  Google Scholar 

  • Verma S.K., Singh S.P.: Multiple metal resistance in the cyanobacteriumNostoc muscorum.Bull Environ. Contam. Toxicol. 54, 614–619 (1995).

    Article  PubMed  CAS  Google Scholar 

  • Vievskii A.N.: The synergistic action of quaternary ammonium derivatives and inhibitors of nitrate reduction in respect toPseudomonas aeruginosa 1.Mikrobiol. Z 56, 16–20 (1994).

    PubMed  CAS  Google Scholar 

  • Williams J.R., Morgan A.G., Rouch D.A., Brown N.L., Lee B.T.O.: Copper resistant enteric bacteria from United Kingdom and Australian piggeries.Appl. Environ. Microbiol. 59, 2531–2537 (1993).

    PubMed  CAS  Google Scholar 

  • Yang C.H., Azad H.R., Cooksey D.A.: A chromosomal locus required for copper resistance.Proc. Nat. Acad. Sci. USA 93, 7315–7320 (1996).

    Article  PubMed  CAS  Google Scholar 

  • Yoneyama H., Nakae T.: Protein C (OprC) of the outer membrane ofPseudomonas aeruginosa is a copper-regulated channel protein.Microbiology 142, 2137–2144 (1996).

    Article  PubMed  CAS  Google Scholar 

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  1. Cell and Molecular Biology Laboratory, Department of Zoology, University of the Punjab, New Campus, 54590, Lahore, Pakistan

    A. R. Shakoori & B. Muneer

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  1. A. R. Shakoori
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Shakoori, A.R., Muneer, B. Copper-resistant bacteria from industrial effluents and their role in remediation of heavy metals in wastewater. Folia Microbiol 47, 43–50 (2002). https://doi.org/10.1007/BF02818564

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