Biology of Metals

, Volume 4, Issue 2, pp 100–106 | Cite as

Silver tolerance and accumulation in yeasts

  • Martin Kierans
  • A. Morven Staines
  • Heather Bennett
  • Geoffrey M. Gadd
Original Articles


Debaryomyces hansenii (NCYC 459 and strain 75-21),Candida albicans (3153A),Saccharomyces cerevisiae (X2180-1B),Rhodotorula rubra (NCYC 797) andAureobasidium pullulans (IMI 45533 and ATCC 42371) were grown on solid medium supplemented with varying concentrations of AgNO3. Although Ag+ is highly toxic towards yeasts, growth on solid media was still possible at Ag concentrations of 1–2 mM. Further subculture on higher Ag concentrations (up to 5 mM) resulted in elevated tolerance. The extent of Ag tolerance depended on whether Ag-containing plates were exposed to light prior to inoculation since light-mediated reduction of Ag+ to Ag0 resulted in the production of a less toxic silver species. Experimental organisms exhibited blackening of colonies and the surrounding agar during growth on AgNO3-containing medium especially at the highest Ag concentrations tested. All organisms accumulated Ag from the medium; electron microscopy revealed that silver was deposited as electron-dense granules in and around cell walls and in the external medium. X-ray microprobe analysis indicated that these granules were metallic Ag0 although AgCl was also present in some organisms. Volatile and non-volatile reducing compounds were produced by several test organisms which presumably effected Ag+ reduction to Ag0.

Key words

Silver tolerance Silver accumulation Yeasts 


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  1. Belly RT, Kydd GC (1982) Silver resistance in microorganisms. Dev Ind Microbiol 23:567–577Google Scholar
  2. Brown TA, Smith DG (1976) The effects of silver nitrate on the growth and ultrastructure of the yeastCryptococcus albidus. Microbios Lett 3:155–162Google Scholar
  3. Charley RC, Bull AT (1979) Bioaccumulation of silver by a multispecies community of bacteria. Arch Microbiol 123:239–244PubMedGoogle Scholar
  4. Gadd GM, Griffiths AJ (1978) Microorganisms and heavy metal toxicity. Microb Ecol 4:303–317Google Scholar
  5. Gadd GM, Laurence OS, Briscoe PA, Trevors JT (1989) Silver accumulation inPseudomonas stutzeri AG259. Biol Metals 2:168–173Google Scholar
  6. Ghandour W, Hubbard JA, Deistung J, Hughes MN, Poole RK (1988) The uptake of silver ions byEscherichia coli K12: toxic effects and interaction with copper ions. Appl Microbiol Biotechnol 28:559–565Google Scholar
  7. Goddard PA, Bull AT (1989a) The isolation and characterisation of bacteria capable of accumulating silver. Appl Microbiol Biotechnol 31:308–313Google Scholar
  8. Goddard PA, Bull AT (1989b) Accumulation of silver by growing and non-growing populations ofCitrobacter intermedius B6. Appl Microbiol Biotechnol 31:314–319Google Scholar
  9. Greenwood NN, Earnshaw A (1984) Chemistry of the elements. Pergamon Press, OxfordGoogle Scholar
  10. Haefeli C, Franklin C, Hardy K (1984) Plasmid determined silver resistance inPseudomonas stutzeri isolated from a silver mine. J Bacteriol 158:389–392PubMedGoogle Scholar
  11. Kaur P, Vadhera DV (1986). Mechanisms of resistance to silver ions inKlebsiella pneumoniae. Antimicrob Agents Chemother 29:165–167PubMedGoogle Scholar
  12. Pighi L, Pumpel T, Schinner F (1989) Selective accumulation of silver by fungi. Biotechnol Lett 11:275–280Google Scholar
  13. Pumpel T, Schinner F (1986) Silver tolerance and silver accumulation of microorganisms from soil materials of a silver mine. Appl Microbiol Biotechnol 24:244–247Google Scholar
  14. Silver S (1983) Bacterial interactions with mineral cations and anions: good ions and bad. In: Westbroek P, De Jong EW (eds) Biomineralisation and biological metal accumulation. Reidel, Dordrecht, pp 439–457Google Scholar
  15. Starodub ME, Trevors JT (1989) Silver, resistance inEscherichia coli R1. J Med Microbiol 29:101–110PubMedGoogle Scholar
  16. Strandberg GW, Shumate SE, Parrott JR (1981) Accumulation of uranium bySaccharomyces cerevisiae andPseudomonas aeruginosa. Microbial cells as biosorbents for heavy metals. Appl Environ Microbiol 41:237–245Google Scholar
  17. Tilton RC, Rosenberg B (1978) Reversal of the silver inhibition of microorganisms by agar. Appl Environ Microbiol 35:1116–1120PubMedGoogle Scholar
  18. Trevors JT (1987) Silver resistance and accumulation in bacteria. Enzyme Microb Technol 9:331–333Google Scholar
  19. Trevors JT, Oddie KM, Belliveau BH (1985) Metal resistance in bacteria. FEMS Microbiol Rev 32:39–54Google Scholar

Copyright information

© Springer-Verlag 1991

Authors and Affiliations

  • Martin Kierans
    • 1
  • A. Morven Staines
    • 1
  • Heather Bennett
    • 1
  • Geoffrey M. Gadd
    • 1
  1. 1.Department of Biological SciencesUniversity of DundeeDundeeUK

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