, Volume 26, Issue 4, pp 609–621 | Cite as

Antimicrobial silver: uses, toxicity and potential for resistance

  • Kristel Mijnendonckx
  • Natalie Leys
  • Jacques Mahillon
  • Simon Silver
  • Rob Van HoudtEmail author


This review gives a comprehensive overview of the widespread use and toxicity of silver compounds in many biological applications. Moreover, the bacterial silver resistance mechanisms and their spread in the environment are discussed. This study shows that it is important to understand in detail how silver and silver nanoparticles exert their toxicity and to understand how bacteria acquire silver resistance. Silver ions have shown to possess strong antimicrobial properties but cause no immediate and serious risk for human health, which led to an extensive use of silver-based products in many applications. However, the risk of silver nanoparticles is not yet clarified and their widespread use could increase silver release in the environment, which can have negative impacts on ecosystems. Moreover, it is shown that silver resistance determinants are widely spread among environmental and clinically relevant bacteria. These resistance determinants are often located on mobile genetic elements, facilitating their spread. Therefore, detailed knowledge of the silver toxicity and resistance mechanisms can improve its applications and lead to a better understanding of the impact on human health and ecosystems.


Silver Silver nanoparticles Resistance Toxicity 



This work was supported by the European Space Agency (ESA-PRODEX) and the Belgian Science Policy (Belspo) through the COMICS project (C90356). Kristel Mijnendonckx is a Ph.D student at the Laboratory of Food and Environmental Microbiology (Université catholique de Louvain, Belgium), and at the Unit of Microbiology (SCK•CEN, Belgium). KM is financed through the COMICS project and an AWM Ph.D Grant from SCK•CEN.


  1. Alexander JW (2009) History of the medical use of silver. Surg Infect (Larchmt) 10:289–292CrossRefGoogle Scholar
  2. Alonso A, Rojo F, Martinez JL (1999) Environmental and clinical isolates of Pseudomonas aeruginosa show pathogenic and biodegradative properties irrespective of their origin. Environ Microbiol 1:421–430PubMedCrossRefGoogle Scholar
  3. Aminov RI (2011) Horizontal gene exchange in environmental microbiota. Front Microbiol 2:158PubMedCrossRefGoogle Scholar
  4. Baker-Austin C, Wright MS, Stepanauskas R, McArthur JV (2006) Co-selection of antibiotic and metal resistance. Trends Microbiol 14:176–182PubMedCrossRefGoogle Scholar
  5. Bragg PD, Rainnie DJ (1974) Effect of silver ions on the respiratory chain of Escherichia coli. Can J Microbiol 20:883–889PubMedCrossRefGoogle Scholar
  6. Bryan GW, Langston WJ (1992) Bioavailability, accumulation and effects of heavy metals in sediments with special reference to United Kingdom estuaries: a review. Environ Pollut 76:89–131PubMedCrossRefGoogle Scholar
  7. Cabiscol E, Tamarit J, Ros J (2000) Oxidative stress in bacteria and protein damage by reactive oxygen species. Int Microbiol 3:3–8PubMedGoogle Scholar
  8. Caille O, Rossier C, Perron K (2007) A copper-activated two-component system interacts with zinc and imipenem resistance in Pseudomonas aeruginosa. J Bacteriol 189:4561–4568PubMedCrossRefGoogle Scholar
  9. Chambers C, Proctor C, Kabler P (1962) Bactericidal effect of low concentrations of silver. Am Water Works Assoc 54:208–216Google Scholar
  10. Chopra I (2007) The increasing use of silver-based products as antimicrobial agents: a useful development or a cause for concern? J Antimicrob Chemother 59:587–590PubMedCrossRefGoogle Scholar
  11. Choudhury P, Kumar R (1998) Multidrug- and metal-resistant strains of Klebsiella pneumoniae isolated from Penaeus monodon of the coastal waters of deltaic Sundarban. Can J Microbiol 44:186–189PubMedGoogle Scholar
  12. Coenye T, Spilker T, Reik R, Vandamme P, Lipuma JJ (2005) Use of PCR analyses to define the distribution of Ralstonia species recovered from patients with cystic fibrosis. J Clin Microbiol 43:3463–3466PubMedCrossRefGoogle Scholar
  13. Cunningham JH, Lin LS (2010) Fate of amoxicillin in mixed-culture bioreactors and its effects on microbial growth and resistance to silver ions. Environ Sci Technol 44:1827–1832PubMedCrossRefGoogle Scholar
  14. Davis IJ, Richards H, Mullany P (2005) Isolation of silver- and antibiotic-resistant Enterobacter cloacae from teeth. Oral Microbiol Immunol 20:191–194PubMedCrossRefGoogle Scholar
  15. De Gusseme B, Hennebel T, Christiaens E, Saveyn H, Verbeken K, Fitts JP, Boon N, Verstraete W (2011) Virus disinfection in water by biogenic silver immobilized in polyvinylidene fluoride membranes. Water Res 45:1856–1864PubMedCrossRefGoogle Scholar
  16. Deshpande LM, Chopade BA (1994) Plasmid mediated silver resistance in Acinetobacter baumannii. Biometals 7:49–56PubMedCrossRefGoogle Scholar
  17. Dibrov P, Dzioba J, Gosink KK, Hase CC (2002) Chemiosmotic mechanism of antimicrobial activity of Ag+ in Vibrio cholerae. Antimicrob Agents Chemother 46:2668–2670PubMedCrossRefGoogle Scholar
  18. Dieppois G, Ducret V, Caille O, Perron K (2012) The transcriptional regulator CzcR modulates antibiotic resistance and quorum sensing in Pseudomonas aeruginosa. PLoS One 7:e38148PubMedCrossRefGoogle Scholar
  19. Drake PL, Hazelwood KJ (2005) Exposure-related health effects of silver and silver compounds: a review. Ann Occup Hyg 49:575–585PubMedCrossRefGoogle Scholar
  20. Edwards-Jones V (2009) The benefits of silver in hygiene, personal care and healthcare. Lett Appl Microbiol 49:147–152PubMedCrossRefGoogle Scholar
  21. El Badawy AM, Luxton TP, Silva RG, Scheckel KG, Suidan MT, Tolaymat TM (2010) Impact of environmental conditions (pH, ionic strength, and electrolyte type) on the surface charge and aggregation of silver nanoparticles suspensions. Environ Sci Technol 44:1260–1266PubMedCrossRefGoogle Scholar
  22. El Badawy AM, Silva RG, Morris B, Scheckel KG, Suidan MT, Tolaymat TM (2011) Surface charge-dependent toxicity of silver nanoparticles. Environ Sci Technol 45:283–287PubMedCrossRefGoogle Scholar
  23. Elechiguerra JL, Burt JL, Morones JR, Camacho-Bragado A, Gao X, Lara HH, Yacaman MJ (2005) Interaction of silver nanoparticles with HIV-1. J Nanobiotechnology 3:6PubMedCrossRefGoogle Scholar
  24. Fabrega J, Luoma SN, Tyler CR, Galloway TS, Lead JR (2011) Silver nanoparticles: behaviour and effects in the aquatic environment. Environ Int 37:517–531PubMedCrossRefGoogle Scholar
  25. Flegal AR, Brown CL, Squire S, Ross JR, Scelfo GM, Hibdon S (2007) Spatial and temporal variations in silver contamination and toxicity in San Francisco Bay. Environ Res 105:34–52PubMedCrossRefGoogle Scholar
  26. Franke S (2007) Microbiology of the toxic noble metal silver. In: Nies D, Silver S (eds) Molecular biology of heavy metals. Microbiology monographs. Springer, BerlinGoogle Scholar
  27. Franke S, Grass G, Nies DH (2001) The product of the ybdE gene of the Escherichia coli chromosome is involved in detoxification of silver ions. Microbiology 147:965–972PubMedGoogle Scholar
  28. Franke S, Grass G, Rensing C, Nies DH (2003) Molecular analysis of the copper-transporting efflux system CusCFBA of Escherichia coli. J Bacteriol 185:3804–3812PubMedCrossRefGoogle Scholar
  29. Gordon O, Vig Slenters T, Brunetto PS, Villaruz AE, Sturdevant DE, Otto M, Landmann R, Fromm KM (2010) Silver coordination polymers for prevention of implant infection: thiol interaction, impact on respiratory chain enzymes, and hydroxyl radical induction. Antimicrob Agents Chemother 54:4208–4218PubMedCrossRefGoogle Scholar
  30. Goris J, De Vos P, Coenye T, Hoste B, Janssens D, Brim H, Diels L, Mergeay M, Kersters K, Vandamme P (2001) Classification of metal-resistant bacteria from industrial biotopes as Ralstonia campinensis sp. nov., Ralstonia metallidurans sp. nov. and Ralstonia basilensis Steinle et al. 1998 emend. Int J Syst Evol Microbiol 51:1773–1782PubMedCrossRefGoogle Scholar
  31. Gudipaty SA, Larsen AS, Rensing C, McEvoy MM (2012) Regulation of Cu(I)/Ag(I) efflux genes in Escherichia coli by the sensor kinase CusS. FEMS Microbiol Lett 330:30–37PubMedCrossRefGoogle Scholar
  32. Gupta A, Maynes M, Silver S (1998) Effects of halides on plasmid-mediated silver resistance in Escherichia coli. Appl Environ Microbiol 64:5042–5045PubMedGoogle Scholar
  33. Gupta A, Matsui K, Lo JF, Silver S (1999) Molecular basis for resistance to silver cations in Salmonella. Nat Med 5:183–188PubMedCrossRefGoogle Scholar
  34. Gupta A, Phung LT, Taylor DE, Silver S (2001) Diversity of silver resistance genes in IncH incompatibility group plasmids. Microbiology 147:3393–3402PubMedGoogle Scholar
  35. Haefeli C, Franklin C, Hardy K (1984) Plasmid-determined silver resistance in Pseudomonas stutzeri isolated from a silver mine. J Bacteriol 158:389–392PubMedGoogle Scholar
  36. Hayashi M, Miyoshi T, Sato M, Unemoto T (1992) Properties of respiratory chain-linked Na+-independent NADH-quinone reductase in a marine Vibrio alginolyticus. Biochim Biophys Acta 1099:145–151PubMedCrossRefGoogle Scholar
  37. Heuer H, Kopmann C, Binh CT, Top EM, Smalla K (2009) Spreading antibiotic resistance through spread manure: characteristics of a novel plasmid type with low %G+C content. Environ Microbiol 11:937–949PubMedCrossRefGoogle Scholar
  38. Holland SL, Dyer PS, Bond CJ, James SA, Roberts IN, Avery SV (2011) Candida argentea sp. nov., a copper and silver resistant yeast species. Fungal Biol 115:909–918PubMedCrossRefGoogle Scholar
  39. Jain PK, Huang XH, El-Sayed IH, El-Sayed MA (2008) Noble metals on the nanoscale: optical and photothermal properties and some applications in imaging, sensing, biology, and medicine. Acc Chem Res 41:1578–1586PubMedCrossRefGoogle Scholar
  40. Janssen PJ, Van Houdt R, Moors H, Monsieurs P, Morin N, Michaux A, Benotmane MA, Leys N, Vallaeys T, Lapidus A, Monchy S, Medigue C, Taghavi S, McCorkle S, Dunn J, van der Lelie D, Mergeay M (2010) The complete genome sequence of Cupriavidus metallidurans strain CH34, a master survivalist in harsh and anthropogenic environments. PLoS One 5:e10433PubMedCrossRefGoogle Scholar
  41. Jelenko C 3rd (1969) Silver nitrate resistant E. coli: report of case. Ann Surg 170:296–299PubMedCrossRefGoogle Scholar
  42. Jung WK, Kim SH, Koo HC, Shin S, Kim JM, Park YK, Hwang SY, Yang H, Park YH (2007) Antifungal activity of the silver ion against contaminated fabric. Mycoses 50:265–269PubMedCrossRefGoogle Scholar
  43. Kaegi R, Voegelin A, Ort C, Sinnet B, Thalmann B, Krismer J, Hagendorfer H, Elumelu M, Mueller E (2013) Fate and transformation of silver nanoparticles in urban wastewater systems. Water Res. doi: 10.1016/j.watres.2012.11.060 Google Scholar
  44. Kim JY, Lee C, Cho M, Yoon J (2008) Enhanced inactivation of E. coli and MS-2 phage by silver ions combined with UV-A and visible light irradiation. Water Res 42:356–362PubMedCrossRefGoogle Scholar
  45. Klasen HJ (2000) Historical review of the use of silver in the treatment of burns. I. Early uses. Burns 26:117–130PubMedCrossRefGoogle Scholar
  46. Klaus T, Joerger R, Olsson E, Granqvist CG (1999) Silver-based crystalline nanoparticles, microbially fabricated. Proc Natl Acad Sci U S A 96:13611–13614PubMedCrossRefGoogle Scholar
  47. Kremer AN, Hoffmann H (2012) Subtractive hybridization yields a silver resistance determinant unique to nosocomial pathogens in the Enterobacter cloacae complex. J Clin Microbiol 50:3249–3257PubMedCrossRefGoogle Scholar
  48. Kumar CG, Mamidyala SK (2011) Extracellular synthesis of silver nanoparticles using culture supernatant of Pseudomonas aeruginosa. Colloids Surf B Biointerfaces 84:462–466PubMedCrossRefGoogle Scholar
  49. La Duc MT, Nicholson W, Kern R, Venkateswaran K (2003) Microbial characterization of the Mars Odyssey spacecraft and its encapsulation facility. Environ Microbiol 5:977–985PubMedCrossRefGoogle Scholar
  50. Langevin S, Vincelette J, Bekal S, Gaudreau C (2011) First case of invasive human infection caused by Cupriavidus metallidurans. J Clin Microbiol 49:744–745PubMedCrossRefGoogle Scholar
  51. Lansdown AB (2010) A pharmacological and toxicological profile of silver as an antimicrobial agent in medical devices. Adv Pharmacol Sci 2010:910686PubMedGoogle Scholar
  52. Li XZ, Nikaido H, Williams KE (1997) Silver-resistant mutants of Escherichia coli display active efflux of Ag+ and are deficient in porins. J Bacteriol 179:6127–6132PubMedGoogle Scholar
  53. Liau SY, Read DC, Pugh WJ, Furr JR, Russell AD (1997) Interaction of silver nitrate with readily identifiable groups: relationship to the antibacterial action of silver ions. Lett Appl Microbiol 25:279–283PubMedCrossRefGoogle Scholar
  54. Lok CN, Ho CM, Chen R, Tam PK, Chiu JF, Che CM (2008) Proteomic identification of the Cus system as a major determinant of constitutive Escherichia coli silver resistance of chromosomal origin. J Proteome Res 7:2351–2356PubMedCrossRefGoogle Scholar
  55. Long F, Su CC, Zimmermann MT, Boyken SE, Rajashankar KR, Jernigan RL, Yu EW (2010) Crystal structures of the CusA efflux pump suggest methionine-mediated metal transport. Nature 467:484–488PubMedCrossRefGoogle Scholar
  56. Matsumura Y, Yoshikata K, Kunisaki S, Tsuchido T (2003) Mode of bactericidal action of silver zeolite and its comparison with that of silver nitrate. Appl Environ Microbiol 69:4278–4281PubMedCrossRefGoogle Scholar
  57. McHugh GL, Moellering RC, Hopkins CC, Swartz MN (1975) Salmonella typhimurium resistant to silver nitrate, chloramphenicol, and ampicillin. Lancet 1:235–240PubMedCrossRefGoogle Scholar
  58. Mijnendonckx K, Provoost A, Ott CM, Venkateswaran K, Mahillon J, Leys N, Van Houdt R (2013) Characterization of the survival ability of Cupriavidus metallidurans and Ralstonia pickettii from space-related environments. Microb Ecol 56:347–360CrossRefGoogle Scholar
  59. Monchy S, Benotmane MA, Janssen P, Vallaeys T, Taghavi S, van der Lelie D, Mergeay M (2007) Plasmids pMOL28 and pMOL30 of Cupriavidus metallidurans are specialized in the maximal viable response to heavy metals. J Bacteriol 189:7417–7425PubMedCrossRefGoogle Scholar
  60. Monsieurs P, Moors H, Van Houdt R, Janssen PJ, Janssen A, Coninx I, Mergeay M, Leys N (2011) Heavy metal resistance in Cupriavidus metallidurans CH34 is governed by an intricate transcriptional network. Biometals 24:1133–1151PubMedCrossRefGoogle Scholar
  61. Morones JR, Elechiguerra JL, Camacho A, Holt K, Kouri JB, Ramirez JT, Yacaman MJ (2005) The bactericidal effect of silver nanoparticles. Nanotechnology 16:2346–2353PubMedCrossRefGoogle Scholar
  62. Munson GP, Lam DL, Outten FW, O’Halloran TV (2000) Identification of a copper-responsive two-component system on the chromosome of Escherichia coli K-12. J Bacteriol 182:5864–5871PubMedCrossRefGoogle Scholar
  63. Nanda A, Saravanan M (2009) Biosynthesis of silver nanoparticles from Staphylococcus aureus and its antimicrobial activity against MRSA and MRSE. Nanomedicine Nanotechnol Biol Med 5:452–456CrossRefGoogle Scholar
  64. Ott CM, Bruce RJ, Pierson DL (2004) Microbial characterization of free floating condensate aboard the Mir space station. Microb Ecol 47:133–136PubMedCrossRefGoogle Scholar
  65. Pal S, Tak YK, Song JM (2007) Does the antibacterial activity of silver nanoparticles depend on the shape of the nanoparticle? A study of the Gram-negative bacterium Escherichia coli. Appl Environ Microbiol 73:1712–1720PubMedCrossRefGoogle Scholar
  66. Panacek A, Kvitek L, Prucek R, Kolar M, Vecerova R, Pizurova N, Sharma VK, Nevecna T, Zboril R (2006) Silver colloid nanoparticles: synthesis, characterization, and their antibacterial activity. J Phys Chem B 110:16248–16253PubMedCrossRefGoogle Scholar
  67. Park HJ, Kim JY, Kim J, Lee JH, Hahn JS, Gu MB, Yoon J (2009) Silver-ion-mediated reactive oxygen species generation affecting bactericidal activity. Water Res 43:1027–1032PubMedCrossRefGoogle Scholar
  68. Perelaer J, Hendriks CE, de Laat AW, Schubert US (2009) One-step inkjet printing of conductive silver tracks on polymer substrates. Nanotechnology 20:165303PubMedCrossRefGoogle Scholar
  69. Perron K, Caille O, Rossier C, Van Delden C, Dumas JL, Kohler T (2004) CzcR-CzcS, a two-component system involved in heavy metal and carbapenem resistance in Pseudomonas aeruginosa. J Biol Chem 279:8761–8768PubMedCrossRefGoogle Scholar
  70. Pokhrel LR, Dubey B (2012) Potential impact of low-concentration silver nanoparticles on predator-prey interactions between predatory dragonfly nymphs and Daphnia magna as a prey. Environ Sci Technol 46:7755–7762PubMedCrossRefGoogle Scholar
  71. Rai MK, Deshmukh SD, Ingle AP, Gade AK (2012) Silver nanoparticles: the powerful nanoweapon against multidrug-resistant bacteria. J Appl Microbiol 112:841–852PubMedCrossRefGoogle Scholar
  72. Rogers JV, Parkinson CV, Choi YW, Speshock JL, Hussain SM (2008) A preliminary assessment of silver nanoparticle inhibition of monkeypox virus plaque formation. Nanoscale Res Lett 3:129–133CrossRefGoogle Scholar
  73. Rosenfeld M, Ramsey BW, Gibson RL (2003) Pseudomonas acquisition in young patients with cystic fibrosis: pathophysiology, diagnosis, and management. Curr Opin Pulm Med 9:492–497PubMedCrossRefGoogle Scholar
  74. Russell AD, Hugo WB (1994) Antimicrobial activity and action of silver. Prog Med Chem 31:351–370PubMedCrossRefGoogle Scholar
  75. Saravanan M, Vemu AK, Bank SK (2011) Rapid biosynthesis of silver nanoparticles from Bacillus megaterium (NCIM 2326) and their antibacterial activity on multi drug resistant clinical pathogens. Colloids Surf B Biointerfaces 88:325–331PubMedCrossRefGoogle Scholar
  76. Schacht VJ, Neumann LV, Sandhi SK, Chen L, Henning T, Klar PJ, Theophel K, Schnell S, Bunge M (2013) Effects of silver nanoparticles on microbial growth dynamics. J Appl Microbiol 114:25–35PubMedCrossRefGoogle Scholar
  77. Schreurs WJ, Rosenberg H (1982) Effect of silver ions on transport and retention of phosphate by Escherichia coli. J Bacteriol 152:7–13PubMedGoogle Scholar
  78. Sedlak RH, Hnilova M, Grosh C, Fong H, Baneyx F, Schwartz D, Sarikaya M, Tamerler C, Traxler B (2012) Engineered Escherichia coli silver-binding periplasmic protein that promotes silver tolerance. Appl Environ Microbiol 78:2289–2296PubMedCrossRefGoogle Scholar
  79. Semeykina AL, Skulachev VP (1990) Submicromolar Ag+ increases passive Na+ permeability and inhibits the respiration-supported formation of Na+ gradient in Bacillus FTU vesicles. FEBS Lett 269:69–72PubMedCrossRefGoogle Scholar
  80. Shahverdi AR, Fakhimi A, Shahverdi HR, Minaian S (2007) Synthesis and effect of silver nanoparticles on the antibacterial activity of different antibiotics against Staphylococcus aureus and Escherichia coli. Nanomedicine Nanotechnol Biol Med 3:168–171CrossRefGoogle Scholar
  81. Silver S (2003) Bacterial silver resistance: molecular biology and uses and misuses of silver compounds. FEMS Microbiol Rev 27:341–353PubMedCrossRefGoogle Scholar
  82. Silver S, Gupta A, Matsui K, Lo JF (1999) Resistance to Ag+ cations in bacteria: environments, genes and proteins. Met Based Drugs 6:315–320PubMedCrossRefGoogle Scholar
  83. Silver S, le Phung T, Silver G (2006) Silver as biocides in burn and wound dressings and bacterial resistance to silver compounds. J Ind Microbiol Biotechnol 33:627–634PubMedCrossRefGoogle Scholar
  84. Sotiriou GA, Pratsinis SE (2010) Antibacterial activity of nanosilver ions and particles. Environ Sci Technol 44:5649–5654PubMedCrossRefGoogle Scholar
  85. Starodub ME, Trevors JT (1989) Silver resistance in Escherichia coli R1. J Med Microbiol 29:101–110PubMedCrossRefGoogle Scholar
  86. Tappin AD, Barriada JL, Braungardt CB, Evans EH, Patey MD, Achterberg EP (2010) Dissolved silver in European estuarine and coastal waters. Water Res 44:4204–4216PubMedCrossRefGoogle Scholar
  87. Thompson R, Elliott V, Mondry A (2009) Argyria: permanent skin discoloration following protracted colloid silver ingestion. BMJ Case Rep 2009:1Google Scholar
  88. Van Houdt R, Mergeay M (2012) Plasmids as secondary chromosomes. In: Bell E, Bond PJS, Klinman PJP, Masters DBSS, Wells PRD (eds) Molecular life sciences: an encyclopedic reference. Springer, BerlinGoogle Scholar
  89. Van Houdt R, Toussaint A, Ryan M, Pembroke J, Mergeay M, Adley CC (2011) The Tn4371 ICE family of bacterial mobile genetic elements. In: Roberts AP, Mullany P (eds) Bacterial integrative mobile genetic elements. Landes Bioscience, AustinGoogle Scholar
  90. Van Houdt R, Monsieurs P, Mijnendonckx K, Provoost A, Janssen A, Mergeay M, Leys N (2012) Variation in genomic islands contribute to genome plasticity in Cupriavidus metallidurans. BMC Genomics 13:111PubMedCrossRefGoogle Scholar
  91. Wolfgang MC, Kulasekara BR, Liang X, Boyd D, Wu K, Yang Q, Miyada CG, Lory S (2003) Conservation of genome content and virulence determinants among clinical and environmental isolates of Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 100:8484–8489PubMedCrossRefGoogle Scholar
  92. World Health Organization (1996) Silver in drinking water: background document for the development of WHO Guidelines for drinking water quality. WHO, Geneva, WHO/SDE/WSH/03.04/14Google Scholar
  93. Wu HP, Liu JF, Wu XJ, Ge MY, Wang YW, Zhang GQ, Jiang JZ (2006) High conductivity of isotropic conductive adhesives filled with silver nanowires. Int J Adhes Adhes 26:617–621CrossRefGoogle Scholar
  94. Xiu ZM, Ma J, Alvarez PJ (2011) Differential effect of common ligands and molecular oxygen on antimicrobial activity of silver nanoparticles versus silver ions. Environ Sci Technol 45:9003–9008PubMedCrossRefGoogle Scholar
  95. Xiu ZM, Zhang QB, Puppala HL, Colvin VL, Alvarez PJ (2012) Negligible particle-specific antibacterial activity of silver nanoparticles. Nano Lett 12:4271–4275PubMedCrossRefGoogle Scholar
  96. Yahya MT, Landeen LK, Messina MC, Kutz SM, Schulze R, Gerba CP (1990) Disinfection of bacteria in water systems by using electrolytically generated copper:silver and reduced levels of free chlorine. Can J Microbiol 36:109–116PubMedCrossRefGoogle Scholar
  97. Yudkins J (1937) The effect of silver ions on some enzymes of Bacterium coli. Enzymologia 2:161–170Google Scholar
  98. Zimmermann M, Udagedara SR, Sze CM, Ryan TM, Howlett GJ, Xiao Z, Wedd AG (2012) PcoE—A metal sponge expressed to the periplasm of copper resistance Escherichia coli. Implication of its function role in copper resistance. J Inorg Biochem 115:186–197PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Kristel Mijnendonckx
    • 1
    • 2
  • Natalie Leys
    • 1
  • Jacques Mahillon
    • 2
  • Simon Silver
    • 3
  • Rob Van Houdt
    • 1
    Email author
  1. 1.Unit of MicrobiologyExpert Group Molecular and Cellular Biology, Belgian Nuclear Research Centre (SCK⋅CEN)MolBelgium
  2. 2.Laboratory of Food and Environmental MicrobiologyUniversité catholique de LouvainLouvain-la-NeuveBelgium
  3. 3.Department of Microbiology and ImmunologyUniversity of IllinoisChicagoUSA

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