User menu

Accès à distance ? S'identifier sur le proxy UCLouvain

Antimicrobial silver: Uses, toxicity and potential for resistance

Primary tabs

Mijnendonckx, Kristel [UCL] Leys, Natalie [UCL] Mahillon, Jacques [UCL] Silver, Simon [University of Illinois, Chicago] Van Houdt, Rob [Belgian Nuclear Research Centre, Mol, Belgium]

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. © 2013 Springer Science+Business Media New York.

Document type Article de périodique (Journal article) – Article de recherche
Access type Accès restreint
Publication date 2013
Language Anglais
Journal information "BioMetals : an international journal on the role of metal ions in biology, biochemistry and medicine" - Vol. 26, no.4, p. 609-621 (2013)
Peer reviewed yes
Publisher Springer Netherlands ((Netherlands) Dordrecht)
issn 0966-0844
e-issn 1572-8773
Publication status Publié
Affiliation UCL - SST/ELI/ELIM - Applied Microbiology
Keywords Resistance ; Silver ; Silver nanoparticles ; Toxicity ; 3131
Links
  1. Alexander J. Wesley, History of the Medical Use of Silver, 10.1089/sur.2008.9941
  2. Alonso Ana, Rojo Fernando, Martinez Jose L., Environmental and clinical isolates of Pseudomonas aeruginosa show pathogenic and biodegradative properties irrespective of their origin, 10.1046/j.1462-2920.1999.00052.x
  3. Aminov Rustam I., Horizontal Gene Exchange in Environmental Microbiota, 10.3389/fmicb.2011.00158
  4. Baker-Austin Craig, Wright Meredith S., Stepanauskas Ramunas, McArthur J.V., Co-selection of antibiotic and metal resistance, 10.1016/j.tim.2006.02.006
  5. Bragg P. D., Rainnie D. J., The effect of silver ions on the respiratory chain ofEscherichia coli, 10.1139/m74-135
  6. Bryan G.W., Langston W.J., Bioavailability, accumulation and effects of heavy metals in sediments with special reference to United Kingdom estuaries: a review, 10.1016/0269-7491(92)90099-v
  7. Cabiscol E, Tamarit J, Ros J (2000) Oxidative stress in bacteria and protein damage by reactive oxygen species. Int Microbiol 3:3–8
  8. Caille O., Rossier C., Perron K., A Copper-Activated Two-Component System Interacts with Zinc and Imipenem Resistance in Pseudomonas aeruginosa, 10.1128/jb.00095-07
  9. Chambers C, Proctor C, Kabler P (1962) Bactericidal effect of low concentrations of silver. Am Water Works Assoc 54:208–216
  10. Chopra I., The increasing use of silver-based products as antimicrobial agents: a useful development or a cause for concern?, 10.1093/jac/dkm006
  11. Choudhury Papiya, Kumar Ranajit, Multidrug- and metal-resistant strains ofKlebsiella pneumoniaeisolated fromPenaeus monodonof the coastal waters of deltaic Sundarban, 10.1139/w97-144
  12. Coenye T., Spilker T., Reik R., Vandamme P., LiPuma J. J., Use of PCR Analyses To Define the Distribution of Ralstonia Species Recovered from Patients with Cystic Fibrosis, 10.1128/jcm.43.7.3463-3466.2005
  13. Cunningham James H., Lin Lian-Shin, Fate of Amoxicillin in Mixed-Culture Bioreactors and Its Effects on Microbial Growth and Resistance to Silver Ions, 10.1021/es9022442
  14. Davis I. J., Richards H., Mullany P., Isolation of silver- and antibiotic-resistant Enterobacter cloacae from teeth, 10.1111/j.1399-302x.2005.00218.x
  15. De Gusseme Bart, Hennebel Tom, Christiaens Eline, Saveyn Hans, Verbeken Kim, Fitts Jeffrey P., Boon Nico, Verstraete Willy, Virus disinfection in water by biogenic silver immobilized in polyvinylidene fluoride membranes, 10.1016/j.watres.2010.11.046
  16. Deshpande LalitagauriMilind, Chopade BaluAnanda, Plasmid mediated silver resistance in Acinetobacter baumannii, 10.1007/bf00205194
  17. Dibrov P., Dzioba J., Gosink K. K., Hase C. C., Chemiosmotic Mechanism of Antimicrobial Activity of Ag+ in Vibrio cholerae, 10.1128/aac.46.8.2668-2670.2002
  18. Dieppois Guennaëlle, Ducret Véréna, Caille Olivier, Perron Karl, The Transcriptional Regulator CzcR Modulates Antibiotic Resistance and Quorum Sensing in Pseudomonas aeruginosa, 10.1371/journal.pone.0038148
  19. Exposure-Related Health Effects of Silver and Silver Compounds: A Review, 10.1093/annhyg/mei019
  20. Edwards-Jones V., The benefits of silver in hygiene, personal care and healthcare, 10.1111/j.1472-765x.2009.02648.x
  21. Badawy Amro M. El, Luxton Todd P., Silva Rendahandi G., Scheckel Kirk G., Suidan Makram T., Tolaymat Thabet M., Impact of Environmental Conditions (pH, Ionic Strength, and Electrolyte Type) on the Surface Charge and Aggregation of Silver Nanoparticles Suspensions, 10.1021/es902240k
  22. El Badawy Amro M., Silva Rendahandi G., Morris Brian, Scheckel Kirk G., Suidan Makram T., Tolaymat Thabet M., Surface Charge-Dependent Toxicity of Silver Nanoparticles, 10.1021/es1034188
  23. Elechiguerra Jose, Burt Justin L, Morones Jose R, Camacho-Bragado Alejandra, Gao Xiaoxia, Lara Humberto H, Yacaman Miguel, 10.1186/1477-3155-3-6
  24. Fabrega Julia, Luoma Samuel N., Tyler Charles R., Galloway Tamara S., Lead Jamie R., Silver nanoparticles: Behaviour and effects in the aquatic environment, 10.1016/j.envint.2010.10.012
  25. Flegal A.R., Brown C.L., Squire S., Ross J.R.M., Scelfo G.M., Hibdon S., Spatial and temporal variations in silver contamination and toxicity in San Francisco Bay, 10.1016/j.envres.2007.05.006
  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, Berlin
  27. Franke Sylvia, Grass Gregor, Nies Dietrich H., The product of the ybdE gene of the Escherichia coli chromosome is involved in detoxification of silver ions, 10.1099/00221287-147-4-965
  28. Franke S., Grass G., Rensing C., Nies D. H., Molecular Analysis of the Copper-Transporting Efflux System CusCFBA of Escherichia coli, 10.1128/jb.185.13.3804-3812.2003
  29. Gordon O., Vig Slenters T., Brunetto P. S., Villaruz A. E., Sturdevant D. E., Otto M., Landmann R., Fromm K. M., Silver Coordination Polymers for Prevention of Implant Infection: Thiol Interaction, Impact on Respiratory Chain Enzymes, and Hydroxyl Radical Induction, 10.1128/aac.01830-09
  30. Goris J., De Vos P., Coenye T., Hoste B., Janssens D., Brim H., Diels L., Mergeay M., Kersters K., Vandamme P., 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, 10.1099/00207713-51-5-1773
  31. Gudipaty Swapna Aravind, Larsen Andrew S., Rensing Christopher, McEvoy Megan M., Regulation of Cu(I)/Ag(I) efflux genes in Escherichia coli by the sensor kinase CusS, 10.1111/j.1574-6968.2012.02529.x
  32. Gupta A, Maynes M, Silver S (1998) Effects of halides on plasmid-mediated silver resistance in Escherichia coli. Appl Environ Microbiol 64:5042–5045
  33. Gupta Amit, Matsui Kazuaki, Lo Jeng-Fan, Silver Simon, 10.1038/5545
  34. Gupta Amit, Phung Le T., Silver Simon, Taylor Diane E., Diversity of silver resistance genes in IncH incompatibility group plasmids, 10.1099/00221287-147-12-3393
  35. Haefeli C, Franklin C, Hardy K (1984) Plasmid-determined silver resistance in Pseudomonas stutzeri isolated from a silver mine. J Bacteriol 158:389–392
  36. Hayashi Maki, Miyoshi Tohoru, Sato Masako, Unemoto Tsutomu, Properties of respiratory chain-linked Na+-independent NADH-quinone reductase in a marine Vibrio alginolyticus, 10.1016/0005-2728(92)90211-j
  37. Heuer Holger, Kopmann Christoph, Binh Chu T. T., Top Eva M., Smalla Kornelia, Spreading antibiotic resistance through spread manure: characteristics of a novel plasmid type with low %G+C content, 10.1111/j.1462-2920.2008.01819.x
  38. Holland Sara L., Dyer Paul S., Bond Chris J., James Steve A., Roberts Ian N., Avery Simon V., Candida argentea sp. nov., a copper and silver resistant yeast species, 10.1016/j.funbio.2011.07.004
  39. Jain Prashant K., Huang Xiaohua, El-Sayed Ivan H., El-Sayed Mostafa A., Noble Metals on the Nanoscale: Optical and Photothermal Properties and Some Applications in Imaging, Sensing, Biology, and Medicine, 10.1021/ar7002804
  40. Janssen Paul J., Van Houdt Rob, Moors Hugo, Monsieurs Pieter, Morin Nicolas, Michaux Arlette, Benotmane Mohammed A., Leys Natalie, Vallaeys Tatiana, Lapidus Alla, Monchy Sébastien, Médigue Claudine, Taghavi Safiyh, McCorkle Sean, Dunn John, van der Lelie Daniël, Mergeay Max, The Complete Genome Sequence of Cupriavidus metallidurans Strain CH34, a Master Survivalist in Harsh and Anthropogenic Environments, 10.1371/journal.pone.0010433
  41. JELENKO CARL, Silver Nitrate Resistant E. Coli : Report of Case, 10.1097/00000658-196908000-00021
  42. Jung Woo Kyung, Kim So Hyun, Koo Hye Cheong, Shin Sook, Kim Jun Man, Park Young Kyung, Hwang Sun Young, Yang Hyesoon, Park Yong Ho, Antifungal activity of the silver ion against contaminated fabric, 10.1111/j.1439-0507.2007.01372.x
  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
  44. Kim Jee Yeon, Lee Changha, Cho Min, Yoon Jeyong, Enhanced inactivation of E. coli and MS-2 phage by silver ions combined with UV-A and visible light irradiation, 10.1016/j.watres.2007.07.024
  45. Klasen H.J., Historical review of the use of silver in the treatment of burns. I. Early uses, 10.1016/s0305-4179(99)00108-4
  46. Klaus T., Joerger R., Olsson E., Granqvist C.-G., Silver-based crystalline nanoparticles, microbially fabricated, 10.1073/pnas.96.24.13611
  47. Kremer A. N., Hoffmann H., Subtractive Hybridization Yields a Silver Resistance Determinant Unique to Nosocomial Pathogens in the Enterobacter cloacae Complex, 10.1128/jcm.00885-12
  48. Kumar C. Ganesh, Mamidyala Suman Kumar, Extracellular synthesis of silver nanoparticles using culture supernatant of Pseudomonas aeruginosa, 10.1016/j.colsurfb.2011.01.042
  49. La Duc Myron T., Nicholson Wayne, Kern Roger, Venkateswaran Kasthuri, Microbial characterization of the Mars Odyssey spacecraft and its encapsulation facility, 10.1046/j.1462-2920.2003.00496.x
  50. Langevin S., Vincelette J., Bekal S., Gaudreau C., First Case of Invasive Human Infection Caused by Cupriavidus metallidurans, 10.1128/jcm.01947-10
  51. Lansdown AB (2010) A pharmacological and toxicological profile of silver as an antimicrobial agent in medical devices. Adv Pharmacol Sci 2010:910686
  52. Li X Z, Nikaido H, Williams K E, Silver-resistant mutants of Escherichia coli display active efflux of Ag+ and are deficient in porins., 10.1128/jb.179.19.6127-6132.1997
  53. Liau S.Y., Read D.C., Pugh W.J., Furr J.R., Russell A.D., Interaction of silver nitrate with readily identifiable groups: relationship to the antibacterialaction of silver ions, 10.1046/j.1472-765x.1997.00219.x
  54. Lok Chun-Nam, Ho Chi-Ming, Chen Rong, Tam Paul Kwong-Hang, Chiu Jen-Fu, Che Chi-Ming, Proteomic Identification of the Cus System as a Major Determinant of ConstitutiveEscherichia coliSilver Resistance of Chromosomal Origin, 10.1021/pr700646b
  55. Long Feng, Su Chih-Chia, Zimmermann Michael T., Boyken Scott E., Rajashankar Kanagalaghatta R., Jernigan Robert L., Yu Edward W., Crystal structures of the CusA efflux pump suggest methionine-mediated metal transport, 10.1038/nature09395
  56. Matsumura Y., Yoshikata K., Kunisaki S.-i., Tsuchido T., Mode of Bactericidal Action of Silver Zeolite and Its Comparison with That of Silver Nitrate, 10.1128/aem.69.7.4278-4281.2003
  57. Larkin Mchugh Gail, Moellering RobertC., Hopkins CyrusC., Swartz MortonN., SALMONELLA TYPHIMURIUM RESISTANT TO SILVER NITRATE, CHLORAMPHENICOL, AND AMPICILLIN, 10.1016/s0140-6736(75)91138-1
  58. Mijnendonckx K., Provoost A., Ott C. M., Venkateswaran K., Mahillon J., Leys N., Van Houdt R., Characterization of the Survival Ability of Cupriavidus metallidurans and Ralstonia pickettii from Space-Related Environments, 10.1007/s00248-012-0139-2
  59. Monchy S., Benotmane M. A., Janssen P., Vallaeys T., Taghavi S., van der Lelie D., Mergeay M., Plasmids pMOL28 and pMOL30 of Cupriavidus metallidurans Are Specialized in the Maximal Viable Response to Heavy Metals, 10.1128/jb.00375-07
  60. Monsieurs Pieter, Moors Hugo, Van Houdt Rob, Janssen Paul J., Janssen Ann, Coninx Ilse, Mergeay Max, Leys Natalie, Heavy metal resistance in Cupriavidus metallidurans CH34 is governed by an intricate transcriptional network, 10.1007/s10534-011-9473-y
  61. Morones Jose Ruben, Elechiguerra Jose Luis, Camacho Alejandra, Holt Katherine, Kouri Juan B, Ramírez Jose Tapia, Yacaman Miguel Jose, The bactericidal effect of silver nanoparticles, 10.1088/0957-4484/16/10/059
  62. Munson G. P., Lam D. L., Outten F. W., O'Halloran T. V., Identification of a Copper-Responsive Two-Component System on the Chromosome of Escherichia coli K-12, 10.1128/jb.182.20.5864-5871.2000
  63. Nanda Anima, Saravanan M., Biosynthesis of silver nanoparticles from Staphylococcus aureus and its antimicrobial activity against MRSA and MRSE, 10.1016/j.nano.2009.01.012
  64. Ott C. M., Bruce R. J., Pierson D. L., Microbial Characterization of Free Floating Condensate aboard the Mir Space Station, 10.1007/s00248-003-1038-3
  65. Pal S., Tak Y. K., Song J. M., Does the Antibacterial Activity of Silver Nanoparticles Depend on the Shape of the Nanoparticle? A Study of the Gram-Negative Bacterium Escherichia coli, 10.1128/aem.02218-06
  66. Panáček Aleš, Kvítek Libor, Prucek Robert, Kolář Milan, Večeřová Renata, Pizúrová Naděžda, Sharma Virender K., Nevěčná Tat‘jana, Zbořil Radek, Silver Colloid Nanoparticles:  Synthesis, Characterization, and Their Antibacterial Activity, 10.1021/jp063826h
  67. Park Hee-Jin, Kim Jee Yeon, Kim Jaeeun, Lee Joon-Hee, Hahn Ji-Sook, Gu Man Bock, Yoon Jeyong, Silver-ion-mediated reactive oxygen species generation affecting bactericidal activity, 10.1016/j.watres.2008.12.002
  68. Perelaer Jolke, Hendriks Chris E, de Laat Antonius W M, Schubert Ulrich S, One-step inkjet printing of conductive silver tracks on polymer substrates, 10.1088/0957-4484/20/16/165303
  69. Perron Karl, Caille Olivier, Rossier Claude, van Delden Christian, Dumas Jean-Luc, Köhler Thilo, CzcR-CzcS, a Two-component System Involved in Heavy Metal and Carbapenem Resistance inPseudomonas aeruginosa, 10.1074/jbc.m312080200
  70. Pokhrel Lok R., Dubey Brajesh, Potential Impact of Low-Concentration Silver Nanoparticles on Predator–Prey Interactions between Predatory Dragonfly Nymphs and Daphnia magna as a Prey, 10.1021/es204055c
  71. Rai M.K., Deshmukh S.D., Ingle A.P., Gade A.K., Silver nanoparticles: the powerful nanoweapon against multidrug-resistant bacteria : Activity of silver nanoparticles against MDR bacteria, 10.1111/j.1365-2672.2012.05253.x
  72. Rogers James V., Parkinson Christopher V., Choi Young W., Speshock Janice L., Hussain Saber M., A Preliminary Assessment of Silver Nanoparticle Inhibition of Monkeypox Virus Plaque Formation, 10.1007/s11671-008-9128-2
  73. Rosenfeld Margaret, Ramsey Bonnie W., Gibson Ronald L., Pseudomonas acquisition in young patients with cystic fibrosis: pathophysiology, diagnosis, and management : , 10.1097/00063198-200311000-00008
  74. Russell A.D., Hugo W.B., 7 Antimicrobial Activity and Action of Silver, Progress in Medicinal Chemistry (1994) ISBN:9780444818072 p.351-370, 10.1016/s0079-6468(08)70024-9
  75. Saravanan M., Vemu Anil Kumar, Barik Sisir Kumar, Rapid biosynthesis of silver nanoparticles from Bacillus megaterium (NCIM 2326) and their antibacterial activity on multi drug resistant clinical pathogens, 10.1016/j.colsurfb.2011.07.009
  76. Schacht V.J., Neumann L.V., Sandhi S.K., Chen L., Henning T., Klar P.J., Theophel K., Schnell S., Bunge M., Effects of silver nanoparticles on microbial growth dynamics, 10.1111/jam.12000
  77. Schreurs WJ, Rosenberg H (1982) Effect of silver ions on transport and retention of phosphate by Escherichia coli. J Bacteriol 152:7–13
  78. Hall Sedlak R., Hnilova M., Grosh C., Fong H., Baneyx F., Schwartz D., Sarikaya M., Tamerler C., Traxler B., Engineered Escherichia coli Silver-Binding Periplasmic Protein That Promotes Silver Tolerance, 10.1128/aem.06823-11
  79. Semeykina Anna L., Skulachev Vladimr P., Submicromolar Ag+increases passive Na+permeability and inhibits the respiration-supported formation of Na+gradient inBacillus FTUvesicles, 10.1016/0014-5793(90)81120-d
  80. Shahverdi Ahmad R., Fakhimi Ali, Shahverdi Hamid R., Minaian Sara, Synthesis and effect of silver nanoparticles on the antibacterial activity of different antibiotics against Staphylococcus aureus and Escherichia coli, 10.1016/j.nano.2007.02.001
  81. Silver Simon, Bacterial silver resistance: molecular biology and uses and misuses of silver compounds, 10.1016/s0168-6445(03)00047-0
  82. Silver Simon, Gupta Amit, Matsui Kazuaki, Lo Jeng-Fan, Resistance to Ag(I) Cations in Bacteria: Environments, Genes and Proteins, 10.1155/mbd.1999.315
  83. Silver Simon, Phung Le T., Silver Gregg, Silver as biocides in burn and wound dressings and bacterial resistance to silver compounds, 10.1007/s10295-006-0139-7
  84. Sotiriou Georgios A., Pratsinis Sotiris E., Antibacterial Activity of Nanosilver Ions and Particles, 10.1021/es101072s
  85. Starodub M. E., Trevors J. T., Silver resistance in Escherichia coli R1, 10.1099/00222615-29-2-101
  86. Tappin Alan D., Barriada Jose L., Braungardt Charlotte B., Evans E. Hywel, Patey Matthew D., Achterberg Eric P., Dissolved silver in European estuarine and coastal waters, 10.1016/j.watres.2010.05.022
  87. Thompson R, Elliott V, Mondry A (2009) Argyria: permanent skin discoloration following protracted colloid silver ingestion. BMJ Case Rep 2009:1
  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, Berlin
  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, Austin
  90. Van Houdt Rob, Monsieurs Pieter, Mijnendonckx Kristel, Provoost Ann, Janssen Ann, Mergeay Max, Leys Natalie, Variation in genomic islands contribute to genome plasticity in Cupriavidus metallidurans, 10.1186/1471-2164-13-111
  91. Wolfgang M. C., Kulasekara B. R., Liang X., Boyd D., Wu K., Yang Q., Miyada C. G., Lory S., Conservation of genome content and virulence determinants among clinical and environmental isolates of Pseudomonas aeruginosa, 10.1073/pnas.0832438100
  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/03.04/14
  93. Wu H.P., Liu J.F., Wu X.J., Ge M.Y., Wang Y.W., Zhang G.Q., Jiang J.Z., High conductivity of isotropic conductive adhesives filled with silver nanowires, 10.1016/j.ijadhadh.2005.10.001
  94. Xiu Zong-Ming, Ma Jie, Alvarez Pedro J. J., Differential Effect of Common Ligands and Molecular Oxygen on Antimicrobial Activity of Silver Nanoparticles versus Silver Ions, 10.1021/es201918f
  95. Xiu Zong-ming, Zhang Qing-bo, Puppala Hema L., Colvin Vicki L., Alvarez Pedro J. J., Negligible Particle-Specific Antibacterial Activity of Silver Nanoparticles, 10.1021/nl301934w
  96. Yahya Moyasar T., Landeen Lee K., Messina Maria C., Kutz Susan M., Schulze Richard, Gerba Charles P., Disinfection of bacteria in water systems by using electrolytically generated copper:silver and reduced levels of free chlorine, 10.1139/m90-020
  97. Yudkins J (1937) The effect of silver ions on some enzymes of Bacterium coli. Enzymologia 2:161–170
  98. Zimmermann Matthias, Udagedara Saumya R., Sze Chak Ming, Ryan Timothy M., Howlett Geoffrey J., Xiao Zhiguang, Wedd Anthony G., PcoE — A metal sponge expressed to the periplasm of copper resistance Escherichia coli. Implication of its function role in copper resistance, 10.1016/j.jinorgbio.2012.04.009
Bibliographic reference Mijnendonckx, Kristel ; Leys, Natalie ; Mahillon, Jacques ; Silver, Simon ; Van Houdt, Rob. Antimicrobial silver: Uses, toxicity and potential for resistance. In: BioMetals : an international journal on the role of metal ions in biology, biochemistry and medicine, Vol. 26, no.4, p. 609-621 (2013)
Permanent URL http://hdl.handle.net/2078.1/140703