1887

Abstract

Metals such as mercury, arsenic, copper and silver have been used in various forms as antimicrobials for thousands of years with until recently, little understanding of their mode of action. The discovery of antibiotics and new organic antimicrobial compounds during the twentieth century saw a general decline in the clinical use of antimicrobial metal compounds, with the exception of the rediscovery of the use of silver for burns treatments and niche uses for other metal compounds. Antibiotics and new antimicrobials were regarded as being safer for the patient and more effective than the metal-based compounds they supplanted. Bacterial metal ion resistances were first discovered in the second half of the twentieth century. The detailed mechanisms of resistance have now been characterized in a wide range of bacteria. As the use of antimicrobial metals is limited, it is legitimate to ask: are antimicrobial metal resistances in pathogenic and commensal bacteria important now? This review details the new, rediscovered and ‘never went away’ uses of antimicrobial metals; examines the prevalence and linkage of antimicrobial metal resistance genes to other antimicrobial resistance genes; and examines the evidence for horizontal transfer of these genes between bacteria. Finally, we discuss the possible implications of the widespread dissemination of these resistances on re-emergent uses of antimicrobial metals and how this could impact upon the antibiotic resistance problem.

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2015-05-01
2019-10-15
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References

  1. Aarestrup F. M. , Hasman H. . ( 2004; ). Susceptibility of different bacterial species isolated from food animals to copper sulphate, zinc chloride and antimicrobial substances used for disinfection. . Vet Microbiol 100:, 83–89. [CrossRef] [PubMed]
    [Google Scholar]
  2. Abrams M. J. , Murrer B. A. . ( 1993; ). Metal compounds in therapy and diagnosis. . Science 261:, 725–730. [CrossRef] [PubMed]
    [Google Scholar]
  3. Adams M. D. , Goglin K. , Molyneaux N. , Hujer K. M. , Lavender H. , Jamison J. J. , MacDonald I. J. , Martin K. M. , Russo T. et al. ( 2008; ). Comparative genome sequence analysis of multidrug-resistant Acinetobacter baumannii . . J Bacteriol 190:, 8053–8064. [CrossRef] [PubMed]
    [Google Scholar]
  4. Alekshun M. N. , Levy S. B. . ( 2006; ). Commensals upon us. . Biochem Pharmacol 71:, 893–900. [CrossRef] [PubMed]
    [Google Scholar]
  5. Alekshun M. N. , Levy S. B. . ( 2007; ). Molecular mechanisms of antibacterial multidrug resistance. . Cell 128:, 1037–1050. [CrossRef] [PubMed]
    [Google Scholar]
  6. Allen H. K. , Donato J. , Wang H. H. , Cloud-Hansen K. A. , Davies J. , Handelsman J. . ( 2010; ). Call of the wild: antibiotic resistance genes in natural environments. . Nat Rev Microbiol 8:, 251–259. [CrossRef] [PubMed]
    [Google Scholar]
  7. Aminov R. I. , Mackie R. I. . ( 2007; ). Evolution and ecology of antibiotic resistance genes. . FEMS Microbiol Lett 271:, 147–161. [CrossRef] [PubMed]
    [Google Scholar]
  8. Ashutosh , Sundar S. , Goyal N. . ( 2007; ). Molecular mechanisms of antimony resistance in Leishmania . . J Med Microbiol 56:, 143–153. [CrossRef] [PubMed]
    [Google Scholar]
  9. Aziz R. K. . ( 2009; ). The case for biocentric microbiology. . Gut Pathog 1:, 16. [CrossRef] [PubMed]
    [Google Scholar]
  10. Baker J. , Sitthisak S. , Sengupta M. , Johnson M. , Jayaswal R. K. , Morrissey J. A. . ( 2010; ). Copper stress induces a global stress response in Staphylococcus aureus and represses sae and agr expression and biofilm formation. . Appl Environ Microbiol 76:, 150–160. [CrossRef] [PubMed]
    [Google Scholar]
  11. Baker J. , Sengupta M. , Jayaswal R. K. , Morrissey J. A. . ( 2011; ). The Staphylococcus aureus CsoR regulates both chromosomal and plasmid-encoded copper resistance mechanisms. . Environ Microbiol 13:, 2495–2507. [CrossRef] [PubMed]
    [Google Scholar]
  12. Baker-Austin C. , Wright M. S. , Stepanauskas R. , McArthur J. V. . ( 2006; ). Co-selection of antibiotic and metal resistance. . Trends Microbiol 14:, 176–182. [CrossRef] [PubMed]
    [Google Scholar]
  13. Barber R.S. , Brande R. , Mitchell K.G. , Cassidy J. . ( 1955; ). High copper mineral mixture for fattening pigs. . Chem Ind 74: , 601.1.
    [Google Scholar]
  14. Barkay T. , Wagner-Döbler I. . ( 2005; ). Microbial transformations of mercury: potentials, challenges, and achievements in controlling mercury toxicity in the environment. . Adv Appl Microbiol 57:, 1–52. [CrossRef] [PubMed]
    [Google Scholar]
  15. Barkay T. , Miller S. M. , Summers A. O. . ( 2003; ). Bacterial mercury resistance from atoms to ecosystems. . FEMS Microbiol Rev 27:, 355–384. [CrossRef] [PubMed]
    [Google Scholar]
  16. Barkay T. , Kritee K. , Boyd E. , Geesey G. . ( 2010; ). A thermophilic bacterial origin and subsequent constraints by redox, light and salinity on the evolution of the microbial mercuric reductase. . Environ Microbiol 12:, 2904–2917. [CrossRef] [PubMed]
    [Google Scholar]
  17. Barnes J. M. , Stoner H. B. . ( 1959; ). The toxicology of tin compounds. . Pharmacol Rev 11:, 211–231.[PubMed]
    [Google Scholar]
  18. Bass L. , Liebert C. A. , Lee M. D. , Summers A. O. , White D. G. , Thayer S. G. , Maurer J. J. . ( 1999; ). Incidence and characterization of integrons, genetic elements mediating multiple-drug resistance, in avian Escherichia coli . . Antimicrob Agents Chemother 43:, 2925–2929.[PubMed]
    [Google Scholar]
  19. Bender C. L. , Cooksey D. A. . ( 1987; ). Molecular cloning of copper resistance genes from Pseudomonas syringae pv. tomato . . J Bacteriol 169:, 470–474.[PubMed]
    [Google Scholar]
  20. Berg J. , Tom-Petersen A. , Nybroe O. . ( 2005; ). Copper amendment of agricultural soil selects for bacterial antibiotic resistance in the field. . Lett Appl Microbiol 40:, 146–151. [CrossRef] [PubMed]
    [Google Scholar]
  21. Black J. . ( 1999; ). The puzzle of pink disease. . J R Soc Med 92:, 478–481.[PubMed]
    [Google Scholar]
  22. Borkow G. , Gabbay J. . ( 2009; ). Copper, an ancient remedy returning to fight microbial, fungal and viral infections. . Curr Chem Biol 3:, 272–278.
    [Google Scholar]
  23. Borkow G. , Gabbay J. , Dardik R. , Eidelman A. I. , Lavie Y. , Grunfeld Y. , Ikher S. , Huszar M. , Zatcoff R. C. , Marikovsky M. . ( 2010; ). Molecular mechanisms of enhanced wound healing by copper oxide-impregnated dressings. . Wound Repair Regen 18:, 266–275. [CrossRef] [PubMed]
    [Google Scholar]
  24. Bosch F. , Rosich L. . ( 2008; ). The contributions of Paul Ehrlich to pharmacology: a tribute on the occasion of the centenary of his Nobel Prize. . Pharmacology 82:, 171–179. [CrossRef] [PubMed]
    [Google Scholar]
  25. Briers Y. , Klumpp J. , Schuppler M. , Loessner M. J. . ( 2011; ). Genome sequence of Listeria monocytogenes Scott A, a clinical isolate from a food-borne listeriosis outbreak. . J Bacteriol 193:, 4284–4285. [CrossRef] [PubMed]
    [Google Scholar]
  26. Brown N. L. , Barrett S. R. , Camakaris J. , Lee B. T. , Rouch D. A. . ( 1995; ). Molecular genetics and transport analysis of the copper-resistance determinant (pco) from Escherichia coli plasmid pRJ1004. . Mol Microbiol 17:, 1153–1166. [CrossRef] [PubMed]
    [Google Scholar]
  27. Brown N. L. , Stoyanov J. V. , Kidd S. P. , Hobman J. L. . ( 2003; ). The MerR family of transcriptional regulators. . FEMS Microbiol Rev 27:, 145–163. [CrossRef] [PubMed]
    [Google Scholar]
  28. Brzuszkiewicz E. , Thürmer A. , Schuldes J. , Leimbach A. , Liesegang H. , Meyer F.-D. , Boelter J. , Petersen H. , Gottschalk G. , Daniel R. . ( 2011; ). Genome sequence analyses of two isolates from the recent Escherichia coli outbreak in Germany reveal the emergence of a new pathotype: Entero-Aggregative-Haemorrhagic Escherichia coli (EAHEC). . Arch Microbiol 193:, 883–891. [CrossRef] [PubMed]
    [Google Scholar]
  29. Casey A. L. , Adams D. , Karpanen T. J. , Lambert P. A. , Cookson B. D. , Nightingale P. , Miruszenko L. , Shillam R. , Christian P. , Elliott T. S. J. . ( 2010; ). Role of copper in reducing hospital environment contamination. . J Hosp Infect 74:, 72–77. [CrossRef] [PubMed]
    [Google Scholar]
  30. Chaloupka K. , Malam Y. , Seifalian A. M. . ( 2010; ). Nanosilver as a new generation of nanoproduct in biomedical applications. . Trends Biotechnol 28:, 580–588. [CrossRef] [PubMed]
    [Google Scholar]
  31. Chaturvedi K. S. , Henderson J. P. . ( 2014; ). Pathogenic adaptations to host-derived antibacterial copper. . Front Cell Infect Microbiol 4:, 3. [CrossRef] [PubMed]
    [Google Scholar]
  32. Chaudhuri R. R. , Sebaihia M. , Hobman J. L. , Webber M. A. , Leyton D. L. , Goldberg M. , Cunningham A. F. , Scott-Tucker A. , Ferguson P. R. et al. ( 2010; ). Complete genome sequence and comparative metabolic profiling of the prototypical enteroaggregative Escherichia coli strain 042. . PLoS One 5:, e8801. [CrossRef] [PubMed]
    [Google Scholar]
  33. Chen Y.-T. , Chang H.-Y. , Lai Y.-C. , Pan C.-C. , Tsai S.-F. , Peng H.-L. . ( 2004; ). Sequencing and analysis of the large virulence plasmid pLVPK of Klebsiella pneumoniae CG43. . Gene 337:, 189–198. [CrossRef] [PubMed]
    [Google Scholar]
  34. Chitambar C. R. . ( 2010; ). Medical applications and toxicities of gallium compounds. . Int J Environ Res Public Health 7:, 2337–2361. [CrossRef] [PubMed]
    [Google Scholar]
  35. 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:, 587–590. [CrossRef] [PubMed]
    [Google Scholar]
  36. Chu L. , Mukhopadhyay D. , Yu H. , Kim K. S. , Misra T. K. . ( 1992; ). Regulation of the Staphylococcus aureus plasmid pI258 mercury resistance operon. . J Bacteriol 174:, 7044–7047.[PubMed]
    [Google Scholar]
  37. Clarkson T. W. , Magos L. . ( 2006; ). The toxicology of mercury and its chemical compounds. . Crit Rev Toxicol 36:, 609–662. [CrossRef] [PubMed]
    [Google Scholar]
  38. Clement J. L. , Jarrett P. S. . ( 1994; ). Antibacterial silver. . Met Based Drugs 1:, 467–482. [CrossRef] [PubMed]
    [Google Scholar]
  39. Cooksey C. . ( 2012; ). Health concerns of heavy metals and metalloids. . Sci Prog 95:, 73–88. [CrossRef] [PubMed]
    [Google Scholar]
  40. Cooksey D. A. , Azad H. R. , Cha J.-S. , Lim C.-K. . ( 1990; ). Copper resistance gene homologs in pathogenic and saprophytic bacterial species from tomato. . Appl Environ Microbiol 56:, 431–435.[PubMed]
    [Google Scholar]
  41. Cooney J. J. , Wuertz S. . ( 1989; ). Toxic effects of tin compounds on microorganisms. . J Ind Microbiol 4:, 375–402. [CrossRef]
    [Google Scholar]
  42. Courvalin P. . ( 2005; ). Antimicrobial drug resistance: “prediction is very difficult, especially about the future”. . Emerg Infect Dis 11:, 1503–1506. [CrossRef]
    [Google Scholar]
  43. Courvalin P. . ( 2008; ). Predictable and unpredictable evolution of antibiotic resistance. . J Intern Med 264:, 4–16. [CrossRef] [PubMed]
    [Google Scholar]
  44. Crossman L. C. . ( 2011; ). Large scale expansion of mobile elements in specific hotspot regions of the German outbreak Escherichia coli O104 : H4. Available from Nature Precedings http://hdl.handle.net/10101/npre.2011.6466.1.
  45. Crossman L. C. , Gould V. C. , Dow J. M. , Vernikos G. S. , Okazaki A. , Sebaihia M. , Saunders D. , Arrowsmith C. , Carver T. et al. ( 2008; ). The complete genome, comparative and functional analysis of Stenotrophomonas maltophilia reveals an organism heavily shielded by drug resistance determinants. . Genome Biol 9:, R74. [CrossRef] [PubMed]
    [Google Scholar]
  46. Crossman L. C. , Chaudhuri R. R. , Beatson S. A. , Wells T. J. , Desvaux M. , Cunningham A. F. , Petty N. K. , Mahon V. , Brinkley C. et al. ( 2010; ). A commensal gone bad: complete genome sequence of the prototypical enterotoxigenic Escherichia coli strain H10407. . J Bacteriol 192:, 5822–5831. [CrossRef] [PubMed]
    [Google Scholar]
  47. Datta N. , Hughes V. M. . ( 1983; ). Plasmids of the same Inc groups in Enterobacteria before and after the medical use of antibiotics. . Nature 306:, 616–617. [CrossRef] [PubMed]
    [Google Scholar]
  48. Davies J. . ( 1995; ). Vicious circles: looking back on resistance plasmids. . Genetics 139:, 1465–1468.[PubMed]
    [Google Scholar]
  49. Davies J. , Davies D. . ( 2010; ). Origins and evolution of antibiotic resistance. . Microbiol Mol Biol Rev 74:, 417–433. [CrossRef] [PubMed]
    [Google Scholar]
  50. Davis I. J. , Richards H. , Mullany P. . ( 2005; ). Isolation of silver- and antibiotic-resistant Enterobacter cloacae from teeth. . Oral Microbiol Immunol 20:, 191–194. [CrossRef] [PubMed]
    [Google Scholar]
  51. Department of Health (2013) Chief Medical Officer Annual Report 2011: volume 2. https://www.gov.uk/government/publications/chief-medical-officer-annual-report-volume-2
  52. Desoize B. . ( 2004; ). Metals and metal compounds in cancer treatment. . Anticancer Res 24: (Suppl 3a), 1529–1544.[PubMed]
    [Google Scholar]
  53. Dey S. , Rosen B. P. . ( 1995; ). Dual mode of energy coupling by the oxyanion-translocating ArsB protein. . J Bacteriol 177:, 385–389.[PubMed]
    [Google Scholar]
  54. Di Pilato V. , Arena F. , Giani T. , Conte V. , Cresti S. , Rossolini G. M. . ( 2014; ). Characterization of pFOX-7a, a conjugative IncL/M plasmid encoding the FOX-7 AmpC-type β-lactamase, involved in a large outbreak in a neonatal intensive care unit. . J Antimicrob Chemother 69:, 2620–2624. [CrossRef] [PubMed]
    [Google Scholar]
  55. Dibrov P. , Dzioba J. , Gosink K. K. , Häse C. C. . ( 2002; ). Chemiosmotic mechanism of antimicrobial activity of Ag+ in Vibrio cholerae . . Antimicrob Agents Chemother 46:, 2668–2670. [CrossRef] [PubMed]
    [Google Scholar]
  56. Djoko K. Y. , Xiao Z. , Wedd A. G. . ( 2008; ). Copper resistance in E. coli: the multicopper oxidase PcoA catalyzes oxidation of copper(I) in CuICuII-PcoC. . ChemBioChem 9:, 1579–1582. [CrossRef] [PubMed]
    [Google Scholar]
  57. Domingues S. , Harms K. , Fricke W. F. , Johnsen P. J. , da Silva G. J. , Nielsen K. M. . ( 2012; ). Natural transformation facilitates transfer of transposons, integrons and gene cassettes between bacterial species. . PLoS Pathog 8:, e1002837. [CrossRef] [PubMed]
    [Google Scholar]
  58. Du H. , Lo T.-M. , Sitompul J. , Chang M. W. . ( 2012; ). Systems-level analysis of Escherichia coli response to silver nanoparticles: the roles of anaerobic respiration in microbial resistance. . Biochem Biophys Res Commun 424:, 657–662. [CrossRef] [PubMed]
    [Google Scholar]
  59. Duffus J. H. . ( 2002; ). “Heavy metals” a meaningless term?. Pure Appl Chem 74:, 793–807. [CrossRef]
    [Google Scholar]
  60. Dupont C. L. , Grass G. , Rensing C. . ( 2011; ). Copper toxicity and the origin of bacterial resistance new insights and applications. . Metallomics 3:, 1109–1118. [CrossRef] [PubMed]
    [Google Scholar]
  61. Edwards-Jones V. . ( 2009; ). The benefits of silver in hygiene, personal care and healthcare. . Lett Appl Microbiol 49:, 147–152. [CrossRef] [PubMed]
    [Google Scholar]
  62. Elek S. D. , Higney L. . ( 1970; ). Resistogram typing a new epidemiological tool: application to Escherichia coli . . J Med Microbiol 3:, 103–110. [CrossRef] [PubMed]
    [Google Scholar]
  63. Elguindi J. , Moffitt S. , Hasman H. , Andrade C. , Raghavan S. , Rensing C. . ( 2011; ). Metallic copper corrosion rates, moisture content, and growth medium influence survival of copper ion-resistant bacteria. . Appl Microbiol Biotechnol 89:, 1963–1970. [CrossRef] [PubMed]
    [Google Scholar]
  64. Eppinger M. , Radnedge L. , Andersen G. , Vietri N. , Severson G. , Mou S. , Ravel J. , Worsham P. L. . ( 2012; ). Novel plasmids and resistance phenotypes in Yersinia pestis: unique plasmid inventory of strain Java 9 mediates high levels of arsenic resistance. . PLoS One 7:, e32911. [CrossRef] [PubMed]
    [Google Scholar]
  65. Espírito-Santo C. , Taudte N. , Nies D. H. , Grass G. . ( 2008; ). Contribution of copper ion resistance to survival of Escherichia coli on metallic copper surfaces. . Appl Environ Microbiol 74:, 977–986. [CrossRef] [PubMed]
    [Google Scholar]
  66. Espírito-Santo C. , Morais P. V. , Grass G. . ( 2010; ). Isolation and characterization of bacteria resistant to metallic copper surfaces. . Appl Environ Microbiol 76:, 1341–1348. [CrossRef] [PubMed]
    [Google Scholar]
  67. Essa A. M. , Julian D. J. , Kidd S. P. , Brown N. L. , Hobman J. L. . ( 2003; ). Mercury resistance determinants related to Tn21, Tn1696, and Tn5053 in enterobacteria from the preantibiotic era. . Antimicrob Agents Chemother 47:, 1115–1119. [CrossRef] [PubMed]
    [Google Scholar]
  68. Fournier P.-E. , Vallenet D. , Barbe V. , Audic S. , Ogata H. , Poirel L. , Richet H. , Robert C. , Mangenot S. et al. ( 2006; ). Comparative genomics of multidrug resistance in Acinetobacter baumannii . . PLoS Genet 2:, e7. [CrossRef] [PubMed]
    [Google Scholar]
  69. Fouts D. E. , Mongodin E. F. , Mandrell R. E. , Miller W. G. , Rasko D. A. , Ravel J. , Brinkac L. M. , DeBoy R. T. , Parker C. T. et al. ( 2005; ). Major structural differences and novel potential virulence mechanisms from the genomes of multiple Campylobacter species. . PLoS Biol 3:, e15. [CrossRef] [PubMed]
    [Google Scholar]
  70. Foye W. O. . ( 1977; ). Antimicrobial activities of mineral elements. . In Microorganisms and Minerals, pp. 387–419. Edited by Weinberg E. D. . . New York:: Marcel Dekker;.
    [Google Scholar]
  71. Franke S. . ( 2007;). Microbiology of the toxic noble metal silver. . In Molecular Microbiology of Heavy Metals. pp. 343–-355. Edited by Nies D. H. , Silver S. . . Berlin:: Springer;. [CrossRef]
    [Google Scholar]
  72. Franke S. , Grass G. , Nies D. H. . ( 2001; ). The product of the ybdE gene of the Escherichia coli chromosome is involved in detoxification of silver ions. . Microbiology 147:, 965–972.[PubMed]
    [Google Scholar]
  73. Franke S. , Grass G. , Rensing C. , Nies D. H. . ( 2003; ). Molecular analysis of the copper-transporting efflux system CusCFBA of Escherichia coli . . J Bacteriol 185:, 3804–3812. [CrossRef] [PubMed]
    [Google Scholar]
  74. Fricke W. F. , Welch T. J. , McDermott P. F. , Mammel M. K. , LeClerc J. E. , White D. G. , Cebula T. A. , Ravel J. . ( 2009; ). Comparative genomics of the IncA/C multidrug resistance plasmid family. . J Bacteriol 191:, 4750–4757. [CrossRef] [PubMed]
    [Google Scholar]
  75. Frost L. S. , Leplae R. , Summers A. O. , Toussaint A. . ( 2005; ). Mobile genetic elements: the agents of open source evolution. . Nat Rev Microbiol 3:, 722–732. [CrossRef] [PubMed]
    [Google Scholar]
  76. Gaetke L. M. , Chow C. K. . ( 2003; ). Copper toxicity, oxidative stress, and antioxidant nutrients. . Toxicology 189:, 147–163. [CrossRef] [PubMed]
    [Google Scholar]
  77. Garner J. P. , Heppell P. S. J. . ( 2005; ). Cerium nitrate in the management of burns. . Burns 31:, 539–547. [CrossRef] [PubMed]
    [Google Scholar]
  78. Ge R. , Sun H. . ( 2007; ). Bioinorganic chemistry of bismuth and antimony: target sites of metallodrugs. . Acc Chem Res 40:, 267–274. [CrossRef] [PubMed]
    [Google Scholar]
  79. German N. , Doyscher D. , Rensing C. . ( 2013; ). Bacterial killing in macrophages and amoeba: do they all use a brass dagger?. Future Microbiol 8:, 1257–1264. [CrossRef] [PubMed]
    [Google Scholar]
  80. Giachi G. , Pallecchi P. , Romualdi A. , Ribechini E. , Lucejko J. J. , Colombini M. P. , Mariotti Lippi M. . ( 2013; ). Ingredients of a 2,000-y-old medicine revealed by chemical, mineralogical, and botanical investigations. . Proc Natl Acad Sci U S A 110:, 1193–1196. [CrossRef] [PubMed]
    [Google Scholar]
  81. Gibaud S. , Jaouen G. . ( 2010; ). Arsenic-based drugs: from Fowler’s solution to modern anticancer chemotherapy. . Top Organomet Chem 32:, 1–20.
    [Google Scholar]
  82. Gilmour M. W. , Thomson N. R. , Sanders M. , Parkhill J. , Taylor D. E. . ( 2004; ). The complete nucleotide sequence of the resistance plasmid R478: defining the backbone components of incompatibility group H conjugative plasmids through comparative genomics. . Plasmid 52:, 182–202. [CrossRef] [PubMed]
    [Google Scholar]
  83. Gordon O. , Vig Slenters T. , Brunetto P. S. , Villaruz A. E. , Sturdevant D. E. , Otto M. , Landmann R. , Fromm K. M. . ( 2010; ). Silver coordination polymers for prevention of implant infection: thiol interaction, impact on respiratory chain enzymes, and hydroxyl radical induction. . Antimicrob Agents Chemother 54:, 4208–4218. [CrossRef] [PubMed]
    [Google Scholar]
  84. Grad Y.H. , Godfrey P. , Cerquiera G.C. , Mariani-Kurkdjian P. , Gouali M. , Bingen E. , Shea T.P. , Haas B.J. , Griggs A. et al. ( 2013; ). Comparative genomics of recent Shiga toxin-producing E. coli O104 : H4: short-term evolution of an emerging pathogen. . MBio 4(1)::e00452-12.
    [Google Scholar]
  85. Grass G. , Thakali K. , Klebba P. E. , Thieme D. , Müller A. , Wildner G. F. , Rensing C. . ( 2004; ). Linkage between catecholate siderophores and the multicopper oxidase CueO in Escherichia coli . . J Bacteriol 186:, 5826–5833. [CrossRef] [PubMed]
    [Google Scholar]
  86. Grass G. , Rensing C. , Solioz M. . ( 2011; ). Metallic copper as an antimicrobial surface. . Appl Environ Microbiol 77:, 1541–1547. [CrossRef] [PubMed]
    [Google Scholar]
  87. Guo Z. , Sadler P. J. . ( 1999; ). Metals in medicine. . Angew Chem Int Ed 38:, 1512–1531. [CrossRef]
    [Google Scholar]
  88. Gupta A. , Maynes M. , Silver S. . ( 1998; ). Effects of halides on plasmid-mediated silver resistance in Escherichia coli . . Appl Environ Microbiol 64:, 5042–5045.[PubMed]
    [Google Scholar]
  89. Gupta A. , Matsui K. , Lo J.-F. , Silver S. . ( 1999; a). Molecular basis for resistance to silver cations in Salmonella . . Nat Med 5:, 183–188. [CrossRef] [PubMed]
    [Google Scholar]
  90. Gupta A. , Phung L. T. , Chakravarty L. , Silver S. . ( 1999; b). Mercury resistance in Bacillus cereus RC607: transcriptional organization and two new open reading frames. . J Bacteriol 181:, 7080–7086.[PubMed]
    [Google Scholar]
  91. Gupta A. , Phung L. T. , Taylor D. E. , Silver S. . ( 2001; ). Diversity of silver resistance genes in IncH incompatibility group plasmids. . Microbiology 147:, 3393–3402.[PubMed]
    [Google Scholar]
  92. Hall B. M. . ( 1970; ). Distribution of mercury resistance among Staphylococcus aureus isolated from a hospital community. . J Hyg (Lond) 68:, 111–119. [CrossRef] [PubMed]
    [Google Scholar]
  93. Hasman H. , Aarestrup F. M. . ( 2002; ). tcrB, a gene conferring transferable copper resistance in Enterococcus faecium: occurrence, transferability, and linkage to macrolide and glycopeptide resistance. . Antimicrob Agents Chemother 46:, 1410–1416. [CrossRef] [PubMed]
    [Google Scholar]
  94. Hasman H. , Franke S. , Rensing C. . ( 2006; ). Resistance to metals used in agricultural production. . In Antimicrobial Resistance in Bacteria of Animal Origin, pp. 99–114. Edited by Aarestrup F. M. . . Washington, DC:: American Society for Microbiology;.
    [Google Scholar]
  95. Hedges R. W. , Baumberg S. . ( 1973; ). Resistance to arsenic compounds conferred by a plasmid transmissible between strains of Escherichia coli . . J Bacteriol 115:, 459–460.[PubMed]
    [Google Scholar]
  96. Hobman J. L. , Brown N. L. . ( 1997; ). Bacterial mercury-resistance genes. . In Metal Ions in Biological Systems, pp. 527–568. Edited by Sigel H. , Sigel A. . . New York:: Marcel Dekker;.
    [Google Scholar]
  97. Hobman J. L. , Silver S. . ( 2007; ). Mercury microbiology: resistance systems, environmental aspects, methylation and human health. . In Molecular Microbiology of Heavy Metals, pp. 358–370. Edited by Nies D. H. , Silver S. . . Berlin:: Springer;.
    [Google Scholar]
  98. Hobman J. , Kholodii G. , Nikiforov V. , Ritchie D. A. , Strike P. , Yurieva O. . ( 1994; ). The sequence of the mer operon of pMER327/419 and transposon ends of pMER327/419, 330 and 05. . Gene 146:, 73–78. [CrossRef] [PubMed]
    [Google Scholar]
  99. Hobman J. L. , Essa A. M. M. , Brown N. L. . ( 2002; ). Mercury resistance (mer) operons in enterobacteria. . Biochem Soc Trans 30:, 719–722. [CrossRef] [PubMed]
    [Google Scholar]
  100. Hobman J. L. , Yamamoto K. , Oshima T. . ( 2007; ) Transcriptomic responses of bacterial cells to sublethal metal ion stress. . In Molecular Microbiology of Heavy Metals, pp. 73–115. Edited by Nies D. H. , Silver S. . . Berlin:: Springer;. [CrossRef]
    [Google Scholar]
  101. Hodson M. E. . ( 2004; ). Heavy metals geochemical bogey men?. Environ Pollut 129:, 341–343. [CrossRef] [PubMed]
    [Google Scholar]
  102. Holden M. T. , Seth-Smith H. M. , Crossman L. C. , Sebaihia M. , Bentley S. D. , Cerdeño-Tárraga A. M. , Thomson N. R. , Bason N. , Quail M. A. et al. ( 2009; ). The genome of Burkholderia cenocepacia J2315, an epidemic pathogen of cystic fibrosis patients. . J Bacteriol 191:, 261–277. [CrossRef] [PubMed]
    [Google Scholar]
  103. Holden M. T. G. , Lindsay J. A. , Corton C. , Quail M. A. , Cockfield J. D. , Pathak S. , Batra R. , Parkhill J. , Bentley S. D. , Edgeworth J. D. . ( 2010; ). Genome sequence of a recently emerged, highly transmissible, multi-antibiotic- and antiseptic-resistant variant of methicillin-resistant Staphylococcus aureus, sequence type 239 (TW). . J Bacteriol 192:, 888–892. [CrossRef] [PubMed]
    [Google Scholar]
  104. Holt K. B. , Bard A. J. . ( 2005; ). Interaction of silver(I) ions with the respiratory chain of Escherichia coli: an electrochemical and scanning electrochemical microscopy study of the antimicrobial mechanism of micromolar Ag+ . . Biochemistry 44:, 13214–13223. [CrossRef] [PubMed]
    [Google Scholar]
  105. Holt K. E. , Thomson N. R. , Wain J. , Phan M. D. , Nair S. , Hasan R. , Bhutta Z. A. , Quail M. A. , Norbertczak H. et al. ( 2007; ). Multidrug-resistant Salmonella enterica serovar paratyphi A harbors IncHI1 plasmids similar to those found in serovar typhi. . J Bacteriol 189:, 4257–4264. [CrossRef] [PubMed]
    [Google Scholar]
  106. Hughes M. F. . ( 2002; ). Arsenic toxicity and potential mechanisms of action. . Toxicol Lett 133:, 1–16. [CrossRef] [PubMed]
    [Google Scholar]
  107. Hughes V. M. , Datta N. . ( 1983; ). Conjugative plasmids in bacteria of the ‘pre-antibiotic’ era. . Nature 302:, 725–726. [CrossRef] [PubMed]
    [Google Scholar]
  108. Huisingh D. . ( 1974; ). Heavy metals: implications for agriculture. . Annu Rev Phytopathol 12:, 375–388. [CrossRef]
    [Google Scholar]
  109. Ip M. , Lui S. L. , Poon V. K. M. , Lung I. , Burd A. . ( 2006; ). Antimicrobial activities of silver dressings: an in vitro comparison. . J Med Microbiol 55:, 59–63. [CrossRef] [PubMed]
    [Google Scholar]
  110. Izumiya H. , Sekizuka T. , Nakaya H. , Taguchi M. , Oguchi A. , Ichikawa N. , Nishiko R. , Yamazaki S. , Fujita N. et al. ( 2011; ). Whole-genome analysis of Salmonella enterica serovar Typhimurium T000240 reveals the acquisition of a genomic island involved in multidrug resistance via IS1 derivatives on the chromosome. . Antimicrob Agents Chemother 55:, 623–630. [CrossRef] [PubMed]
    [Google Scholar]
  111. Jiang J. , Alvarez C. , Kukutla P. , Yu W. , Xu J. . ( 2012; ). Draft genome sequences of Enterobacter sp. isolate Ag1 from the midgut of the malaria mosquito Anopheles gambiae . . J Bacteriol 194:, 5481. [CrossRef] [PubMed]
    [Google Scholar]
  112. Johnson T. J. , Siek K. E. , Johnson S. J. , Nolan L. K. . ( 2005; ). DNA sequence and comparative genomics of pAPEC-O2-R, an avian pathogenic Escherichia coli transmissible R plasmid. . Antimicrob Agents Chemother 49:, 4681–4688. [CrossRef] [PubMed]
    [Google Scholar]
  113. Johnson T. J. , Wannemeuhler Y. M. , Scaccianoce J. A. , Johnson S. J. , Nolan L. K. . ( 2006; ). Complete DNA sequence, comparative genomics, and prevalence of an IncHI2 plasmid occurring among extraintestinal pathogenic Escherichia coli isolates. . Antimicrob Agents Chemother 50:, 3929–3933. [CrossRef] [PubMed]
    [Google Scholar]
  114. Jolliffe D. M. . ( 1993; ). A history of the use of arsenicals in man. . J R Soc Med 86:, 287–289.[PubMed]
    [Google Scholar]
  115. Jones F. T. . ( 2007; ). A broad view of arsenic. . Poult Sci 86:, 2–14. [CrossRef] [PubMed]
    [Google Scholar]
  116. Kazantzis G. . ( 2000; ). Thallium in the environment and health effects. . Environ Geochem Health 22:, 275–280. [CrossRef]
    [Google Scholar]
  117. Khachatourians G. G. . ( 1998; ). Agricultural use of antibiotics and the evolution and transfer of antibiotic-resistant bacteria. . CMAJ 159:, 1129–1136.[PubMed]
    [Google Scholar]
  118. Kholodii G. , Mindlin S. , Petrova M. , Minakhina S. . ( 2003; ). Tn5060 from the Siberian permafrost is most closely related to the ancestor of Tn21 prior to integron acquisition. . FEMS Microbiol Lett 226:, 251–255. [CrossRef] [PubMed]
    [Google Scholar]
  119. Kiyono M. , Sone Y. , Nakamura R. , Pan-Hou H. , Sakabe K. . ( 2009; ). The MerE protein encoded by transposon Tn21 is a broad mercury transporter in Escherichia coli . . FEBS Lett 583:, 1127–1131. [CrossRef] [PubMed]
    [Google Scholar]
  120. Klasen H. J. . ( 2000; a). Historical review of the use of silver in the treatment of burns. I. Early uses. . Burns 26:, 117–130. [CrossRef] [PubMed]
    [Google Scholar]
  121. Klasen H. J. . ( 2000; b). A historical review of the use of silver in the treatment of burns. II. Renewed interest for silver. . Burns 26:, 131–138. [CrossRef] [PubMed]
    [Google Scholar]
  122. Kremer A. N. , Hoffmann H. . ( 2012; ). Subtractive hybridization yields a silver resistance determinant unique to nosocomial pathogens in the Enterobacter cloacae complex. . J Clin Microbiol 50:, 3249–3257. [CrossRef] [PubMed]
    [Google Scholar]
  123. Kruger M. C. , Bertin P. N. , Heipieper H. J. , Arsène-Ploetze F. . ( 2013; ). Bacterial metabolism of environmental arsenic mechanisms and biotechnological applications. . Appl Microbiol Biotechnol 97:, 3827–3841. [CrossRef] [PubMed]
    [Google Scholar]
  124. Kucerova E. , Clifton S. W. , Xia X.-Q. , Long F. , Porwollik S. , Fulton L. , Fronick C. , Minx P. , Kyung K. et al. ( 2010; ). Genome sequence of Cronobacter sakazakii BAA-894 and comparative genomic hybridization analysis with other Cronobacter species. . PLoS One 5:, e9556. [CrossRef] [PubMed]
    [Google Scholar]
  125. Kuenne C. , Voget S. , Pischimarov J. , Oehm S. , Goesmann A. , Daniel R. , Hain T. , Chakraborty T. . ( 2010; ). Comparative analysis of plasmids in the genus Listeria . . PLoS One 5:, e12511. [CrossRef] [PubMed]
    [Google Scholar]
  126. Kumagai Y. , Sumi D. . ( 2007; ). Arsenic: signal transduction, transcription factor, and biotransformation involved in cellular response and toxicity. . Annu Rev Pharmacol Toxicol 47:, 243–262. [CrossRef] [PubMed]
    [Google Scholar]
  127. Lee S. , Rakic-Martinez M. , Graves L. M. , Ward T. J. , Siletzky R. M. , Kathariou S. . ( 2013; ). Genetic determinants for cadmium and arsenic resistance among Listeria monocytogenes serotype 4b isolates from sporadic human listeriosis patients. . Appl Environ Microbiol 79:, 2471–2476. [CrossRef] [PubMed]
    [Google Scholar]
  128. Lee S. , Ward T. J. , Graves L. M. , Tarr C. L. , Siletzky R. M. , Kathariou S. . ( 2014; ). Population structure of Listeria monocytogenes serotype 4b isolates from sporadic human listeriosis cases in the United States from 2003 to 2008. . Appl Environ Microbiol 80:, 3632–3644. [CrossRef] [PubMed]
    [Google Scholar]
  129. Lemire J. A. , Harrison J. J. , Turner R. J. . ( 2013; ). Antimicrobial activity of metals: mechanisms, molecular targets and applications. . Nat Rev Microbiol 11:, 371–384. [CrossRef] [PubMed]
    [Google Scholar]
  130. Lenihan J. . ( 1988; ). The Crumbs of Creation. Bristol:: Adam Hilger;.
    [Google Scholar]
  131. Levings R. S. , Partridge S. R. , Djordjevic S. P. , Hall R. M. . ( 2007; ). SGI1-K, a variant of the SGI1 genomic island carrying a mercury resistance region, in Salmonella enterica serovar Kentucky. . Antimicrob Agent Chemother 51, 317–323.[CrossRef]
    [Google Scholar]
  132. Levy S. B. , Marshall B. . ( 2004; ). Antibacterial resistance worldwide: causes, challenges and responses. . Nat Med 10: (Suppl), S122–S129. [CrossRef] [PubMed]
    [Google Scholar]
  133. Liebert C. A. , Hall R. M. , Summers A. O. . ( 1999; ). Transposon Tn21, flagship of the floating genome. . Microbiol Mol Biol Rev 63:, 507–522.[PubMed]
    [Google Scholar]
  134. Lin Y.-F. , Walmsley A. R. , Rosen B. P. . ( 2006; ). An arsenic metallochaperone for an arsenic detoxification pump. . Proc Natl Acad Sci U S A 103:, 15617–15622. [CrossRef] [PubMed]
    [Google Scholar]
  135. Liu J. , Lu Y. , Wu Q. , Goyer R. A. , Waalkes M. P. . ( 2008; ). Mineral arsenicals in traditional medicines: orpiment, realgar, and arsenolite. . J Pharmacol Exp Ther 326:, 363–368. [CrossRef] [PubMed]
    [Google Scholar]
  136. Liu T. , Ramesh A. , Ma Z. , Ward S. K. , Zhang L. , George G. N. , Talaat A. M. , Sacchettini J. C. , Giedroc D. P. . ( 2007; ). CsoR is a novel Mycobacterium tuberculosis copper-sensing transcriptional regulator. . Nat Chem Biol 3:, 60–68. [CrossRef] [PubMed]
    [Google Scholar]
  137. Loh J. V. , Percival S. L. , Woods E. J. , Williams N. J. , Cochrane C. A. . ( 2009; ). Silver resistance in MRSA isolated from wound and nasal sources in humans and animals. . Int Wound J 6:, 32–38. [CrossRef] [PubMed]
    [Google Scholar]
  138. Lok C.-N. , Ho C.-M. , Chen R. , He Q.-Y. , Yu W.-Y. , Sun H. , Tam P. K.-H. , Chiu J.-F. , Che C.-M. . ( 2006; ). Proteomic analysis of the mode of antibacterial action of silver nanoparticles. . J Proteome Res 5:, 916–924. [CrossRef] [PubMed]
    [Google Scholar]
  139. Lok C.-N. , Ho C.-M. , Chen R. , He Q.-Y. , Yu W.-Y. , Sun H. , Tam P. K.-H. , Chiu J.-F. , Che C.-M. . ( 2007; ). Silver nanoparticles: partial oxidation and antibacterial activities. . J Biol Inorg Chem 12:, 527–534. [CrossRef] [PubMed]
    [Google Scholar]
  140. Macomber L. , Imlay J. A. . ( 2009; ). The iron–sulfur clusters of dehydratases are primary intracellular targets of copper toxicity. . Proc Natl Acad Sci U S A 106:, 8344–8349. [CrossRef] [PubMed]
    [Google Scholar]
  141. Macomber L. , Rensing C. , Imlay J. A. . ( 2007; ). Intracellular copper does not catalyze the formation of oxidative DNA damage in Escherichia coli . . J Bacteriol 189:, 1616–1626. [CrossRef] [PubMed]
    [Google Scholar]
  142. Mahony D. E. , Lim-Morrison S. , Bryden L. , Faulkner G. , Hoffman P. S. , Agocs L. , Briand G. G. , Burford N. , Maguire H. . ( 1999; ). Antimicrobial activities of synthetic bismuth compounds against Clostridium difficile . . Antimicrob Agents Chemother 43:, 582–588.[PubMed]
    [Google Scholar]
  143. Malachowa N. , DeLeo F. R. . ( 2010; ). Mobile genetic elements of Staphylococcus aureus . . Cell Mol Life Sci 67:, 3057–3071. [CrossRef] [PubMed]
    [Google Scholar]
  144. Marais F. , Mehtar S. , Chalkley L. . ( 2010; ). Antimicrobial efficacy of copper touch surfaces in reducing environmental bioburden in a South African community healthcare facility. . J Hosp Infect 74:, 80–82. [CrossRef] [PubMed]
    [Google Scholar]
  145. Marshall B. M. , Ochieng D. J. , Levy S. B. . ( 2009; ). Commensals: underappreciated reservoir of antibiotic resistance. . Microbe 4:, 231–238.
    [Google Scholar]
  146. Martins Simões P. , Rasigade J. P. , Lemriss H. , Butin M. , Ginevra C. , Lemriss S. , Goering R. V. , Ibrahimi A. , Picaud J. C. et al. ( 2013; ). Characterization of a novel composite staphylococcal cassette chromosome mec (SCCmec-SCCcad/ars/cop) in the neonatal sepsis-associated Staphylococcus capitis pulsotype NRCS-A. . Antimicrob Agents Chemother 57:, 6354–6357. [CrossRef] [PubMed]
    [Google Scholar]
  147. Mazel D. . ( 2006; ). Integrons: agents of bacterial evolution. . Nat Rev Microbiol 4:, 608–620. [CrossRef] [PubMed]
    [Google Scholar]
  148. Mazel D. , Dychinco B. , Webb V. A. , Davies J. . ( 2000; ). Antibiotic resistance in the ECOR collection: integrons and identification of a novel aad gene. . Antimicrob Agents Chemother 44:, 1568–1574. [CrossRef] [PubMed]
    [Google Scholar]
  149. McCallum R. I. . ( 1977; ). President’s address. Observations upon antimony. . Proc R Soc Med 70:, 756–763.[PubMed]
    [Google Scholar]
  150. McHugh G. L. , Moellering R. C. , Hopkins C. C. , Swartz M. N. . ( 1975; ). Salmonella typhimurium resistant to silver nitrate, chloramphenicol and ampicillin. A new threat in burn units?. Lancet 305:, 235–240. [CrossRef]
    [Google Scholar]
  151. Mergeay M. , Monchy S. , Vallaeys T. , Auquier V. , Benotmane A. , Bertin P. , Taghavi S. , Dunn J. , van der Lelie D. , Wattiez R. . ( 2003; ). Ralstonia metallidurans, a bacterium specifically adapted to toxic metals: towards a catalogue of metal-responsive genes. . FEMS Microbiol Rev 27:, 385–410. [CrossRef] [PubMed]
    [Google Scholar]
  152. Meynell E. , Datta N. . ( 1966; ). The relation of resistance transfer factors to the F-factor (sex-factor) of Escherichia coli K12. . Genet Res 7:, 134–140. [CrossRef] [PubMed]
    [Google Scholar]
  153. Mijnendonckx K. , Leys N. , Mahillon J. , Silver S. , Van Houdt R. . ( 2013; ). Antimicrobial silver: uses, toxicity and potential for resistance. . Biometals 26:, 609–621. [CrossRef] [PubMed]
    [Google Scholar]
  154. Mikolay A. , Huggett S. , Tikana L. , Grass G. , Braun J. , Nies D. H. . ( 2010; ). Survival of bacteria on metallic copper surfaces in a hospital trial. . Appl Microbiol Biotechnol 87:, 1875–1879. [CrossRef] [PubMed]
    [Google Scholar]
  155. Mindlin S. , Petrova M. . ( 2013; ). Mercury resistance transposons. . In Bacterial Integrative Mobile Genetic Elements, pp. 33–52. Edited by Roberts A. P. , Mullany P. . . Austin, TX:: Landes Bioscience;.
    [Google Scholar]
  156. Monchy S. , Benotmane M. A. , 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:, 7417–7425. [CrossRef] [PubMed]
    [Google Scholar]
  157. Moore B. . ( 1960; ). A new screen test and selective medium for the rapid detection of epidemic strains of Staph. aureus . . Lancet 276:, 453–458. [CrossRef] [PubMed]
    [Google Scholar]
  158. Morby A. P. , Hobman J. L. , Brown N. L. . ( 1995; ). The role of cysteine residues in the transport of mercuric ions by the Tn501 MerT and MerP mercury-resistance proteins. . Mol Microbiol 17:, 25–35. [CrossRef] [PubMed]
    [Google Scholar]
  159. Morones-Ramirez J. R. , Winkler J. A. , Spina C. S. , Collins J. J. . ( 2013; ). Silver enhances antibiotic activity against Gram-negative bacteria. . Sci Transl Med 5:, 190ra81. [CrossRef] [PubMed]
    [Google Scholar]
  160. Moyer C. A. , Brentano L. , Gravens D. L. , Margraf H. W. , Monafo W. W. Jr . ( 1965; ). Treatment of large human burns with 0.5 % silver nitrate solution. . Arch Surg 90:, 812–867. [CrossRef] [PubMed]
    [Google Scholar]
  161. Munson G. P. , Lam D. L. , Outten F. W. , O’Halloran T. V. . ( 2000; ). Identification of a copper-responsive two-component system on the chromosome of Escherichia coli K-12. . J Bacteriol 182:, 5864–5871. [CrossRef] [PubMed]
    [Google Scholar]
  162. Nakahara H. , Ishikawa T. , Sarai Y. , Kondo I. , Mitsuhashi S. . ( 1977; ). Frequency of heavy-metal resistance in bacteria from inpatients in Japan. . Nature 266:, 165–167. [CrossRef] [PubMed]
    [Google Scholar]
  163. Nakaya R. , Nakamura A. , Murata Y. . ( 1960; ). Resistance transfer agents in Shigella . . Biochem Biophys Res Commun 3:, 654–659. [CrossRef] [PubMed]
    [Google Scholar]
  164. Neyt C. , Iriarte M. , Thi V. H. , Cornelis G. R. . ( 1997; ). Virulence and arsenic resistance in Yersiniae . . J Bacteriol 179:, 612–619.[PubMed]
    [Google Scholar]
  165. Nieboer E. , Richardson D. H. S. . ( 1980; ). The replacement of the nondescript term ‘heavy metals’ by a biologically and chemically significant classification of heavy metals. . Environ Pollut B 1:, 3–26. [CrossRef]
    [Google Scholar]
  166. Nies D. H. . ( 1999; ). Microbial heavy-metal resistance. . Appl Microbiol Biotechnol 51:, 730–750. [CrossRef] [PubMed]
    [Google Scholar]
  167. Nishino K. , Yamasaki S. , Hayashi-Nishino M. , Yamaguchi A. . ( 2010; ). Effect of NlpE overproduction on multidrug resistance in Escherichia coli . . Antimicrob Agents Chemother 54:, 2239–2243. [CrossRef] [PubMed]
    [Google Scholar]
  168. Novais A. , Baquero F. , Machado E. , Cantón R. , Peixe L. , Coque T. M. . ( 2010; ). International spread and persistence of TEM-24 is caused by the confluence of highly penetrating Enterobacteriaceae clones and an IncA/C2 plasmid containing Tn1696 : : Tn1 and IS5075-Tn21. . Antimicrob Agents Chemother 54:, 825–834. [CrossRef] [PubMed]
    [Google Scholar]
  169. Novelli F. , Recine M. , Sparatore F. , Juliano C. . ( 1999; ). Gold(I) complexes as antimicrobial agents. . Farmaco 54:, 232–236. [CrossRef] [PubMed]
    [Google Scholar]
  170. Novick R. P. , Roth C. . ( 1968; ). Plasmid-linked resistance to inorganic salts in Staphylococcus aureus . . J Bacteriol 95:, 1335–1342. [CrossRef] [PubMed]
    [Google Scholar]
  171. Nowack B. , Krug H. F. , Height M. . ( 2011; ). 120 years of nanosilver history: implications for policy makers. . Environ Sci Technol 45:, 1177–1183. [CrossRef] [PubMed]
    [Google Scholar]
  172. Oremland R. S. , Stolz J. F. . ( 2003; ). The ecology of arsenic. . Science 300:, 939–944. [CrossRef] [PubMed]
    [Google Scholar]
  173. Osman D. , Cavet J. S. . ( 2008; ). Copper homeostasis in bacteria. . Adv Appl Microbiol 65:, 217–247. [CrossRef] [PubMed]
    [Google Scholar]
  174. Outten F. W. , Outten C. E. , Hale J. , O’Halloran T. V. . ( 2000; ). Transcriptional activation of an Escherichia coli copper efflux regulon by the chromosomal MerR homologue, cueR . . J Biol Chem 275:, 31024–31029. [CrossRef] [PubMed]
    [Google Scholar]
  175. Outten F. W. , Huffman D. L. , Hale J. A. , O’Halloran T. V. . ( 2001; ). The independent cue and cus systems confer copper tolerance during aerobic and anaerobic growth in Escherichia coli . . J Biol Chem 276:, 30670–30677. [CrossRef] [PubMed]
    [Google Scholar]
  176. Paauw A. , Caspers M. P. M. , Leverstein-van Hall M. A. , Schuren F. H. J. , Montijn R. C. , Verhoef J. , Fluit A. C. . ( 2009; ). Identification of resistance and virulence factors in an epidemic Enterobacter hormaechei outbreak strain. . Microbiology 155:, 1478–1488. [CrossRef] [PubMed]
    [Google Scholar]
  177. Pages D. , Rose J. , Conrod S. , Cuine S. , Carrier P. , Heulin T. , Achouak W. . ( 2008; ). Heavy metal tolerance in Stenotrophomonas maltophilia . . PLoS One 3:, e1539. [CrossRef] [PubMed]
    [Google Scholar]
  178. Panyala N. R. , Peña-Méndez E. M. , Havel J. . ( 2008; ). Silver or silver nanoparticles: a hazardous threat to the environment and human health. . J Appl Biomed 6:, 117–129.
    [Google Scholar]
  179. Park H.-J. , Kim J. Y. , Kim J. , Lee J.-H. , Hahn J.-S. , Gu M. B. , Yoon J. . ( 2009; ). Silver-ion-mediated reactive oxygen species generation affecting bactericidal activity. . Water Res 43:, 1027–1032. [CrossRef] [PubMed]
    [Google Scholar]
  180. Parkhill J. , Dougan G. , James K. D. , Thomson N. R. , Pickard D. , Wain J. , Churcher C. , Mungall K. L. , Bentley S. D. et al. ( 2001; ). Complete genome sequence of a multiple drug resistant Salmonella enterica serovar Typhi CT18. . Nature 413:, 848–852. [CrossRef] [PubMed]
    [Google Scholar]
  181. Partridge S. R. . ( 2011; ). Analysis of antibiotic resistance regions in Gram-negative bacteria. . FEMS Microbiol Rev 35:, 820–855. [CrossRef] [PubMed]
    [Google Scholar]
  182. Partridge S. R. , Brown H. J. , Stokes H. W. , Hall R. M. . ( 2001; ). Transposons Tn1696 and Tn21 and their integrons In4 and In2 have independent origins. . Antimicrob Agents Chemother 45:, 1263–1270. [CrossRef] [PubMed]
    [Google Scholar]
  183. Perreten V. , Chanchaithong P. , Prapasarakul N. , Rossano A. , Blum S. E. , Elad D. , Schwendener S. . ( 2013; ). Novel pseudo-staphylococcal cassette chromosome mec element (ψSCCmec57395) in methicillin-resistant Staphylococcus pseudintermedius CC45. . Antimicrob Agents Chemother 57:, 5509–5515. [CrossRef] [PubMed]
    [Google Scholar]
  184. Perry M. R. , Wyllie S. , Prajapati V. K. , Feldmann J. , Sundar S. , Boelaert M. , Fairlamb A. H. . ( 2011; ). Visceral leishmaniasis and arsenic: an ancient poison contributing to antimonial treatment failure in the Indian subcontinent?. PLoS Negl Trop Dis 5:, e1227. [CrossRef] [PubMed]
    [Google Scholar]
  185. Perry M. R. , Wyllie S. , Raab A. , Feldmann J. , Fairlamb A. H. . ( 2013; ). Chronic exposure to arsenic in drinking water can lead to resistance to antimonial drugs in a mouse model of visceral leishmaniasis. . Proc Natl Acad Sci U S A 110:, 19932–19937. [CrossRef] [PubMed]
    [Google Scholar]
  186. Petersen C. , Møller L. B. . ( 2000; ). Control of copper homeostasis in Escherichia coli by a P-type ATPase, CopA, and a MerR-like transcriptional activator, CopR. . Gene 261:, 289–298. [CrossRef] [PubMed]
    [Google Scholar]
  187. Pirnay J.-P. , De Vos D. , Cochez C. , Bilocq F. , Pirson J. , Struelens M. , Duinslaeger L. , Cornelis P. , Zizi M. , Vanderkelen A. . ( 2003; ). Molecular epidemiology of Pseudomonas aeruginosa colonization in a burn unit: persistence of a multidrug-resistant clone and a silver sulfadiazine-resistant clone. . J Clin Microbiol 41:, 1192–1202. [CrossRef] [PubMed]
    [Google Scholar]
  188. Pontel L. B. , Scampoli N. L. , Porwollik S. , Checa S. K. , McClelland M. , Soncini F. C. . ( 2014; ). Identification of a Salmonella ancillary copper detoxification mechanism by a comparative analysis of the genome-wide transcriptional response to copper and zinc excess. . Microbiology 160:, 1659–1669. [CrossRef] [PubMed]
    [Google Scholar]
  189. Porter F. D. , Silver S. , Ong C. , Nakahara H. . ( 1982; ). Selection for mercurial resistance in hospital settings. . Antimicrob Agents Chemother 22:, 852–858. [CrossRef] [PubMed]
    [Google Scholar]
  190. Post V. , Hall R. M. . ( 2009; ). AbaR5, a large multiple-antibiotic resistance region found in Acinetobacter baumannii . . Antimicrob Agents Chemother 53:, 2667–2671. [CrossRef] [PubMed]
    [Google Scholar]
  191. Post V. , White P. A. , Hall R. M. . ( 2010; ). Evolution of AbaR5-type genomic resistance islands in multiply antibiotic resistance Acinetobacter baumannii . . Antimicrob Agents Chemother 65:, 1162–1170. [CrossRef] [PubMed]
    [Google Scholar]
  192. Przygoda G. , Feldmann J. , Cullen W. R. . ( 2001; ). The arsenic eaters of Styria: a different picture of people who were chronically exposed to arsenic. . Appl Organomet Chem 15:, 457–462. [CrossRef]
    [Google Scholar]
  193. Randall C. P. , Oyama L. B. , Bostock J. M. , Chopra I. , O’Neill A. J. . ( 2013; ). The silver cation (Ag+): antistaphylococcal activity, mode of action and resistance studies. . J Antimicrob Chemother 68:, 131–138. [CrossRef] [PubMed]
    [Google Scholar]
  194. Ray S. , Mohan R. , Singh J. K. , Samantaray M. K. , Shaikh M. M. , Panda D. , Ghosh P. . ( 2007; ). Anticancer and antimicrobial metallopharmaceutical agents based on palladium, gold, and silver N-heterocyclic carbene complexes. . J Am Chem Soc 129:, 15042–15053. [CrossRef] [PubMed]
    [Google Scholar]
  195. Reith M. E. , Singh R. K. , Curtis B. , Boyd J. M. , Bouevitch A. , Kimball J. , Munholland J. , Murphy C. , Sarty D. et al. ( 2008; ). The genome of Aeromonas salmonicida subsp. salmonicida A449: insights into the evolution of a fish pathogen. . BMC Genomics 9:, 427. [CrossRef] [PubMed]
    [Google Scholar]
  196. Ren Y. , Ren Y. , Zhou Z. , Guo X. , Li Y. , Feng L. , Wang L. . ( 2010; ). Complete genome sequence of Enterobacter cloacae subsp. cloacae type strain ATCC 13047. . J Bacteriol 192:, 2463–2464. [CrossRef] [PubMed]
    [Google Scholar]
  197. Rensing C. , Grass G. . ( 2003; ). Escherichia coli mechanisms of copper homeostasis in a changing environment. . FEMS Microbiol Rev 27:, 197–213. [CrossRef] [PubMed]
    [Google Scholar]
  198. Reva O. N. , Bezuidt O. . ( 2012; ). Distribution of horizontally transferred heavy metal resistance operons in recent outbreak bacteria. . Mobile Genet Elements 2:, 96–100. [CrossRef] [PubMed]
    [Google Scholar]
  199. Richmond M. H. , John M. . ( 1964; ). Co-transduction by a staphylococcal phage of the genes responsible for penicillinase synthesis and resistance to mercury salts. . Nature 202:, 1360–1361. [CrossRef] [PubMed]
    [Google Scholar]
  200. Ripoll F. , Pasek S. , Schenowitz C. , Dossat C. , Barbe V. , Rottman M. , Macheras E. , Heym B. , Herrmann J.-L. et al. ( 2009; ). Non mycobacterial virulence genes in the genome of the emerging pathogen Mycobacterium abscessus . . PLoS One 4:, e5660. [CrossRef] [PubMed]
    [Google Scholar]
  201. Rouch D. A. , Brown N. L. . ( 1997; ). Copper-inducible transcriptional regulation at two promoters in the Escherichia coli copper resistance determinant pco . . Microbiology 143:, 1191–1202. [CrossRef] [PubMed]
    [Google Scholar]
  202. Roy P. H. , Tetu S. G. , Larouche A. , Elbourne L. , Tremblay S. , Ren Q. , Dodson R. , Harkins D. , Shay R. et al. ( 2010; ). Complete genome sequence of the multiresistant taxonomic outlier Pseudomonas aeruginosa PA7. . PLoS One 5:, e8842. [CrossRef] [PubMed]
    [Google Scholar]
  203. Russell P. E. . ( 2005; ). A century of fungicide evolution. . J Agric Sci 143:, 11–25. [CrossRef]
    [Google Scholar]
  204. Ryan D. , Colleran E. . ( 2002; ). Arsenical resistance in the IncHI2 plasmids. . Plasmid 47:, 234–240. [CrossRef] [PubMed]
    [Google Scholar]
  205. Sahlman L. , Wong W. , Powlowski J. . ( 1997; ). A mercuric ion uptake role for the integral inner membrane protein, MerC, involved in bacterial mercuric ion resistance. . J Biol Chem 272:, 29518–29526. [CrossRef] [PubMed]
    [Google Scholar]
  206. Sampei G. , Furuya N. , Tachibana K. , Saitou Y. , Suzuki T. , Mizobuchi K. , Komano T. . ( 2010; ). Complete genome sequence of the incompatibility group I1 plasmid R64. . Plasmid 64:, 92–103. [CrossRef] [PubMed]
    [Google Scholar]
  207. Sandegren L. , Linkevicius M. , Lytsy B. , Melhus A. , Andersson D. I. . ( 2012; ). Transfer of an Escherichia coli ST131 multiresistance cassette has created a Klebsiella pneumoniae-specific plasmid associated with a major nosocomial outbreak. . J Antimicrob Chemother 67:, 74–83. [CrossRef] [PubMed]
    [Google Scholar]
  208. Sapkota A. R. , Lefferts L. Y. , McKenzie S. , Walker P. . ( 2007; ). What do we feed to food-production animals? A review of animal feed ingredients and their potential impacts on human health. . Environ Health Perspect 115:, 663–670. [CrossRef] [PubMed]
    [Google Scholar]
  209. Schottel J. , Mandal A. , Clark D. , Silver S. , Hedges R. W. . ( 1974; ). Volatilisation of mercury and organomercurials determined by inducible R-factor systems in enteric bacteria. . Nature 251:, 335–337. [CrossRef] [PubMed]
    [Google Scholar]
  210. Shore A. C. , Deasy E. C. , Slickers P. , Brennan G. , O’Connell B. , Monecke S. , Ehricht R. , Coleman D. C. . ( 2011; ). Detection of staphylococcal cassette chromosome mec type XI carrying highly divergent mecA, mecI, mecR1, blaZ, and ccr genes in human clinical isolates of clonal complex 130 methicillin-resistant Staphylococcus aureus . . Antimicrob Agents Chemother 55:, 3765–3773. [CrossRef] [PubMed]
    [Google Scholar]
  211. Silbergeld E. K. , Graham J. , Price L. B. . ( 2008; ). Industrial food animal production, antimicrobial resistance, and human health. . Annu Rev Public Health 29:, 151–169. [CrossRef] [PubMed]
    [Google Scholar]
  212. Silver S. . ( 1998; ). Genes for all metals a bacterial view of the periodic table. The 1996 Thom Award Lecture. . J Ind Microbiol Biotechnol 20:, 1–12. [CrossRef] [PubMed]
    [Google Scholar]
  213. Silver S. . ( 2003; ). Bacterial silver resistance: molecular biology and uses and misuses of silver compounds. . FEMS Microbiol Rev 27:, 341–353. [CrossRef] [PubMed]
    [Google Scholar]
  214. Silver S. , Phung L. T. . ( 1996; ). Bacterial heavy metal resistance: new surprises. . Annu Rev Microbiol 50:, 753–789. [CrossRef] [PubMed]
    [Google Scholar]
  215. Silver S. , Phung T. . ( 2005; ). A bacterial view of the periodic table: genes and proteins for toxic inorganic ions. . J Ind Microbiol Biotechnol 32:, 587–605. [CrossRef] [PubMed]
    [Google Scholar]
  216. Silver S. , Phung T. , Silver G. . ( 2006; ). Silver as biocides in burn and wound dressings and bacterial resistance to silver compounds. . J Ind Microbiol Biotechnol 33:, 627–634. [CrossRef] [PubMed]
    [Google Scholar]
  217. Singer R. S. , Ward M. P. , Maldonado G. . ( 2006; ). Can landscape ecology untangle the complexity of antibiotic resistance?. Nat Rev Microbiol 4:, 943–952. [CrossRef] [PubMed]
    [Google Scholar]
  218. Skurnik D. , Ruimy R. , Ready D. , Ruppe E. , Bernède-Bauduin C. , Djossou F. , Guillemot D. , Pier G. B. , Andremont A. . ( 2010; ). Is exposure to mercury a driving force for the carriage of antibiotic resistance genes?. J Med Microbiol 59:, 804–807. [CrossRef] [PubMed]
    [Google Scholar]
  219. Šlejkovec Z. , Falnoga I. , van Elteren J. T. . ( 2012; ). Arsenic trioxide versus tetraarsenic oxide in biomedical research: misunderstandings and misinterpretations. . Biometals 25:, 231–235. [CrossRef] [PubMed]
    [Google Scholar]
  220. Smaldone G. T. , Helmann J. D. . ( 2007; ). CsoR regulates the copper efflux operon copZA in Bacillus subtilis . . Microbiology 153:, 4123–4128. [CrossRef] [PubMed]
    [Google Scholar]
  221. Smith D. H. . ( 1967; ). R factors mediate resistance to mercury, nickel, and cobalt. . Science 156:, 1114–1116. [CrossRef] [PubMed]
    [Google Scholar]
  222. Soge O. O. , Beck N. K. , White T. M. , No D. B. , Roberts M. C. . ( 2008; ). A novel transposon, Tn6009, composed of a Tn916 element linked with a Staphylococcus aureus mer operon. . J Antimicrob Chemother 62:, 674–680. [CrossRef] [PubMed]
    [Google Scholar]
  223. Solioz M. , Abicht H. K. , Mermod M. , Mancini S. . ( 2010; ). Response of Gram-positive bacteria to copper stress. . J Biol Inorg Chem 15:, 3–14. [CrossRef] [PubMed]
    [Google Scholar]
  224. Sone Y. , Nakamura R. , Pan-Hou H. , Sato M. H. , Itoh T. , Kiyono M. . ( 2013; ). Increase methylmercury accumulation in Arabidopsis thaliana expressing bacterial broad-spectrum mercury transporter MerE. . AMB Express 3:, 52. [CrossRef] [PubMed]
    [Google Scholar]
  225. Stepanauskas R. , Glenn T. C. , Jagoe C. H. , Tuckfield R. C. , Lindell A. H. , King C. J. , McArthur J. V. . ( 2006; ). Coselection for microbial resistance to metals and antibiotics in freshwater microcosms. . Environ Microbiol 8:, 1510–1514. [CrossRef] [PubMed]
    [Google Scholar]
  226. Stoyanov J. V. , Hobman J. L. , Brown N. L. . ( 2001; ). CueR (ybbI) of Escherichia coli is a MerR family regulator controlling expression of the copper exporter CopA. . Mol Microbiol 39:, 502–512. [CrossRef] [PubMed]
    [Google Scholar]
  227. Summers A. O. . ( 2002; ). Generally overlooked fundamentals of bacterial genetics and ecology. . Clin Infect Dis 34: (Suppl 3), S85–S92. [CrossRef] [PubMed]
    [Google Scholar]
  228. Summers A. O. . ( 2006; ). Genetic linkage and horizontal gene transfer, the roots of the antibiotic multi-resistance problem. . Anim Biotechnol 17:, 125–135. [CrossRef] [PubMed]
    [Google Scholar]
  229. Sundar S. , Chakravarty J. . ( 2010; ). Antimony toxicity. . Int J Environ Res Public Health 7:, 4267–4277. [CrossRef] [PubMed]
    [Google Scholar]
  230. Sütterlin S. , Tano E. , Bergsten A. , Tallberg A.-B. , Melhus A. . ( 2012; ). Effects of silver-based wound dressings on the bacterial flora in chronic leg ulcers and its susceptibility in vitro to silver. . Acta Derm Venereol 92:, 34–39. [CrossRef] [PubMed]
    [Google Scholar]
  231. Taylor D. E. . ( 1999; ). Bacterial tellurite resistance. . Trends Microbiol 7:, 111–115. [CrossRef] [PubMed]
    [Google Scholar]
  232. Tetaz T. J. , Luke R. K. J. . ( 1983; ). Plasmid-controlled resistance to copper in Escherichia coli . . J Bacteriol 154:, 1263–1268.[PubMed]
    [Google Scholar]
  233. Toleman M. A. , Walsh T. R. . ( 2011; ). Combinatorial events of insertion sequences and ICE in Gram-negative bacteria. . FEMS Microbiol Rev 35:, 912–935. [CrossRef] [PubMed]
    [Google Scholar]
  234. Trotter R. T. II . ( 1990; ). The cultural parameters of lead poisoning: a medical anthropologist’s view of intervention in environmental lead exposure. . Environ Health Perspect 89:, 79–84. [CrossRef] [PubMed]
    [Google Scholar]
  235. Van Houdt R. , Mijnendonckx K. , Leys N. . ( 2012; ). Microbial contamination monitoring and control during human space missions. . Planet Space Sci 60:, 115–120. [CrossRef]
    [Google Scholar]
  236. Venturini C. , Beatson S. A. , Djordjevic S. P. , Walker M. J. . ( 2010; ). Multiple antibiotic resistance gene recruitment onto the enterohemorrhagic Escherichia coli virulence plasmid. . FASEB J 24:, 1160–1166. [CrossRef] [PubMed]
    [Google Scholar]
  237. Waldron K. J. , Robinson N. J. . ( 2009; ). How do bacterial cells ensure that metalloproteins get the correct metal?. Nat Rev Microbiol 7:, 25–35. [CrossRef] [PubMed]
    [Google Scholar]
  238. Wang L. , Jeon B. , Sahin O. , Zhang Q. . ( 2009; ). Identification of an arsenic resistance and arsenic-sensing system in Campylobacter jejuni . . Appl Environ Microbiol 75:, 5064–5073. [CrossRef] [PubMed]
    [Google Scholar]
  239. Watanabe T. . ( 1963; ). Infective heredity of multiple drug resistance in bacteria. . Bacteriol Rev 27:, 87–115.[PubMed]
    [Google Scholar]
  240. Williams J. R. , Morgan A. G. , Rouch D. A. , Brown N. L. , Lee B. T. O. . ( 1993; ). Copper-resistant enteric bacteria from United Kingdom and Australian piggeries. . Appl Environ Microbiol 59:, 2531–2537.[PubMed]
    [Google Scholar]
  241. Wilson J. R. , Leang C. , Morby A. P. , Hobman J. L. , Brown N. L. . ( 2000; ). MerF is a mercury transport protein: different structures but a common mechanism for mercuric ion transporters?. FEBS Lett 472:, 78–82. [CrossRef] [PubMed]
    [Google Scholar]
  242. Wireman J. , Liebert C. A. , Smith T. , Summers A. O. . ( 1997; ). Association of mercury resistance with antibiotic resistance in the gram-negative fecal bacteria of primates. . Appl Environ Microbiol 63:, 4494–4503.[PubMed]
    [Google Scholar]
  243. Wise R. , Hart T. , Cars O. , Streulens M. , Helmuth R. , Huovinen P. , Sprenger M. . ( 1998; ). Antimicrobial resistance. Is a major threat to public health. . BMJ 317:, 609–610. [CrossRef] [PubMed]
    [Google Scholar]
  244. Woods E. J. , Cochrane C. A. , Percival S. L. . ( 2009; ). Prevalence of silver resistance genes in bacteria isolated from human and horse wounds. . Vet Microbiol 138:, 325–329. [CrossRef] [PubMed]
    [Google Scholar]
  245. Wright M. S. , Loeffler Peltier G. , Stepanauskas R. , McArthur J. V. . ( 2006; ). Bacterial tolerances to metals and antibiotics in metal-contaminated and reference streams. . FEMS Microbiol Ecol 58:, 293–302. [CrossRef] [PubMed]
    [Google Scholar]
  246. Wright M. S. , Baker-Austin C. , Lindell A. H. , Stepanauskas R. , Stokes H. W. , McArthur J. V. . ( 2008; ). Influence of industrial contamination on mobile genetic elements: class 1 integron abundance and gene cassette structure in aquatic bacterial communities. . ISME J 2:, 417–428. [CrossRef] [PubMed]
    [Google Scholar]
  247. Xu F. F. , Imlay J. A. . ( 2012; ). Silver(I), mercury(II), cadmium(II), and zinc(II) target exposed enzymic iron-sulfur clusters when they toxify Escherichia coli . . Appl Environ Microbiol 78:, 3614–3621. [CrossRef] [PubMed]
    [Google Scholar]
  248. Yang N. , Sun H. . ( 2007; ). Biocoordination chemistry of bismuth: recent advances. . Coord Chem Rev 251:, 2354–2366. [CrossRef]
    [Google Scholar]
  249. Yu D. , Pi B. , Chen Y. , Wang Y. , Ruan Z. , Otto M. , Yu Y. . ( 2014; ). Characterization of the staphylococcal cassette chromosome composite island of Staphylococcus haemolyticus SH32, a methicillin-resistant clinical isolate from China. . PLoS One 9:, e87346. [CrossRef] [PubMed]
    [Google Scholar]
  250. Zhang C. X. , Lippard S. J. . ( 2003; ). New metal complexes as potential therapeutics. . Curr Opin Chem Biol 7:, 481–489. [CrossRef] [PubMed]
    [Google Scholar]
  251. Zimmermann M. , Udagedara S. R. , Sze C. M. , Ryan T. M. , Howlett G. J. , Xiao Z. , Wedd A. G. . ( 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:, 186–197. [CrossRef] [PubMed]
    [Google Scholar]
  252. Zühlsdorf M. T. , Wiedemann B. . ( 1992; ). Tn21-specific structures in gram-negative bacteria from clinical isolates. . Antimicrob Agents Chemother 36:, 1915–1921. [CrossRef] [PubMed]
    [Google Scholar]
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