Antimicrobial activity of metals: Mechanisms, molecular targets and applications

Nature Reviews Microbiology

Volumn 11, Issue 6, 2013, Pages 371-384

  Lemire, Joseph A ^a   Harrison, Joe J ^b   Turner, Raymond J ^a  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIMONY; ARSENIC; CADMIUM; CHROMIUM; COBALT; IRON; LEAD; MANGANESE; METAL; MOLYBDENUM; NANOMATERIAL; NICKEL; PORIN; REACTIVE OXYGEN METABOLITE; SILVER; TRANSITION ELEMENT; TUNGSTEN; VANADIUM; ZINC;

ANTIMICROBIAL ACTIVITY; ATOM; BACTERIAL CELL; BACTERIAL MEMBRANE; BACTERIOSTASIS; BINDING AFFINITY; BORDETELLA BRONCHISEPTICA; CHEMICAL INTERACTION; DRUG MECHANISM; ELECTRON SPIN RESONANCE; ENZYME ACTIVITY; ESCHERICHIA COLI; EUKARYOTE; GENOTOXICITY; GEOBACTER SULFURREDUCENS; HAEMOPHILUS INFLUENZAE; HOMEOSTASIS; INORGANIC CHEMISTRY; LACTOBACILLUS PLANTARUM; LIGAND BINDING; MOLECULAR MIMICRY; MOLECULARLY TARGETED THERAPY; MYCOBACTERIUM MARINUM; NONHUMAN; OXIDATION REDUCTION POTENTIAL; OXIDATIVE STRESS; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; REVIEW; RHODOBACTER CAPSULATUS; SACCHAROMYCES CEREVISIAE; SPECIES DIFFERENTIATION; THERMODYNAMICS;

ANTI-BACTERIAL AGENTS; BACTERIA; HUMANS; METALS; MOLECULAR STRUCTURE;

EID: 84878014208     PISSN: 17401526     EISSN: 17401534     Source Type: Journal    
DOI: 10.1038/nrmicro3028     Document Type: Review

References (171)

1. Waldron, K. J. & Robinson, N. J. How do bacterial cells ensure that metalloproteins get the correct metal? Nature Rev. Microbiol. 7, 25-35 (2009).
2. Andreini, C., Bertini, I. & Rosato, A. A hint to search for metalloproteins in gene banks. Bioinformatics 20, 1373-1380 (2004). (Pubitemid 38931406)
3. Harrison, J. J., Ceri, H., Stremick, C. & Turner, R. J. Biofilm susceptibility to metal toxicity. Environ. Microbiol. 6, 1220-1227 (2004). (Pubitemid 39606292)
4. Nies, D. H. Microbial heavy-metal resistance. Appl. Microbiol. Biotechnol. 51, 730-750 (1999). (Pubitemid 29304744)
5. Afessa, B. et al. Association between a silver-coated endotracheal tube and reduced mortality in patients with ventilator-associated pneumonia. Chest 137, 1015-1021 (2010).
6. Kollef, M. H. et al. Silver-coated endotracheal tubes and incidence of ventilator-associated pneumonia: the NASCENT randomized trial. JAMA 300, 805-813 (2008). A large-scale, multicentre clinical trial showing that patients receiving Ag-coated endotracheal tubes had a significant reduction in the incidence of ventilator-associated pneumonia.
7. Saint, S., Elmore, J. G., Sullivan, S. D., Emerson, S. S. & Koepsell, T. D. The efficacy of silver alloy-coated urinary catheters in preventing urinary tract infection: a meta-analysis. Am. J. Med. 105, 236-241 (1998). (Pubitemid 28443213)
8. Banin, E. et al. The potential of desferrioxamine-gallium as an anti-Pseudomonas therapeutic agent. Proc. Natl Acad. Sci. USA 105, 16761-16766 (2008).
9. Kaneko, Y., Theondel, M., Olakanmi, O., Britigan, B. E. & Singh, P. K. The transition metal gallium disrupts Pseudomonas aeruginosa iron metabolism and has antimicrobial and antibiofilm activity. J. Clin. Invest. 117, 877-888 (2007). A paper describing how Ga interferes with Fe sensing in P. aeruginosa. (Pubitemid 46556744)
10. Harrison, J. J. et al. Copper and quaternary ammonium cations exert synergistic bactericidal and anti-biofilm activity against Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 52, 2870-2881 (2008).
11. Middaugh, J. et al. Aluminum triggers decreased aconitase activity via Fe-S cluster disruption and the overexpression of isocitrate dehydrogenase and isocitrate lyase: a metabolic network mediating cellular survival. J. Biol. Chem. 280, 3159-3165 (2005). (Pubitemid 40223777)
12. Macomber, L., Elsey, S. P. & Hausinger, R. P. Fructose-1, 6-bisphosphate aldolase (class II) is the primary site of nickel toxicity in Escherichia coli. Mol. Microbiol. 82, 1291-1300 (2011). A study that correlates bacteriostasis to Ni-dependent inhibition of a glycolytic enzyme in E. coli.
13. Macomber, L. & Imlay, J. A. The iron-sulfur clusters of dehydratases are primary intracellular targets of copper toxicity. Proc. Natl Acad. Sci. USA 106, 8344-8349 (2009). Work which demonstrates that Cu abolishes the activity of sensitive enzymes with solvent-accessible Fe-S clusters and that this is responsible for growth inhibition of E. coli.
14. Wright, J. B., Lam, K. & Burell, R. E. Wound management in an era of increasing bacterial antibiotic resistance: a role for topical silver treatment. Am. J. Infect. Control 26, 572-577 (1998). (Pubitemid 28565074)
15. Mikolay, A. et al. Survival of bacteria on metallic copper surfaces in a hospital trial. Appl. Microbiol. Biotechnol. 87, 1875-1879 (2010).
16. Haas, K. L. & Franz, K. J. Application of metal coordination chemistry to explore and manipulate cell biology. Chem. Rev. 109, 4921-4960 (2009).
17. Ma, Z., Jacobsen, F. E. & Giedroc, D. P. Coordination chemistry of bacterial metal transport and sensing. Chem. Rev. 109, 4644-4681 (2009).
18. Finney, L. A. & O'Halloran, T. V. Transition metal speciation in the cell: insights from the chemistry of metal ion receptors. Science 300, 931-936 (2003). (Pubitemid 36548870)
19. Irving, H. & Williams, R. J. P. The stability of transition-metal complexes. J. Chem. Soc. 1953, 3192-3210 (1953).
20. Waldron, K. J., Rutherford, J. C., Ford, D. & Robinson, N. J. Metalloproteins and metal sensing. Nature 460, 823-830 (2009).
21. Elias, M. et al. The molecular basis of phosphate discrimination in arsenate-rich environments. Nature 491, 134-137 (2012).
22. Clarkson, T. W. Molecular and ionic mimicry of toxic metals. Annu. Rev. Pharmacol. Toxicol. 33, 545-571 (1993). (Pubitemid 23116018)
23. Jennette, K. W. The role of metals in carcinogenesis: biochemistry and metabolism. Environ. Health Perspect. 40, 233-252 (1981). The first definition of ionic and molecular mimicry in the field of toxicology.
24. Pearson, R. G. Hard and soft acids and bases. J. Am. Chem. Soc. 85, 3533-3539 (1963). A landmark description of the preferences of metal ions for different types of donor ligands.
25. Parr, R. G. & Pearson, R. G. Absolute hardness: companion parameter to absolute electronegativity. J. Am. Chem. Soc. 105, 7512-7516 (1983).
26. Workentine, M. L., Harrison, J. J., Stenroos, P. U., Ceri, H. & Turner, R. J. Pseudomonas fluorescens' view of the periodic table. Environ. Microbiol. 10, 238-250 (2008). A study that establishes statistical correlations between the microbiological toxicity of metal ions and their chemical properties.
27. Nies, D. H. Efflux-mediated heavy metal resistance in prokaryotes. FEMS Microbiol. Rev. 27, 313-339 (2003). (Pubitemid 36700434)
28. Harrison, J. J., Ceri, H. & Turner, R. J. Multimetal resistance and tolerance in microbial biofilms. Nature Rev. Microbiol. 5, 928-938 (2007). (Pubitemid 350131181)
29. Stewart, E. J., Aslund, F. & Beckwith, J. Disulfide bond formation in the Escherichia coli cytoplasm: an in vivo role reversal for the thioredoxins. EMBO J. 17, 5543-5550 (1998). (Pubitemid 28445966)
30. Gadd, G. M. Metals, minerals and microbes: geomicrobiology and bioremediation. Microbiology 156, 609-643 (2010).
31. Cornelis, G., Johnson, C. A., Gerven, T. V. & Vandecasteele, C. Leaching mechanisms of oxyanionic metalloid and metal species in alkaline solid wastes: a review. Appl. Geochem. 23, 955-976 (2008).
32. Allen, H. E., Hall, R. H. & Brisbin, T. D. Metal speciation: effects on aquatic toxicity. Environ. Sci. Technol. 14, 441-443 (1980). (Pubitemid 10079366)
33. Allen, H. E. & Hansen, D. J. The importance of trace metal speciation to water quality criteria. Water Environ. Res. 68, 42-54 (1996). (Pubitemid 26030867)
34. Saier, M. H. Jr, Tran, C. V. & Barabote, R. D. TCDB: the Transporter Classification Database for membrane transport protein analyses and information. Nucleic Acids Res. 34, D181-D186 (2006).
35. Schue, M., Dover, L. G., Besra, G. S., Parkhill, J. & Brown, N. L. Sequence and analysis of a plasmid-encoded mercury resistance operon from Mycobacterium marinum identifies MerH, a new mercuric ion transporter. J. Bacteriol. 191, 439-444 (2009).
36. Barkay, T., Miller, S. M. & Summers, A. O. Bacterial mercury resistance from atoms to ecosystems. FEMS Microbiol. Rev. 27, 355-384 (2003). (Pubitemid 36700435)
37. Lopez, M. L., Garcia-Gimenez, E., Aguilella, V. M. & Alcaraz, A. Critical assessment of OmpF channel selectivity: merging information from different experimental protocols. J. Phys. Condens. Matter 22, 454106 (2010).
38. Hohle, T. H., Franck, W. L., Stacey, G. & O'Brian, M. R. Bacterial outer membrane channel for divalent metal ion acquisition. Proc. Natl Acad. Sci. USA 108, 15390-15395 (2011).
39. Makui, H. et al. Identification of the Escherichia coli K-12 Nramp orthologue (MntH) as a selective divalent metal ion transporter. Mol. Microbiol. 35, 1065-1078 (2000). (Pubitemid 30137776)
40. Feng, Q. L. et al. A mechanistic study of the antibacterial effect of silver ions on Escherichia coli and Staphylococcus aureus. J. Biomed. Mater. Res. 52, 662-668 (2000).
41. Cohen, A., Nelson, H. & Nelson, N. The family of SMF metal ion transporters in yeast cells. J. Biol. Chem. 275, 33388-33394 (2000).
42. Grass, G. et al. The metal permease ZupT from Escherichia coli is a transporter with a broad substrate spectrum. J. Bacteriol. 187, 1604-1611 (2005). (Pubitemid 40289360)
43. Lin, W., Chai, J., Love, J. & Fu, D. Selective electrodiffusion of zinc ions in a Zrt-, Irt-like protein, ZIPB. J. Biol. Chem. 285, 39013-39020 (2010).
44. Anderson, D. S., Adhikari, P., Nowalk, A. J., Chen, C. Y. & Mietzner, T. A. The hFbpABC transporter from Haemophilus influenzae functions as a binding-protein-dependent ABC transporter with high specificity and affinity for ferric iron. J. Bacteriol. 186, 6220-6229 (2004). (Pubitemid 39187010)
45. Hao, Z., Chen, S. & Wilson, D. B. Cloning, expression, and characterization of cadmium and manganese uptake genes from Lactobacillus plantarum. Appl. Environ. Microbiol. 65, 4746-4752 (1999).
46. Sanders, O. I., Rensing, C., Kuroda, M., Mitra, B. & Rosen, B. P. Antimonite is accumulated by the glycerol facilitator GlpF in Escherichia coli. J. Bacteriol. 179, 3365-3367 (1997). (Pubitemid 27203017)
47. Meng, Y. L., Liu, Z. & Rosen, B. P. As(iii) and Sb(iii) uptake by GlpF and efflux by ArsB in Escherichia coli. J. Biol. Chem. 279, 18334-18341 (2004). (Pubitemid 38623248)
48. Wysocki, R. et al. The glycerol channel Fps1p mediates the uptake of arsenite and antimonite in Saccharomyces cerevisiae. Mol. Microbiol. 40, 1391-1401 (2001). (Pubitemid 32635307)
49. Pereira, Y. et al. Chromate causes sulfur starvation in yeast. Toxicol. Sci. 106, 400-412 (2008).
50. Borghese, R. & Zannoni, D. Acetate permease (ActP) Is responsible for tellurite (TeO32-) uptake and resistance in cells of the facultative phototroph Rhodobacter capsulatus. Appl. Environ. Microbiol. 76, 942-944 (2010).
51. Elias, A. O. et al. Tellurite enters Escherichia coli mainly through the PitA phosphate transporter. Microbiologyopen 1, 259-267 (2012).
52. Willsky, G. R. & Malamy, M. H. Effect of arsenate on inorganic phosphate transport in Escherichia coli. J. Bacteriol. 144, 366-374 (1980). (Pubitemid 11211057)
53. Hussein, S., Hantke, K. & Braun, V. Citrate-dependent iron transport system in Escherichia coli K-12. Eur. J. Biochem. 117, 431-437 (1981). (Pubitemid 11055393)
54. Jensen, L. T., Ajua-Alemanji, M. & Culotta, V. C. The Saccharomyces cerevisiae high affinity phosphate transporter encoded by PHO84 also functions in manganese homeostasis. J. Biol. Chem. 278, 42036-42040 (2003). (Pubitemid 37310468)
55. Beard, S. J. et al. Evidence for the transport of zinc(ii) ions via the pit inorganic phosphate transport system in Escherichia coli. FEMS Microbiol. Lett. 184, 231-235 (2000). (Pubitemid 30125345)
56. Schaefer, J. K. & Morel, F. M. M. High methylation rates of mercury bound to cysteine by Geobacter sulfurreducens. Nature Geosci. 2, 123-126 (2009).
57. Bellenger, J. P., Wichard, T., Kustka, A. B. & Kraepiel, A. M. L. Uptake of molybdenum and vanadium by a nitrogen-fixing soil bacterium using siderophores. Nature Geosci. 1, 243-246 (2008).
58. Schalk, I. J., Hannauer, M. & Braud, A. New roles for bacterial siderophores in metal transport and tolerance. Environ. Microbiol. 13, 2844-2854 (2011).
59. Braud, A., Hannauer, M., Mislin, G. L. & Schalk, I. J. The Pseudomonas aeruginosa pyochelin-iron uptake pathway and its metal specificity. J. Bacteriol. 191, 3517-3525 (2009).
60. Hannauer, M. et al. The PvdRT-OpmQ efflux pump controls the metal selectivity of the iron uptake pathway mediated by the siderophore pyoverdine in Pseudomonas aeruginosa. Environ. Microbiol. 14, 1696-1708 (2012).
61. Braud, A., Hoegy, F., Jezequel, K., Lebeau, T. & Schalk, I. J. New insights into the metal specificity of the Pseudomonas aeruginosa pyoverdine-iron uptake pathway. Environ. Microbiol. 11, 1079-1091 (2009).
62. Imlay, J. A., Chin, S. M. & Linn, S. Toxic DNA damage by hydrogen peroxide through the Fenton reaction in vivo and in vitro. Science 240, 640-642 (1988).
63. Macomber, L., Rensing, C. & Imlay, J. A. Intracellular copper does not catalyze the formation of oxidative DNA damage in Escherichia coli. J. Bacteriol. 189, 1616-1626 (2007). Research demonstrating that Cu catalyses the formation of the hydroxyl radical in vivo and suggests that this chemistry is localized to the periplasmic space of E. coli. (Pubitemid 46446123)
64. Harrison, J. J. et al. Chromosomal antioxidant genes have metal ion-specifc roles as determinants of bacterial metal tolerance. Environ. Microbiol. 11, 2491-2509 (2009).
65. Perez, J. M. et al. Bacterial toxicity of potassium tellurite: unveiling an ancient enigma. PLoS ONE 2, e211 (2007).
66. Nunoshiba, T. et al. Role of iron and superoxide for generation of hydroxyl radical, oxidative DNA lesions, and mutagenesis in Escherichia coli. J. Biol. Chem. 274, 34832-34837 (1999). (Pubitemid 129509528)
67. Touati, D., Jacques, M., Tardat, B., Bouchard, L. & Despied, S. Lethal oxidative damage and mutagenesis are generated by iron in Δfur mutants of Escherichia coli: protective role of superoxide dismutase. J. Bacteriol. 177, 2305-2314 (1995). A report that links Fe toxicity to lethal DNA damage in E. coli.
68. Warnes, S. L. & Keevil, C. W. Mechanism of copper surface toxicity in vancomycin-resistant enterococci following wet or dry surface contact. Appl. Environ. Microbiol. 77, 6049-6059 (2011).
69. Warnes, S. L., Caves, V. & Keevil, C. W. Mechanism of copper surface toxicity in Escherichia coli O157:H7 and Salmonella involves immediate membrane depolarization followed by slower rate of DNA destruction which differs from that observed for Gram-positive bacteria. Environ. Microbiol. 14, 1730-1743 (2012).
70. Imlay, J. A. Pathways of oxidative damage. Annu. Rev. Microbiol. 57, 395-418 (2003). The definitive review of O toxicity in bacteria. (Pubitemid 37392949)
71. Itoh, M. et al. Mechanism of chromium(vi) toxicity in Escherichia coli: is hydrogen peroxide essential in Cr(vi) toxicity? J. Biochem. 117, 780-786 (1995).
72. Geslin, C., Llanos, J., Prieur, D. & Jeanthon, C. The manganese and iron superoxide dismutases protect Escherichia coli from heavy metal toxicity. Res. Microbiol. 152, 901-905 (2001). (Pubitemid 33043834)
73. Parvatiyar, K. et al. Global analysis of cellular factors and responses involved in Pseudomonas aeruginosa resistance to arsenite. J. Bacteriol. 187, 4853-4864 (2005). (Pubitemid 40962202)
74. Sumner, E. R. et al. Oxidative protein damage causes chromium toxicity in yeast. Microbiology 151, 1939-1948 (2005). (Pubitemid 40909036)
75. Calderon, I. L. et al. Tellurite-mediated disabling of [4Fe-4S] clusters of Escherichia coli dehydratases. Microbiology 155, 1840-1846 (2009).
76. Teitzel, G. M. et al. Survival and growth in the presence of elevated copper: transcriptional profiling of copper-stressed Pseudomonas aeruginosa. J. Bacteriol. 188, 7242-7256 (2006). (Pubitemid 44547629)
77. Jin, Y. H. et al. Global transcriptome and deletome profiles of yeast exposed to transition metals. PLoS Genet. 4, e1000053 (2008).
78. Valko, M., Morris, H. & Cronin, M. T. D. Metals, toxicity and oxidative stress. Curr. Med. Chem. 12, 1161-1208 (2005). A comprehensive summary of in vitro metal chemistry and its relationship to toxicology.
79. Stohs, S. J. & Bagchi, D. Oxidative mechanisms in the toxicity of metal ions. Free Radic. Biol. Med. 18, 321-336 (1995).
80. Faulkner, M. J. & Helmann, J. D. Peroxide stress elicits adaptive changes in bacterial metal ion homeostasis. Antioxid. Redox Signal. 15, 175-189 (2011).
81. Strlič, M., Kolar, J., Šelih, V.-S., Kočar, D. & Pihlar, B. A comparative study of several transition metals in Fenton-like reaction systems at circum-neutral pH. Acta Chim. Slov. 50, 619-632 (2003). (Pubitemid 38142655)
82. Barnese, K., Gralla, E. B., Valentine, J. S. & Cabelli, D. E. Biologically relevant mechanism for catalytic superoxide removal by simple manganese compounds. Proc. Natl Acad. Sci. USA 109, 6892-6897 (2012).
83. Anjem, A. & Imlay, J. A. Mononuclear iron enzymes are primary targets of hydrogen peroxide stress. J. Biol. Chem. 287, 15544-15556 (2012).
84. Anjem, A., Varghese, S. & Imlay, J. A. Manganese import is a key element of the OxyR response to hydrogen peroxide in Escherichia coli. Mol. Microbiol. 72, 844-858 (2009).
85. Xu, F. F. & Imlay, J. A. 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 (2012). Work which demonstrates that soft metals may be toxic because they destroy the Fe-S clusters of dehydratases in E. coli.
86. Outten, C. E. & O'Halloran, T. V. Femtomolar sensitivity of metalloregulatory proteins controlling zinc homeostasis. Science 292, 2488-2492 (2001). (Pubitemid 32605687)
87. Keyer, K. & Imlay, J. A. Superoxide accelerates DNA damage by elevating free-iron levels. Proc. Natl Acad. Sci. USA 93, 13635-13640 (1996). (Pubitemid 26424171)
88. Xu, H. et al. Role of reactive oxygen species in the antibacterial mechanism of silver nanoparticles on Escherichia coli O157:H7. Biometals 25, 45-53 (2012).
89. Park, H. J. et al. Silver-ion-mediated reactive oxygen species generation affecting bactericidal activity. Water Res. 43, 1027-1032 (2009).
90. Gordon, O. et al. 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 (2010).
91. Stojiljkovic, I., Kumar, V. & Srinivasan, N. Non-iron metalloporphyrins: potent antibacterial compounds that exploit haem/Hb uptake systems of pathogenic bacteria. Mol. Microbiol. 31, 429-442 (1999). (Pubitemid 29046086)
92. Valko, M., Rhodes, C. J., Moncol, J., Izakovic, M. & Mazur, M. Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chem. Biol. Interact. 160, 1-40 (2006). (Pubitemid 43227479)
93. Helbig, K., Grosse, C. & Nies, D. H. Cadmium toxicity in glutathione mutants of Escherichia coli. J. Bacteriol. 190, 5439-5454 (2008).
94. Helbig, K., Bleuel, C., Krauss, G. J. & Nies, D. H. Glutathione and transition-metal homeostasis in Escherichia coli. J. Bacteriol. 190, 5431-5438 (2008).
95. 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 antibacterial action of silver ions. Lett. Appl. Microbiol. 25, 279-283 (1997). (Pubitemid 27438351)
96. Fauchon, M. et al. Sulfur sparing in the yeast proteome in response to sulfur demand. Mol. Cell 9, 713-723 (2002). A study that identifies the S-sparing response in S. cerevisiae as a mechanism to cope with Cd toxicity. (Pubitemid 34454884)
97. Stadtman, E. R. & Levine, R. L. Free radical-mediated oxidation of free amino acids and amino acid residues in proteins. Amino Acids 25, 207-218 (2003). (Pubitemid 38043943)
98. Stadtman, E. R. Oxidation of free amino acids and amino acid residues in proteins by radiolysis and by metal-catalyzed reactions. Annu. Rev. Biochem. 62, 797-821 (1993). (Pubitemid 23237888)
99. Erskine, P. T. et al. X-ray structure of 5-aminolaevulinate dehydratase, a hybrid aldolase. Nature Struct. Biol. 4, 1025-1031 (1997). A paper that defines the structural basis for the replacement of Zn by Pb at the active site of ALAD. (Pubitemid 27525807)
100. Ogunseitan, O. A., Yang, S. & Ericson, J. Microbial δ-aminolevulinate dehydratase as a biosensor of lead bioavailability in contaminated environments. Soil Biol. Biochem. 32, 1899-1906 (2000). (Pubitemid 32053284)
101. Ciriolo, M. R. et al. Purification and characterization of Ag, Zn-superoxide dismutase from Saccharomyces cerevisiae exposed to silver. J. Biol. Chem. 269, 25783-25787 (1994). (Pubitemid 24336277)
102. Zhang, Y. M. & Rock, C. O. Membrane lipid homeostasis in bacteria. Nature Rev. Microbiol. 6, 222-233 (2008). (Pubitemid 351256317)
103. Li, W. R. et al. Antibacterial activity and mechanism of silver nanoparticles on Escherichia coli. Appl. Microbiol. Biotechnol. 85, 1115-1122 (2010).
104. Jung, W. K. et al. Antibacterial activity and mechanism of action of the silver ion in Staphylococcus aureus and Escherichia coli. Appl. Environ. Microbiol. 74, 2171-2178 (2008).
105. Yamanaka, M., Hara, K. & Kudo, J. Bactericidal actions of a silver ion solution on Escherichia coli, studied by energy-filtering transmission electron microscopy and proteomic analysis. Appl. Environ. Microbiol. 71, 7589-7593 (2005). (Pubitemid 43194262)
106. Yaganza, E. S., Rioux, D., Simard, M., Arul, J. & Tweddell, R. J. Ultrastructural alterations of Erwinia carotovora subsp. atroseptica caused by treatment with aluminum chloride and sodium metabisulfite. Appl. Environ. Microbiol. 70, 6800-6808 (2004). (Pubitemid 39518592)
107. Lok, C. N. et al. Proteomic analysis of the mode of antibacterial action of silver nanoparticles. J. Proteome Res. 5, 916-924 (2006).
108. Bragg, P. D. & Rainnie, D. J. The effect of silver ions on the respiratory chain of Escherichia coli. Can. J. Microbiol. 20, 883-889 (1974).
109. Fadeeva, M. S., Bertsova, Y. V., Euro, L. & Bogachev, A. V. Cys377 residue in NqrF subunit confers Ag+ sensitivity of Na+-translocating NADH:quinone oxidoreductase from Vibrio harveyi. Biochemistry 76, 186-195 (2011).
110. Dibrov, P., Dzioba, J., Gosink, K. K. & Hase, C. C. Chemiosmotic mechanism of antimicrobial activity of Ag+ in Vibrio cholerae. Antimicrob. Agents Chemother. 46, 2668-2670 (2002). Evidence that Ag cations induce massive leakage of protons through membranes. (Pubitemid 34793484)
111. Hong, R., Kang, T. Y., Michels, C. A. & Gadura, N. Membrane lipid peroxidation in copper alloy-mediated contact killing of Escherichia coli. Appl. Environ. Microbiol. 78, 1776-1784 (2012).
112. Howlett, N. G. & Avery, S. V. Induction of lipid peroxidation during heavy metal stress in Saccharomyces cerevisiae and influence of plasma membrane fatty acid unsaturation. Appl. Environ. Microbiol. 63, 2971-2976 (1997). (Pubitemid 27337781)
113. Grass, G., Rensing, C. & Solioz, M. Metallic copper as an antimicrobial surface. Appl. Environ. Microbiol. 77, 1541-1547 (2011).
114. Janero, D. R. Malondialdehyde and thiobarbituric acid-reactivity as diagnostic indices of lipid peroxidation and peroxidative tissue injury. Free Radic. Biol. Med. 9, 515-540 (1990). (Pubitemid 120036914)
115. Linley, E., Denyer, S. P., McDonnell, G., Simons, C. & Maillard, J. Y. Use of hydrogen peroxide as a biocide: new consideration of its mechanisms of biocidal action. J. Antimicrob. Chemother. 67, 1589-1596 (2012).
116. Nishioka, H. Mutagenic activities of metal compounds in bacteria. Mutat. Res. 31, 185-189 (1975).
117. Green, M. H., Muriel, W. J. & Bridges, B. A. Use of a simplified fluctuation test to detect low levels of mutagens. Mutat. Res. 38, 33-42 (1976).
118. Wong, P. K. Mutagenicity of heavy metals. Bull. Environ. Contam. Toxicol. 40, 597-603 (1988).
119. Asakura, K. et al. Genotoxicity studies of heavy metals: lead, bismuth, indium, silver and antimony. J. Occup. Health 51, 498-512 (2009).
120. Rogers, H. J., Woods, V. E. & Synge, C. Antibacterial effect of the scandium and indium complexes of enterochelin on Escherichia coli. J. Gen. Microbiol. 128, 2389-2394 (1982). (Pubitemid 13205102)
121. Olakanmi, O. et al. Gallium disrupts iron uptake by intracellular and extracellular Francisella strains and exhibits therapeutic efficacy in a murine pulmonary infection model. Antimicrob. Agents Chemother. 54, 244-253 (2010).
122. Malfertheiner, P. et al. Helicobacter pylori eradication with a capsule containing bismuth subcitrate potassium, metronidazole, and tetracycline given with omeprazole versus clarithromycin-based triple therapy: a randomised, open-label, non-inferiority, Phase 3 trial. Lancet 377, 905-913 (2011).
123. Andrews, P. C. et al. Remarkable in vitro bactericidal activity of bismuth(iii) sulfonates against Helicobacter pylori. Dalton Trans. 41, 11798-11806 (2012).
124. Stout, J. E. & Yu, V. L. Experiences of the first 16 hospitals using copper-silver ionization for Legionella control: implications for the evaluation of other disinfection modalities. Infect. Control Hosp. Epidemiol. 24, 563-568 (2003). The results of field testing suggesting that the use of Cu-Ag ionization systems can eliminate hospital outbreaks of Legionnaires' disease. (Pubitemid 37039612)
125. Rai, M., Yadav, A. & Gade, A. Silver nanoparticles as a new generation of antimicrobials. Biotechnol. Adv. 27, 76-83 (2009).
126. Sharma, V. K., Yngard, R. A. & Lin, Y. Silver nanoparticles: green synthesis and their antimicrobial activities. Adv. Colloid Interface Sci. 145, 83-96 (2009).
127. Sondi, I. & Salopek-Sondi, B. Silver nanoparticles as antimicrobial agent: a case study on E. coli as a model for Gram-negative bacteria. J. Colloid Interface Sci. 275, 177-182 (2004). (Pubitemid 38670216)
128. Stoimenov, P. K., Klinger, R. L., Marchin, G. L. & Klabunde, K. J. Metal oxide nanoparticles as bactericidal agents. Langmuir 18, 6679-6686 (2002). (Pubitemid 35383306)
129. Ruparelia, J. P., Chatterjee, A. K., Duttagupta, S. P. & Mukherji, S. Strain specificity in antimicrobial activity of silver and copper nanoparticles. Acta Biomater. 4, 707-716 (2008). (Pubitemid 351461288)
130. Bandyopadhyay, S., Peralta-Videa, J. R., Plascencia- Villa, G., Jose-Yacaman, M. & Gardea-Torresdey, J. L. Comparative toxicity assessment of CeO2 and ZnO nanoparticles towards Sinorhizobium meliloti, a symbiotic alfalfa associated bacterium: use of advanced microscopic and spectroscopic techniques. J. Hazard. Mater. 241-242, 379-386 (2012).
131. Luef, B. et al. Iron-reducing bacteria accumulate ferric oxyhydroxide nanoparticle aggregates that may support planktonic growth. ISME J. 7, 338-350 (2012).
132. Morones, J. R. et al. The bactericidal effect of silver nanoparticles. Nanotechnology 16, 2346-2353 (2005). (Pubitemid 41376178)
133. 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. Appl. Environ. Microbiol. 73, 1712-1720 (2007). (Pubitemid 46449051)
134. El Badawy, A. M. et al. Surface charge-dependent toxicity of silver nanoparticles. Environ. Sci. Technol. 45, 283-287 (2011).
135. Gunawan, C., Teoh, W. Y., Marquis, C. P. & Amal, R. Cytotoxic origin of copper(ii) oxide nanoparticles: comparative studies with micron-sized particles, leachate, and metal salts. ACS Nano 5, 7214-7225 (2011).
136. Applerot, G. et al. Understanding the antibacterial mechanism of CuO nanoparticles: revealing the route of induced oxidative stress. Small 8, 3326-3337 (2012).
137. Sotiriou, G. A. & Pratsinis, S. E. Antibacterial activity of nanosilver ions and particles. Environ. Sci. Technol. 44, 5649-5654 (2010).
138. Xiu, Z. M., Zhang, Q. B., Puppala, H. L., Colvin, V. L. & Alvarez, P. J. Negligible particle-specific antibacterial activity of silver nanoparticles. Nano Lett. 12, 4271-4275 (2012). The demonstration that metal nanoparticles that cannot become ionized are non-toxic to bacteria.
139. Highsmith, J. Nanoparticles in biotechnology, drug development and drug delivery. Report No. BIO113A (BCC Research: Market Forecasting, 2012).
140. Wilks, S. A., Michels, H. & Keevil, C. W. The survival of Escherichia coli O157 on a range of metal surfaces. Int. J. Food Microbiol. 105, 445-454 (2005). (Pubitemid 41728897)
141. Quaranta, D. et al. Mechanisms of contact-mediated killing of yeast cells on dry metallic copper surfaces. Appl. Environ. Microbiol. 77, 416-426 (2011).
142. Espirito Santo, C. et al. Bacterial killing by dry metallic copper surfaces. Appl. Environ. Microbiol. 77, 794-802 (2011).
143. Warnes, S. L., Highmore, C. J. & Keevil, C. W. Horizontal transfer of antibiotic resistance genes on abiotic touch surfaces: implications for public health. mBio 3, e00489-12 (2012).
144. Hoffman, L. R. & Ramsey, B. W. Cystic fibrosis therapeutics: the road ahead. Chest 143, 207-213 (2013).
145. Gans, J., Wolinsky, M. & Dunbar, J. Computational improvements reveal great bacterial diversity and high metal toxicity in soil. Science 309, 1387-1390 (2005). (Pubitemid 41209368)
146. Alexander, J. W. History of the medical use of silver. Surg. Infect. 10, 289-292 (2009).
147. Borkow, G. & Gabbay, J. Copper, an ancient remedy returning to fight microbial, fungal and viral infections. Curr. Chem. Biol. 3, 272-278 (2009).
148. Ayres, P. G. Alexis Millardet: France's forgotten mycologist. Mycologist 18, 23-26 (2004).
149. Dixon, B. Pushing Bordeaux mixture. Lancet Infect. Dis. 4, 594 (2004).
150. Sims, J. M. On the treatment of vesicovaginal fistula. Am. J. Med. Sci. 45, 59-82 (1852).
151. Crede, C. S. F. Die verhütung der augenentzündung der neugeborenen. Arch. Gynakol. 17, 50-53 (1881) (in German).
152. Silver, S., Phung le, T. & Silver, G. Silver as biocides in burn and wound dressings and bacterial resistance to silver compounds. J. Ind. Microbiol. Biotechnol. 33, 627-634 (2006). (Pubitemid 43876124)
153. Pereira, J. Materia medica, or pharmacology, and general therapeutics. Lond. Med. Gaz. 18, 305-314 (1836).
154. Frazer, A. D. & Edin, M. B. Tellurium in the treatment of syphillis. Lancet 216, 133-134 (1930).
155. Keyes, E. L. The treatment of gonorrhea of the male urethra. JAMA 75, 1325-1329 (1920).
156. Hodges, N. D. C. The value of mercuric chloride as a disinfectant. Science 13, 62-64 (1889).
157. Ehrlich, P. & Bertheim, A. Über das salzsaure 3. 3'-Diamino-4. 4' -dioxy-arsenobenzol und seine nächsten Verwandten. Ber. Dtsch. Chem. Ges. 45, 756-766 (1912) (in German).
158. Changela, A. et al. Molecular basis of metal-ion selectivity and zeptomolar sensitivity by CueR. Science 301, 1383-1387 (2003). (Pubitemid 37075815)
159. Silver, S. & Phung, L. T. Bacterial heavy metal resistance: new surprises. Annu. Rev. Microbiol. 50, 753-789 (1996). (Pubitemid 26337481)
160. Dimkpa, C. O. et al. Involvement of siderophores in the reduction of metal-induced inhibition of auxin synthesis in Streptomyces spp. Chemosphere 74, 19-25 (2008).
161. Chaturvedi, K. S., Hung, C. S., Crowley, J. R., Stapleton, A. E. & Henderson, J. P. The siderophore yersiniabactin binds copper to protect pathogens during infection. Nature Chem. Biol. 8, 731-736 (2012).
162. Johnston, C. W. et al. Gold biomineralization by a metallophore from a gold-associated microbe. Nature Chem. Biol. 9, 241-243 (2013).
163. Mullen, M. D. et al. Bacterial sorption of heavy metals. Appl. Environ. Microbiol. 55, 3143-3149 (1989). (Pubitemid 20002126)
164. Langley, S. & Beveridge, T. J. Effect of O-side-chain- lipopolysaccharide chemistry on metal binding. Appl. Environ. Microbiol. 65, 489-498 (1999). (Pubitemid 29075088)
165. Zannoni, D., Borsetti, F., Harrison, J. J. & Turner, R. J. The bacterial response to the chalcogen metalloids Se and Te. Adv. Microb. Physiol. 53, 1-71 (2008).
166. Carrondo, M. A. Ferritins, iron uptake and storage from the bacterioferritin viewpoint. EMBO J. 22, 1959-1968 (2003). (Pubitemid 36565522)
167. Lemire, J., Mailloux, R., Auger, C., Whalen, D. & Appanna, V. D. Pseudomonas fluorescens orchestrates a fine metabolic-balancing act to counter aluminum toxicity. Environ. Microbiol. 12, 1384-1390 (2010).
168. Zhou, Y., Kong, Y., Kundu, S., Cirillo, J. D. & Liang, H. Antibacterial activities of gold and silver nanoparticles against Escherichia coli and bacillus Calmette-Guérin. J. Nanobiotechnology 10, 19 (2012).
169. Yu, D. & Yam, V. W. Hydrothermal-induced assembly of colloidal silver spheres into various nanoparticles on the basis of HTAB-modified silver mirror reaction. J. Phys. Chem. B 109, 5497-5503 (2005). (Pubitemid 40519448)
170. Sun, Y. & Xia, Y. Shape-controlled synthesis of gold and silver nanoparticles. Science 298, 2176-2179 (2002). (Pubitemid 35471239)
171. Saier, M. H. Jr. A functional-phylogenetic classification system for transmembrane solute transporters. Microbiol. Mol. Biol. Rev. 64, 354-411 (2000). (Pubitemid 30412678)