Chapter 5 : Resistance to Metals Used in Agricultural Production

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Metal compounds are widely used in livestock production because they are necessary supplements and play a very important role as essential trace elements that are part of the nutritional requirements of most animal species. However, copper and zinc compounds are also added to feed in larger concentrations for achieving additional beneficial effects. Therefore, we will focus this chapter on copper and zinc; their use and indications; the concerns related to the selection of resistance, toxicity, and environmental pollution and policies; and the alternatives and new developments regarding their use. Compounds derived from the nonessential metal arsenic, such as roxarsone, which have been used in livestock for feed supplementation in some countries around the world, will not be discussed in great detail in this chapter.

Citation: Rensing C, Moodley A, Cavaco L, McDevitt S. 2018. Resistance to Metals Used in Agricultural Production, p 83-107. In Schwarz S, Cavaco L, Shen J (ed), Antimicrobial Resistance in Bacteria from Livestock and Companion Animals. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.ARBA-0025-2017
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Figure 1

Copper fitness (or pathogenicity) island in . Genes and protein products of the enterobacterial copper fitness island composed of the - and -determinants. The genes, including their transcriptional/translational direction, are indicated below the illustration of the proposed or experimentally determined function of the proteins encoded by the system. Refer to text for details. (Reprinted with permission [ ].)

Citation: Rensing C, Moodley A, Cavaco L, McDevitt S. 2018. Resistance to Metals Used in Agricultural Production, p 83-107. In Schwarz S, Cavaco L, Shen J (ed), Antimicrobial Resistance in Bacteria from Livestock and Companion Animals. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.ARBA-0025-2017
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Image of Figure 2
Figure 2

Copper fitness island in . Genes and proposed protein products of the copper island in HF50105 (GenBank accession number AITS01000024). The genes, including their transcriptional/translational direction, are indicated below the illustration of the proposed function of the proteins. (Refer to text for details.) Adjacent to and separating the genes involved in copper resistance are genes encoding prolipoprotein diacylglyceryl transferase (A), integral membrane protein (B), predicted metal-binding protein/chaperone (C), hypothetical protein (H), transposase (T), and disrupted P-type ATPase (F) that have been identified. (Reprinted with permission [ ].)

Citation: Rensing C, Moodley A, Cavaco L, McDevitt S. 2018. Resistance to Metals Used in Agricultural Production, p 83-107. In Schwarz S, Cavaco L, Shen J (ed), Antimicrobial Resistance in Bacteria from Livestock and Companion Animals. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.ARBA-0025-2017
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1. Suttle NF . 2010. Mineral Nutrition of Livestock, 4th ed. CABI Publishing, Wallingford, United Kingdom. p 283 342.
2. European Commission Scientific Committee for Animal Nutrition (SCAN) . 2003. Opinion of the Scientific Committee for Animal Nutrition on the use of copper in feedingstuffs.
3. European Commission . 2003. Commission Regulation (EC) no 1334/2003 of 25 July 2003. Amending the conditions for authorisation of a number of additives in feedingstuffs belonging to the group of trace elements.
4. EFSA Panel on Additives and Products or Substances used in Animal Feed (FEEDAP) . 2016. Revision of the currently authorised maximum copper content in complete feed. EFSA J 14 : e04563.[CrossRef]
5. European Medicines Agency (EMA), Committee for Veterinary Medicinal Products (CVMP) . 1998. Copper chloride, copper gluconate, copper heptanoate, copper oxide, copper methionate, copper sulfate and dicopper oxide: Summary Report. EMEA/MRL/431/98-FINAL.
6. Todd WR,, Elvehjem CA,, Hart EB . 1980. Nutrition classics. The American Journal of Physiology. Volume 107, 1934, pages 146–156. “Zinc in the nutrition of the rat” by W.R. Todd, C.A. Elvehjem and E.B. Hart. Nutr Rev 38 : 151 154.[CrossRef]
7. Tucker HF,, Salmon WD . 1955. Parakeratosis or zinc deficiency disease in the pig. Proc Soc Exp Biol Med 88 : 613 616.[CrossRef][PubMed]
8. O’Dell BL,, Newberne PM,, Savage JE . 1958. Significance of dietary zinc for the growing chicken. J Nutr 65 : 503 518.[CrossRef][PubMed]
9. Chesters JK . 1983. Zinc metabolism in animals: pathology, immunology and genetics. J Inherit Metab Dis 6( Suppl 1) : 34 38.[CrossRef][PubMed]
10. Jezyk PF,, Haskins ME,, MacKay-Smith WE,, Patterson DF . 1986. Lethal acrodermatitis in bull terriers. J Am Vet Med Assoc 188 : 833 839.[PubMed]
11. Hambidge KM,, Casey CE,, Krebs NF, . 1986. Zinc, p 1 137. In Mertz W (ed), Trace Elements in Human and Animal Nutrition, vol 2. Academic Press, San Diego, CA.[CrossRef]
12. European Commission’s Scientific Committee for Animal Nutrition (SCAN) . 2003. Opinion of the Scientific Committee for Animal Nutrition on the use of zinc in feedingstuffs.
13. EFSA Panel on Additives and Products or Substances Used in Animal Feed (FEEDAP) . 2014. Scientific Opinion on the potential reduction of the currently authorised maximum zinc content in complete feed. EFSA J 12 : 3668.[CrossRef]
14. European Medicines Agency (EMA) . 2016. Committee for Medicinal Products for Veterinary Use (CVMP) meeting 6–8 December 2016. http://www.ema.europa.eu/ema/index.jsp?curl=pages/news_and_events/events/2015/09/event_detail_001206.jsp&mid=WC0b01ac058004d5c3
15. DANMAP . 2014. Use of Antimicrobial Agents and Occurrence of Antimicrobial Resistance in Bacteria from Food Animals, Food and Humans in Denmark. DANMAP, Copenhagen, Denmark.
16. BelVetSAC . 2015. Belgian Veterinary Surveillance of Antibacterial Consumption National consumption report.
17. BelVetSAC . 2014. Belgian Veterinary Surveillance of Antibacterial Consumption National consumption report.
18. Slifierz M . 2016. The effects of zinc therapy on the co-selection of methicillin-resistance in livestock-associated Staphylococcus aureus and the bacterial ecology of the porcine microbiota. PhD thesis. University of Guelph, Guelph, Canada.
19. Jacela JY,, DeRouchey JM,, Tokach MD,, Goodband RD,, Nelssen JL,, Renter DG,, Dritz SS . 2010. Feed additives for swine: fact sheets–high dietary levels of copper and zinc for young pigs, and phytase. J Swine Health Prod 18 : 87 91.
20. Poulsen HD . 1995. Zinc oxide for weanling piglets. Acta Agriculturae Scandinavica 45 : 159 167.
21. European Food Safety Authority . 2014. Dietary exposure to inorganic arsenic. EFSA J 12 : 3597.[CrossRef]
22. Antman KH . 2001. Introduction: the history of arsenic trioxide in cancer therapy. Oncologist 6( Suppl 2) : 1 2.[CrossRef][PubMed]
23. Smith AH,, Marshall G,, Yuan Y,, Steinmaus C,, Liaw J,, Smith MT,, Wood L,, Heirich M,, Fritzemeier RM,, Pegram MD,, Ferreccio C . 2014. Rapid reduction in breast cancer mortality with inorganic arsenic in drinking water. EBioMedicine 1 : 58 63.[CrossRef][PubMed]
24. Nigra AE,, Nachman KE,, Love DC,, Grau-Perez M,, Navas-Acien A . 2017. Poultry consumption and arsenic exposure in the U.S. population. Environ Health Perspect 125 : 370 377.[PubMed]
25. Caldas D,, Pestana IA,, Almeida MG,, Henry FC,, Salomão MSMB,, de Souza CMM . 2016. Risk of ingesting As, Cd, and Pb in animal products in north Rio de Janeiro state, Brazil. Chemosphere 164 : 508 515.[CrossRef]
26. Zhang XY,, Zhou MY,, Li LL,, Jiang YJ,, Zou XT . 2017. Effects of arsenic supplementation in feed on laying performance, arsenic retention of eggs and organs, biochemical indices and endocrine hormones. Br Poult Sci 58 : 63 68.[CrossRef][PubMed]
27. Xi GF,, Zhou SB,, Ding HC,, Yao CX,, Kong JJ . 2014. Characteristics of arsenic content in the livestock farms’ surrounding environment in Shanghai suburbs. Huan Jing Ke Xue 35 : 1928 1932. (In Chinese.)[PubMed]
28. Jensen BB . 2016. Extensive literature search on the ‘effects of copper intake levels in the gut microbiota profile of target animals, in particular piglets’. EFSA Supporting Publications 13 : 1024E-n/a.[CrossRef]
29. European Medicines Agency (EMA), Committee for Veterinary Medicinal Products (CVMP) . 2016. European public MRL assessment report (EPMAR): copper carbonate (all food producing species). EMA/CVMP/ 758734/2015.
30. Ou D,, Li D,, Cao Y,, Li X,, Yin J,, Qiao S,, Wu G . 2007. Dietary supplementation with zinc oxide decreases expression of the stem cell factor in the small intestine of weanling pigs. J Nutr Biochem 18 : 820 826.[CrossRef][PubMed]
31. Schulte JN,, Brockmann GA,, Kreuzer-Redmer S . 2016. Feeding a high dosage of zinc oxide affects suppressor of cytokine gene expression in Salmonella Typhimurium infected piglets. Vet Immunol Immunopathol 178 : 10 13.[CrossRef][PubMed]
32. European Medicines Agency (EMA), Committee for Veterinary Medicinal Products (CVMP) . 1996. Zinc salts. EMEA/MRL/113/96-FINAL:
33. United States Department of Agriculture (USDA) . 2017. Livestock slaughter 2016 summary. USDA National Agricultural Statistics Service, Washington, DC.
34. European Medicines Agency (EMA), European Surveillance of Veterinary Antimicrobial Consumption (ESVAC) . 2016. Sales of veterinary antimicrobial agents in 29 European countries in 2014. EMA/61769/2016.
35. National Research Council, Committee on Nutrient Requirements of Swine . 2012. Nutrient Requirements of Swine. National Academies Press, Washington, DC.
36. Stolte J,, Tesfai M,, Øygarden L,, Kværnø S,, Keizer J,, Verheijen F,, Panagos P,, Ballabio C,, Hessel R (ed) . 2016. Soil Threats in Europe. EUR 27607 EN doi:10.2788/488054. (print); doi:10.2788/828742 (online).
37. Jensen J,, Larsen MM,, Bak J . 2016. National monitoring study in Denmark finds increased and critical levels of copper and zinc in arable soils fertilized with pig slurry. Environ Pollut 214 : 334 340.[CrossRef][PubMed]
38. Bak JL,, Jensen J,, Larsen MM . 2015. Belysning af kobber- og zinkindholdet i jord. Indhold og udvikling i kvadratnettet og måling på udvalgte brugstyper. Aarhus Universitet, DCE – Nationalt Center for Miljø og Energi, 72 s. - Videnskabelig rapport fra DCE - Nationalt Center for Miljø og Energi nr. 159.
39. Joint Research Center (JRC) European Union . 2010. Risk assessment report. CAS: 7440-66-6; EINECS No: 231-175-3 ZINC METAL.
40. Johnson TJ,, Siek KE,, Johnson SJ,, Nolan LK . 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]
41. Salem AZM,, Ammar H,, Lopez S,, Gohar YM,, González JS . 2011. Sensitivity of ruminal bacteria isolates of sheep, cattle and buffalo to some heavy metals. Anim Feed Sci Technol 163 : 143 149.[CrossRef]
42. Chen S,, Li X,, Sun G,, Zhang Y,, Su J,, Ye J . 2015. Heavy metal induced antibiotic resistance in bacterium LSJC7. Int J Mol Sci 16 : 23390 23404.[CrossRef][PubMed]
43. Henriques I,, Tacão M,, Leite L,, Fidalgo C,, Araújo S,, Oliveira C,, Alves A . 2016. Co-selection of antibiotic and metal(loid) resistance in Gram-negative epiphytic bacteria from contaminated salt marshes. Mar Pollut Bull 109 : 427 434.[CrossRef][PubMed]
44. Hasman H,, Franke S,, Rensing C, . 2005. Resistance to metals used in agricultural production, p 99 114. In Aarestrup FM,, Wegener HC (ed), Antimicrobial Resistance in Bacteria of Animal Origin. ASM Press, Washington, DC.
45. Jacob ME,, Fox JT,, Nagaraja TG,, Drouillard JS,, Amachawadi RG,, Narayanan SK . 2010. Effects of feeding elevated concentrations of copper and zinc on the antimicrobial susceptibilities of fecal bacteria in feedlot cattle. Foodborne Pathog Dis 7 : 643 648.[CrossRef][PubMed]
46. Bednorz C,, Oelgeschläger K,, Kinnemann B,, Hartmann S,, Neumann K,, Pieper R,, Bethe A,, Semmler T,, Tedin K,, Schierack P,, Wieler LH,, Guenther S . 2013. The broader context of antibiotic resistance: zinc feed supplementation of piglets increases the proportion of multi-resistant Escherichia coli in vivo. Int J Med Microbiol 303 : 396 403.[CrossRef][PubMed]
47. Toroglu S,, Dincer S . 2009. Heavy metal resistances of Enterobacteriaceae from Aksu River (Turkey) polluted with different sources. Asian J Chem 21 : 411 420.
48. Kumar PA,, Joseph B,, Patterson J . 2011. Antibiotic and heavy metal resistance profile of pathogens isolated from infected fish in Tuticorin, south-east coast of India. Indian J Fish 58 : 121 125.
49. Deredjian A,, Colinon C,, Brothier E,, Favre-Bonté S,, Cournoyer B,, Nazaret S . 2011. Antibiotic and metal resistance among hospital and outdoor strains of Pseudomonas aeruginosa. Res Microbiol 162 : 689 700.[CrossRef][PubMed]
50. Wei LS,, Musa N,, Wee W . 2010. Bacterial flora from a healthy freshwater Asian sea bass ( Lates calcarifer) fingerling hatchery with emphasis on their antimicrobial and heavy metal resistance pattern. Vet Arh 80 : 411 420.
51. Cavaco LM,, Hasman H,, Stegger M,, Andersen PS,, Skov R,, Fluit AC,, Ito T,, Aarestrup FM . 2010. Cloning and occurrence of czrC, a gene conferring cadmium and zinc resistance in methicillin-resistant Staphylococcus aureus CC398 isolates. Antimicrob Agents Chemother 54 : 3605 3608.[CrossRef][PubMed]
52. Fard RM,, Heuzenroeder MW,, Barton MD . 2011. Antimicrobial and heavy metal resistance in commensal enterococci isolated from pigs. Vet Microbiol 148 : 276 282.[CrossRef][PubMed]
53. Medardus JJ,, Molla BZ,, Nicol M,, Morrow WM,, Rajala-Schultz PJ,, Kazwala R,, Gebreyes WA . 2014. In-feed use of heavy metal micronutrients in U.S. swine production systems and its role in persistence of multidrug-resistant salmonellae. Appl Environ Microbiol 80 : 2317 2325.[CrossRef][PubMed]
54. Mourão J,, Marçal S,, Ramos P,, Campos J,, Machado J,, Peixe L,, Novais C,, Antunes P . 2016. Tolerance to multiple metal stressors in emerging non-typhoidal MDR Salmonella serotypes: a relevant role for copper in anaerobic conditions. J Antimicrob Chemother 71 : 2147 2157.[CrossRef][PubMed]
55. Amachawadi RG,, Scott HM,, Vinasco J,, Tokach MD,, Dritz SS,, Nelssen JL,, Nagaraja TG . 2015. Effects of in-feed copper, chlortetracycline, and tylosin on the prevalence of transferable copper resistance gene, tcrB, among fecal enterococci of weaned piglets. Foodborne Pathog Dis 12 : 670 678.[CrossRef][PubMed]
56. Aarestrup FM,, 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]
57. Hacioglu N,, Tosunoglu M . 2014. Determination of antimicrobial and heavy metal resistance profiles of some bacteria isolated from aquatic amphibian and reptile species. Environ Monit Assess 186 : 407 413.[CrossRef][PubMed]
58. Fang L,, Li X,, Li L,, Li S,, Liao X,, Sun J,, Liu Y . 2016. Co-spread of metal and antibiotic resistance within ST3-IncHI2 plasmids from E. coli isolates of food-producing animals. Sci Rep 6 : 25312.[CrossRef][PubMed]
59. Akinbowale OL,, Peng H,, Grant P,, Barton MD . 2007. Antibiotic and heavy metal resistance in motile aeromonads and pseudomonads from rainbow trout ( Oncorhynchus mykiss) farms in Australia. Int J Antimicrob Agents 30 : 177 182.[CrossRef][PubMed]
60. He Y,, Jin L,, Sun F,, Hu Q,, Chen L . 2016. Antibiotic and heavy-metal resistance of Vibrio parahaemolyticus isolated from fresh shrimps in Shanghai fish markets, China. Environ Sci Pollut Res Int 23 : 15033 15040.[CrossRef]
61. Hu Q,, Chen L . 2016. Virulence and antibiotic and heavy metal resistance of Vibrio parahaemolyticus isolated from crustaceans and shellfish in Shanghai, China. J Food Prot 79 : 1371 1377.[CrossRef]
62. Williams RJ,, Fraústo Da Silva JJ . 2003. Evolution was chemically constrained. J Theor Biol 220 : 323 343.[CrossRef][PubMed]
63. Hong Enriquez RP,, Do TN . 2012. Bioavailability of metal ions and evolutionary adaptation. Life (Basel) 2 : 274 285.[CrossRef][PubMed]
64. Macomber L,, Imlay JA . 2009. The iron-sulfur clusters of dehydratases are primary intracellular targets of copper toxicity. Proc Natl Acad Sci USA 106 : 8344 8349.[CrossRef][PubMed]
65. Dupont CL,, Grass G,, Rensing C . 2011. Copper toxicity and the origin of bacterial resistance: new insights and applications. Metallomics 3 : 1109 1118.[CrossRef][PubMed]
66. Chillappagari S,, Seubert A,, Trip H,, Kuipers OP,, Marahiel MA,, Miethke M . 2010. Copper stress affects iron homeostasis by destabilizing iron-sulfur cluster formation in Bacillus subtilis. J Bacteriol 192 : 2512 2524.[CrossRef][PubMed]
67. Chillappagari S,, Miethke M,, Trip H,, Kuipers OP,, Marahiel MA . 2009. Copper acquisition is mediated by YcnJ and regulated by YcnK and CsoR in Bacillus subtilis. J Bacteriol 191 : 2362 2370.[CrossRef][PubMed]
68. Hirooka K,, Edahiro T,, Kimura K,, Fujita Y . 2012. Direct and indirect regulation of the ycnKJI operon involved in copper uptake through two transcriptional repressors, YcnK and CsoR, in Bacillus subtilis. J Bacteriol 194 : 5675 5687.[CrossRef]
69. Yamada-Ankei T,, Iwasaki H,, Mori T . 1977. Production of copper coproporphyrin III by Bacillus cereus. I. Purification and identification of copper coproporphyrin III. J Biochem 81 : 835 842.[CrossRef][PubMed]
70. Balasubramanian R,, Kenney GE,, Rosenzweig AC . 2011. Dual pathways for copper uptake by methanotrophic bacteria. J Biol Chem 286 : 37313 37319.[CrossRef][PubMed]
71. Teitzel GM,, Geddie A,, De Long SK,, Kirisits MJ,, Whiteley M,, Parsek MR . 2006. Survival and growth in the presence of elevated copper: transcriptional profiling of copper-stressed Pseudomonas aeruginosa. J Bacteriol 188 : 7242 7256.[CrossRef][PubMed]
72. Whiting GC,, Rowbury RJ . 1995. Increased resistance of Escherichia coli to acrylic acid and to copper ions after cold-shock. Lett Appl Microbiol 20 : 240 242.[CrossRef][PubMed]
73. Taudte N,, Grass G . 2010. Point mutations change specificity and kinetics of metal uptake by ZupT from Escherichia coli. Biometals 23 : 643 656.[CrossRef][PubMed]
74. Grass G,, Franke S,, Taudte N,, Nies DH,, Kucharski LM,, Maguire ME,, Rensing C . 2005. The metal permease ZupT from Escherichia coli is a transporter with a broad substrate spectrum. J Bacteriol 187 : 1604 1611.[CrossRef][PubMed]
75. Guerinot ML . 2000. The ZIP family of metal transporters. Biochim Biophys Acta 1465 : 190 198.[CrossRef][PubMed]
76. Cha JS,, Cooksey DA . 1993. Copper hypersensitivity and uptake in Pseudomonas syringae containing cloned components of the copper resistance operon. Appl Environ Microbiol 59 : 1671 1674.[PubMed]
77. Fitch MW,, Graham DW,, Arnold RG,, Agarwal SK,, Phelps P,, Speitel GE Jr,, Georgiou G . 1993. Phenotypic characterization of copper-resistant mutants of Methylosinus trichosporium OB3b. Appl Environ Microbiol 59 : 2771 2776.[PubMed]
78. Anttila J,, Heinonen P,, Nenonen T,, Pino A,, Iwaï H,, Kauppi E,, Soliymani R,, Baumann M,, Saksi J,, Suni N,, Haltia T . 2011. Is coproporphyrin III a copper-acquisition compound in Paracoccus denitrificans? Biochim Biophys Acta 1807 : 311 318.[CrossRef][PubMed]
79. DiSpirito AA,, Zahn JA,, Graham DW,, Kim HJ,, Larive CK,, Derrick TS,, Cox CD,, Taylor A . 1998. Copper-binding compounds from Methylosinus trichosporium OB3b. J Bacteriol 180 : 3606 3613.[PubMed]
80. Kim HJ,, Graham DW,, DiSpirito AA,, Alterman MA,, Galeva N,, Larive CK,, Asunskis D,, Sherwood PM . 2004. Methanobactin, a copper-acquisition compound from methane-oxidizing bacteria. Science 305 : 1612 1615.[CrossRef][PubMed]
81. Zahn JA,, DiSpirito AA . 1996. Membrane-associated methane monooxygenase from Methylococcus capsulatus (Bath). J Bacteriol 178 : 1018 1029.[CrossRef][PubMed]
82. Nicolaisen K,, Hahn A,, Valdebenito M,, Moslavac S,, Samborski A,, Maldener I,, Wilken C,, Valladares A,, Flores E,, Hantke K,, Schleiff E . 2010. The interplay between siderophore secretion and coupled iron and copper transport in the heterocyst-forming cyanobacterium Anabaena sp. PCC 7120. Biochim Biophys Acta 1798 : 2131 2140.[CrossRef][PubMed]
83. Argüello JM . 2003. Identification of ion-selectivity determinants in heavy-metal transport P 1B-type ATPases. J Membr Biol 195 : 93 108.[CrossRef][PubMed]
84. Argüello JM,, González-Guerrero M . 2008. Cu + -ATPases brake system. Structure 16 : 833 834.[CrossRef][PubMed]
85. Argüello JM,, González-Guerrero M,, Raimunda D . 2011. Bacterial transition metal P (1B)-ATPases: transport mechanism and roles in virulence. Biochemistry 50 : 9940 9949.[CrossRef][PubMed]
86. Argüello JM,, Eren E,, González-Guerrero M . 2007. The structure and function of heavy metal transport P 1B-ATPases. Biometals 20 : 233 248.[CrossRef][PubMed]
87. Raimunda D,, González-Guerrero M,, Leeber BW III,, Argüello JM . 2011. The transport mechanism of bacterial Cu +-ATPases: distinct efflux rates adapted to different function. Biometals 24 : 467 475.[CrossRef][PubMed]
88. Rosenzweig AC,, Argüello JM . 2012. Toward a molecular understanding of metal transport by P(1B)-type ATPases. Curr Top Membr 69 : 113 136.[CrossRef][PubMed]
89. Solioz M,, Odermatt A,, Krapf R . 1994. Copper pumping ATPases: common concepts in bacteria and man. FEBS Lett 346 : 44 47.[CrossRef][PubMed]
90. Solioz M,, Vulpe C . 1996. CPx-type ATPases: a class of P-type ATPases that pump heavy metals. Trends Biochem Sci 21 : 237 241.[CrossRef][PubMed]
91. Odermatt A,, Suter H,, Krapf R,, Solioz M . 1992. An ATPase operon involved in copper resistance by Enterococcus hirae. Ann N Y Acad Sci 671( 1 Ion-Motive AT) : 484 486.[CrossRef]
92. Solioz M,, Odermatt A . 1995. Copper and silver transport by CopB-ATPase in membrane vesicles of Enterococcus hirae. J Biol Chem 270 : 9217 9221.[CrossRef][PubMed]
93. Solioz M,, Stoyanov JV . 2003. Copper homeostasis in Enterococcus hirae. FEMS Microbiol Rev 27 : 183 195.[CrossRef][PubMed]
94. Odermatt A,, Krapf R,, Solioz M . 1994. Induction of the putative copper ATPases, CopA and CopB, of Enterococcus hirae by Ag + and Cu 2+, and Ag + extrusion by CopB. Biochem Biophys Res Commun 202 : 44 48.[CrossRef][PubMed]
95. Odermatt A,, Solioz M . 1995. Two trans-acting metalloregulatory proteins controlling expression of the copper-ATPases of Enterococcus hirae. J Biol Chem 270 : 4349 4354.[CrossRef][PubMed]
96. González-Guerrero M,, Raimunda D,, Cheng X,, Argüello JM . 2010. Distinct functional roles of homologous Cu + efflux ATPases in Pseudomonas aeruginosa. Mol Microbiol 78 : 1246 1258.[CrossRef][PubMed]
97. Gaballa A,, Cao M,, Helmann JD . 2003. Two MerR homologues that affect copper induction of the Bacillus subtilis copZA operon. Microbiology 149 : 3413 3421.[CrossRef][PubMed]
98. Reyes A,, Leiva A,, Cambiazo V,, Méndez MA,, González M . 2006. Cop-like operon: structure and organization in species of the Lactobacillale order. Biol Res 39 : 87 93.[CrossRef][PubMed]
99. Grass G,, Rensing C . 2001. Genes involved in copper homeostasis in Escherichia coli. J Bacteriol 183 : 2145 2147.[CrossRef][PubMed]
100. Outten FW,, Huffman DL,, Hale JA,, O’Halloran TV . 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]
101. Rensing C,, Grass G . 2003. Escherichia coli mechanisms of copper homeostasis in a changing environment. FEMS Microbiol Rev 27 : 197 213.[CrossRef][PubMed]
102. Outten FW,, Outten CE,, Hale J,, O’Halloran TV . 2000. Transcriptional activation of an Escherichia coli copper efflux regulon by the chromosomal MerR homologue, cueR. J Biol Chem 275 : 31024 31029.[CrossRef][PubMed]
103. Petersen C,, Møller LB . 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]
104. Stoyanov JV,, Hobman JL,, Brown NL . 2001. CueR (YbbI) of Escherichia coli is a MerR family regulator controlling expression of the copper exporter CopA. Mol Microbiol 39 : 502 511.[CrossRef][PubMed]
105. Changela A,, Chen K,, Xue Y,, Holschen J,, Outten CE,, O’Halloran TV,, Mondragón A . 2003. Molecular basis of metal-ion selectivity and zeptomolar sensitivity by CueR. Science 301 : 1383 1387.[CrossRef][PubMed]
106. Rensing C,, Fan B,, Sharma R,, Mitra B,, Rosen BP . 2000. CopA: An Escherichia coli Cu(I)-translocating P-type ATPase. Proc Natl Acad Sci USA 97 : 652 656.[CrossRef][PubMed]
107. Fan B,, Rosen BP . 2002. Biochemical characterization of CopA, the Escherichia coli Cu(I)-translocating P-type ATPase. J Biol Chem 277 : 46987 46992.[CrossRef][PubMed]
108. Grass G,, Rensing C . 2001. CueO is a multi-copper oxidase that confers copper tolerance in Escherichia coli. Biochem Biophys Res Commun 286 : 902 908.[CrossRef][PubMed]
109. Kim C,, Lorenz WW,, Hoopes JT,, Dean JF . 2001. Oxidation of phenolate siderophores by the multicopper oxidase encoded by the Escherichia coli yacK gene. J Bacteriol 183 : 4866 4875.[CrossRef][PubMed]
110. Roberts SA,, Weichsel A,, Grass G,, Thakali K,, Hazzard JT,, Tollin G,, Rensing C,, Montfort WR . 2002. Crystal structure and electron transfer kinetics of CueO, a multicopper oxidase required for copper homeostasis in Escherichia coli. Proc Natl Acad Sci USA 99 : 2766 2771.[CrossRef][PubMed]
111. Roberts SA,, Wildner GF,, Grass G,, Weichsel A,, Ambrus A,, Rensing C,, Montfort WR . 2003. A labile regulatory copper ion lies near the T1 copper site in the multicopper oxidase CueO. J Biol Chem 278 : 31958 31963.[CrossRef][PubMed]
112. Grass G,, Thakali K,, Klebba PE,, Thieme D,, Müller A,, Wildner GF,, Rensing C . 2004. Linkage between catecholate siderophores and the multicopper oxidase CueO in Escherichia coli. J Bacteriol 186 : 5826 5833.[CrossRef][PubMed]
113. Singh SK,, Grass G,, Rensing C,, Montfort WR . 2004. Cuprous oxidase activity of CueO from Escherichia coli. J Bacteriol 186 : 7815 7817.[CrossRef][PubMed]
114. Sakurai T,, Kataoka K . 2007. Basic and applied features of multicopper oxidases, CueO, bilirubin oxidase, and laccase. Chem Rec 7 : 220 229.[CrossRef]
115. Djoko KY,, Chong LX,, Wedd AG,, Xiao Z . 2010. Reaction mechanisms of the multicopper oxidase CueO from Escherichia coli support its functional role as a cuprous oxidase. J Am Chem Soc 132 : 2005 2015.[CrossRef][PubMed]
116. Singh SK,, Roberts SA,, McDevitt SF,, Weichsel A,, Wildner GF,, Grass GB,, Rensing C,, Montfort WR . 2011. Crystal structures of multicopper oxidase CueO bound to copper(I) and silver(I): functional role of a methionine-rich sequence. J Biol Chem 286 : 37849 37857.[CrossRef][PubMed]
117. Lim SY,, Joe MH,, Song SS,, Lee MH,, Foster JW,, Park YK,, Choi SY,, Lee IS . 2002. CuiD is a crucial gene for survival at high copper environment in Salmonella enterica serovar Typhimurium. Mol Cells 14 : 177 184.[PubMed]
118. Kosman DJ . 2010. Multicopper oxidases: a workshop on copper coordination chemistry, electron transfer, and metallophysiology. J Biol Inorg Chem 15 : 15 28.[CrossRef][PubMed]
119. Rademacher C,, Moser R,, Lackmann JW,, Klinkert B,, Narberhaus F,, Masepohl B . 2012. Transcriptional and posttranscriptional events control copper-responsive expression of a Rhodobacter capsulatus multicopper oxidase. J Bacteriol 194 : 1849 1859.[CrossRef][PubMed]
120. Nies DH,, Herzberg M . 2013. A fresh view of the cell biology of copper in enterobacteria. Mol Microbiol 87 : 447 454.[CrossRef][PubMed]
121. Silveira E,, Freitas AR,, Antunes P,, Barros M,, Campos J,, Coque TM,, Peixe L,, Novais C . 2014. Co-transfer of resistance to high concentrations of copper and first-line antibiotics among Enterococcus from different origins (humans, animals, the environment and foods) and clonal lineages. J Antimicrob Chemother 69 : 899 906.[CrossRef][PubMed]
122. Padilla-Benavides T,, George Thompson AM,, McEvoy MM,, Argüello JM . 2014. Mechanism of ATPase-mediated Cu + export and delivery to periplasmic chaperones: the interaction of Escherichia coli CopA and CusF. J Biol Chem 289 : 20492 20501.[CrossRef][PubMed]
123. Franke S,, Grass G,, Rensing C,, Nies DH . 2003. Molecular analysis of the copper-transporting efflux system CusCFBA of Escherichia coli. J Bacteriol 185 : 3804 3812.[CrossRef][PubMed]
124. Munson GP,, Lam DL,, Outten FW,, O’Halloran TV . 2000. Identification of a copper-responsive two-component system on the chromosome of Escherichia coli K-12. J Bacteriol 182 : 5864 5871.[CrossRef][PubMed]
125. Franke S,, Grass G,, Nies DH . 2001. The product of the ybdE gene of the Escherichia coli chromosome is involved in detoxification of silver ions. Microbiology 147 : 965 972.[CrossRef][PubMed]
126. Bagai I,, Liu W,, Rensing C,, Blackburn NJ,, McEvoy MM . 2007. Substrate-linked conformational change in the periplasmic component of a Cu(I)/Ag(I) efflux system. J Biol Chem 282 : 35695 35702.[CrossRef][PubMed]
127. Su CC,, Yang F,, Long F,, Reyon D,, Routh MD,, Kuo DW,, Mokhtari AK,, Van Ornam JD,, Rabe KL,, Hoy JA,, Lee YJ,, Rajashankar KR,, Yu EW . 2009. Crystal structure of the membrane fusion protein CusB from Escherichia coli. J Mol Biol 393 : 342 355.[CrossRef][PubMed]
128. Long F,, Su CC,, Zimmermann MT,, Boyken SE,, Rajashankar KR,, Jernigan RL,, Yu EW . 2010. Crystal structures of the CusA efflux pump suggest methionine-mediated metal transport. Nature 467 : 484 488.[CrossRef][PubMed]
129. Kulathila R,, Kulathila R,, Indic M,, van den Berg B . 2011. Crystal structure of Escherichia coli CusC, the outer membrane component of a heavy metal efflux pump. PLoS One 6 : e15610.[CrossRef][PubMed]
130. Su CC,, Long F,, Zimmermann MT,, Rajashankar KR,, Jernigan RL,, Yu EW . 2011. Crystal structure of the CusBA heavy-metal efflux complex of Escherichia coli. Nature 470 : 558 562.[CrossRef][PubMed]
131. Kim EH,, Nies DH,, McEvoy MM,, Rensing C . 2011. Switch or funnel: how RND-type transport systems control periplasmic metal homeostasis. J Bacteriol 193 : 2381 2387.[CrossRef][PubMed]
132. Loftin IR,, Franke S,, Roberts SA,, Weichsel A,, Héroux A,, Montfort WR,, Rensing C,, McEvoy MM . 2005. A novel copper-binding fold for the periplasmic copper resistance protein CusF. Biochemistry 44 : 10533 10540.[CrossRef][PubMed]
133. Kittleson JT,, Loftin IR,, Hausrath AC,, Engelhardt KP,, Rensing C,, McEvoy MM . 2006. Periplasmic metal-resistance protein CusF exhibits high affinity and specificity for both CuI and AgI. Biochemistry 45 : 11096 11102.[CrossRef][PubMed]
134. Xue Y,, Davis AV,, Balakrishnan G,, Stasser JP,, Staehlin BM,, Focia P,, Spiro TG,, Penner-Hahn JE,, O’Halloran TV . 2008. Cu(I) recognition via cation-pi and methionine interactions in CusF. Nat Chem Biol 4 : 107 109.[CrossRef][PubMed]
135. Bagai I,, Rensing C,, Blackburn NJ,, McEvoy MM . 2008. Direct metal transfer between periplasmic proteins identifies a bacterial copper chaperone. Biochemistry 47 : 11408 11414.[CrossRef][PubMed]
136. Bersch B,, Derfoufi KM,, De Angelis F,, Auquier V,, Ekendé EN,, Mergeay M,, Ruysschaert JM,, Vandenbussche G . 2011. Structural and metal binding characterization of the C-terminal metallochaperone domain of membrane fusion protein SilB from Cupriavidus metallidurans CH34. Biochemistry 50 : 2194 2204.[CrossRef][PubMed]
137. Mealman TD,, Bagai I,, Singh P,, Goodlett DR,, Rensing C,, Zhou H,, Wysocki VH,, McEvoy MM . 2011. Interactions between CusF and CusB identified by NMR spectroscopy and chemical cross-linking coupled to mass spectrometry. Biochemistry 50 : 2559 2566.[CrossRef][PubMed]
138. Chacón KN,, Mealman TD,, McEvoy MM,, Blackburn NJ . 2014. Tracking metal ions through a Cu/Ag efflux pump assigns the functional roles of the periplasmic proteins. Proc Natl Acad Sci USA 111 : 15373 15378.[CrossRef][PubMed]
139. Meir A,, Natan A,, Moskovitz Y,, Ruthstein S . 2015. EPR spectroscopy identifies Met and Lys residues that are essential for the interaction between the CusB N-terminal domain and metallochaperone CusF. Metallomics 7 : 1163 1172.[CrossRef][PubMed]
140. Pontel LB,, Soncini FC . 2009. Alternative periplasmic copper-resistance mechanisms in Gram negative bacteria. Mol Microbiol 73 : 212 225.[CrossRef][PubMed]
141. Osman D,, Waldron KJ,, Denton H,, Taylor CM,, Grant AJ,, Mastroeni P,, Robinson NJ,, Cavet JS . 2010. Copper homeostasis in Salmonella is atypical and copper-CueP is a major periplasmic metal complex. J Biol Chem 285 : 25259 25268.[CrossRef][PubMed]
142. Yun BY,, Piao S,, Kim YG,, Moon HR,, Choi EJ,, Kim YO,, Nam BH,, Lee SJ,, Ha NC . 2011. Crystallization and preliminary X-ray crystallographic analysis of Salmonella Typhimurium CueP. Acta Crystallogr Sect F Struct Biol Cryst Commun 67 : 675 677.[CrossRef][PubMed]
143. Yoon BY,, Yeom JH,, Kim JS,, Um SH,, Jo I,, Lee K,, Kim YH,, Ha NC . 2014. Direct ROS scavenging activity of CueP from Salmonella enterica serovar Typhimurium. Mol Cells 37 : 100 108.[CrossRef][PubMed]
144. Williams JR,, Morgan AG,, Rouch DA,, Brown NL,, Lee BT . 1993. Copper-resistant enteric bacteria from United Kingdom and Australian piggeries. Appl Environ Microbiol 59 : 2531 2537.[PubMed]
145. Tetaz TJ,, Luke RK . 1983. Plasmid-controlled resistance to copper in Escherichia coli. J Bacteriol 154 : 1263 1268.[PubMed]
146. Brown NL,, Barrett SR,, Camakaris J,, Lee BT,, Rouch DA . 1995. Molecular genetics and transport analysis of the copper-resistance determinant ( pco) from Escherichia coli plasmid pRJ1004. Mol Microbiol 17 : 1153 1166.[CrossRef][PubMed]
147. Rouch DA,, Brown NL . 1997. Copper-inducible transcriptional regulation at two promoters in the Escherichia coli copper resistance determinant pco. Microbiology 143 : 1191 1202.[CrossRef][PubMed]
148. Lee SM,, Grass G,, Rensing C,, Barrett SR,, Yates CJ,, Stoyanov JV,, Brown NL . 2002. The Pco proteins are involved in periplasmic copper handling in Escherichia coli. Biochem Biophys Res Commun 295 : 616 620.[CrossRef]
149. Zimmermann M,, Udagedara SR,, Sze CM,, Ryan TM,, Howlett GJ,, Xiao Z,, Wedd AG . 2012. PcoE: a metal sponge expressed to the periplasm of copper resistance Escherichia coli. Implication of its function role in copper resistance. J Inorg Biochem 115 : 186 197.[CrossRef][PubMed]
150. Hao X,, Lüthje FL,, Qin Y,, McDevitt SF,, Lutay N,, Hobman JL,, Asiani K,, Soncini FC,, German N,, Zhang S,, Zhu YG,, Rensing C . 2015. Survival in amoeba: a major selection pressure on the presence of bacterial copper and zinc resistance determinants? Identification of a “copper pathogenicity island”. Appl Microbiol Biotechnol 99 : 5817 5824.[CrossRef][PubMed]
151. Staehlin BM,, Gibbons JG,, Rokas A,, O’Halloran TV,, Slot JC . 2016. Evolution of a heavy metal homeostasis/resistance island reflects increasing copper stress in Enterobacteria. Genome Biol Evol 8 : 811 826.
152. McHugh GL,, Moellering RC,, Hopkins CC,, Swartz MN . 1975. Salmonella typhimurium resistant to silver nitrate, chloramphenicol, and ampicillin. Lancet 1 : 235 240.[CrossRef]
153. Gupta A,, Matsui K,, Lo JF,, Silver S . 1999. Molecular basis for resistance to silver cations in Salmonella. Nat Med 5 : 183 188.[CrossRef][PubMed]
154. Randall CP,, Gupta A,, Jackson N,, Busse D,, O’Neill AJ . 2015. Silver resistance in Gram-negative bacteria: a dissection of endogenous and exogenous mechanisms. J Antimicrob Chemother 70 : 1037 1046.
155. Lüthje FL,, Hasman H,, Aarestrup FM,, Alwathnani HA,, Rensing C . 2014. Genome sequences of two copper-resistant Escherichia coli strains isolated from copper-fed pigs. Genome Announc 2 : e01341.[CrossRef][PubMed]
156. Qin Y,, Hasman H,, Aarestrup FM,, Alwathnani HA,, Rensing C . 2014. Genome sequences of three highly copper-resistant Salmonella enterica subsp. I serovar Typhimurium strains isolated from pigs in Denmark. Genome Announc 2 : e01334-14.[CrossRef][PubMed]
157. Peters JE,, Fricker AD,, Kapili BJ,, Petassi MT . 2014. Heteromeric transposase elements: generators of genomic islands across diverse bacteria. Mol Microbiol 93 : 1084 1092.
158. Chaturvedi KS,, Henderson JP . 2014. Pathogenic adaptations to host-derived antibacterial copper. Front Cell Infect Microbiol 4 : 3.[CrossRef][PubMed]
159. Schubert S,, Dufke S,, Sorsa J,, Heesemann J . 2004. A novel integrative and conjugative element (ICE) of Escherichia coli: the putative progenitor of the Yersinia high-pathogenicity island. Mol Microbiol 51 : 837 848.[CrossRef][PubMed]
160. Rakin A,, Schneider L,, Podladchikova O . 2012. Hunger for iron: the alternative siderophore iron scavenging systems in highly virulent Yersinia. Front Cell Infect Microbiol 2 : 151/1.
161. Aviv G,, Tsyba K,, Steck N,, Salmon-Divon M,, Cornelius A,, Rahav G,, Grassl GA,, Gal-Mor O . 2014. A unique megaplasmid contributes to stress tolerance and pathogenicity of an emergent Salmonella enterica serovar Infantis strain. Environ Microbiol 16 : 977 994.[CrossRef][PubMed]
162. Chaturvedi KS,, Hung CS,, Giblin DE,, Urushidani S,, Austin AM,, Dinauer MC,, Henderson JP . 2014. Cupric yersiniabactin is a virulence-associated superoxide dismutase mimic. ACS Chem Biol 9 : 551 561.[CrossRef][PubMed]
163. Fodah RA,, Scott JB,, Tam HH,, Yan P,, Pfeffer TL,, Bundschuh R,, Warawa JM . 2014. Correlation of Klebsiella pneumoniae comparative genetic analyses with virulence profiles in a murine respiratory disease model. PLoS One 9 : e107394.[CrossRef][PubMed]
164. Freitas AR,, Coque TM,, Novais C,, Hammerum AM,, Lester CH,, Zervos MJ,, Donabedian S,, Jensen LB,, Francia MV,, Baquero F,, Peixe L . 2011. Human and swine hosts share vancomycin-resistant Enterococcus faecium CC17 and CC5 and Enterococcus faecalis CC2 clonal clusters harboring Tn1546 on indistinguishable plasmids. J Clin Microbiol 49 : 925 931.[CrossRef][PubMed]
165. Zhang S,, Wang D,, Wang Y,, Hasman H,, Aarestrup FM,, Alwathnani HA,, Zhu YG,, Rensing C . 2015. Genome sequences of copper resistant and sensitive Enterococcus faecalis strains isolated from copper-fed pigs in Denmark. Stand Genomic Sci 10 : 35-015-0021-1.[CrossRef]
166. Hasman H,, Aarestrup FM . 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]
167. Amachawadi RG,, Shelton NW,, Jacob ME,, Shi X,, Narayanan SK,, Zurek L,, Dritz SS,, Nelssen JL,, Tokach MD,, Nagaraja TG . 2010. Occurrence of tcrB, a transferable copper resistance gene, in fecal enterococci of swine. Foodborne Pathog Dis 7 : 1089 1097.[CrossRef][PubMed]
168. Amachawadi RG,, Scott HM,, Alvarado CA,, Mainini TR,, Vinasco J,, Drouillard JS,, Nagaraja TG . 2013. Occurrence of the transferable copper resistance gene tcrB among fecal enterococci of U.S. feedlot cattle fed copper-supplemented diets. Appl Environ Microbiol 79 : 4369 4375.[CrossRef][PubMed]
169. Pasquaroli S,, Di Cesare A,, Vignaroli C,, Conti G,, Citterio B,, Biavasco F . 2014. Erythromycin- and copper-resistant Enterococcus hirae from marine sediment and co-transfer of erm(B) and tcrB to human Enterococcus faecalis. Diagn Microbiol Infect Dis 80 : 26 28.[CrossRef][PubMed]
170. Hasman H . 2005. The tcrB gene is part of the tcrYAZB operon conferring copper resistance in Enterococcus faecium and Enterococcus faecalis. Microbiology 151 : 3019 3025.[CrossRef][PubMed]
171. Rensing C,, Alwathnani HA,, McDevitt SF, . 2016. The copper metallome in prokaryotic cells, p 161 173. In de Bruijn FJ (ed), Stress and Environmental Regulation of Gene Expression and Adaptation in Bacteria. John Wiley & Sons, Inc., Hoboken, NJ.[CrossRef]
172. Hedges SB,, Chen H,, Kumar S,, Wang DY,, Thompson AS,, Watanabe H . 2001. A genomic timescale for the origin of eukaryotes. BMC Evol Biol 1 : 4.[CrossRef][PubMed]
173. Outten CE,, O’Halloran TV . 2001. Femtomolar sensitivity of metalloregulatory proteins controlling zinc homeostasis. Science 292 : 2488 2492.[CrossRef][PubMed]
174. Patzer SI,, Hantke K . 1998. The ZnuABC high-affinity zinc uptake system and its regulator Zur in Escherichia coli. Mol Microbiol 28 : 1199 1210.[CrossRef][PubMed]
175. Sabri M,, Houle S,, Dozois CM . 2009. Roles of the extraintestinal pathogenic Escherichia coli ZnuACB and ZupT zinc transporters during urinary tract infection. Infect Immun 77 : 1155 1164.[CrossRef][PubMed]
176. Patzer SI,, Hantke K . 2000. The zinc-responsive regulator Zur and its control of the znu gene cluster encoding the ZnuABC zinc uptake system in Escherichia coli. J Biol Chem 275 : 24321 24332.[CrossRef][PubMed]
177. Sigdel TK,, Easton JA,, Crowder MW . 2006. Transcriptional response of Escherichia coli to TPEN. 188 : 6709 6713.[PubMed]
178. Gilston BA,, Wang S,, Marcus MD,, Canalizo-Hernández MA,, Swindell EP,, Xue Y,, Mondragón A,, O’Halloran TV . 2014. Structural and mechanistic basis of zinc regulation across the E. coli Zur regulon. PLoS Biol 12 : e1001987.[CrossRef][PubMed]
179. Mergeay M,, Nies D,, Schlegel HG,, Gerits J,, Charles P,, Van Gijsegem F . 1985. Alcaligenes eutrophus CH34 is a facultative chemolithotroph with plasmid-bound resistance to heavy metals. J Bacteriol 162 : 328 334.[PubMed]
180. Kirsten A,, Herzberg M,, Voigt A,, Seravalli J,, Grass G,, Scherer J,, Nies DH . 2011. Contributions of five secondary metal uptake systems to metal homeostasis of Cupriavidus metallidurans CH34. J Bacteriol 193 : 4652 4663.[CrossRef][PubMed]
181. Herzberg M,, Bauer L,, Nies DH . 2014. Deletion of the zupT gene for a zinc importer influences zinc pools in Cupriavidus metallidurans CH34. Metallomics 6 : 421 436.[CrossRef][PubMed]
182. Grass G,, Wong MD,, Rosen BP,, Smith RL,, Rensing C . 2002. ZupT is a Zn(II) uptake system in Escherichia coli. J Bacteriol 184 : 864 866.[CrossRef][PubMed]
183. Cerasi M,, Liu JZ,, Ammendola S,, Poe AJ,, Petrarca P,, Pesciaroli M,, Pasquali P,, Raffatellu M,, Battistoni A . 2014. The ZupT transporter plays an important role in zinc homeostasis and contributes to Salmonella enterica virulence. Metallomics 6 : 845 853.[CrossRef][PubMed]
184. Jackson RJ,, Binet MR,, Lee LJ,, Ma R,, Graham AI,, McLeod CW,, Poole RK . 2008. Expression of the PitA phosphate/metal transporter of Escherichia coli is responsive to zinc and inorganic phosphate levels. FEMS Microbiol Lett 289 : 219 224.[CrossRef][PubMed]
185. Beard SJ,, Hashim R,, Wu G,, Binet MR,, Hughes MN,, Poole RK . 2000. Evidence for the transport of zinc(II) ions via the pit inorganic phosphate transport system in Escherichia coli. FEMS Microbiol Lett 184 : 231 235.[CrossRef][PubMed]
186. Webb M . 1970. Interrelationships between the utilization of magnesium and the uptake of other bivalent cations by bacteria. Biochim Biophys Acta 222 : 428 439.[CrossRef]
187. Krom BP,, Huttinga H,, Warner JB,, Lolkema JS . 2002. Impact of the Mg(2+)-citrate transporter CitM on heavy metal toxicity in Bacillus subtilis. Arch Microbiol 178 : 370 375.[CrossRef][PubMed]
188. Knoop V,, Groth-Malonek M,, Gebert M,, Eifler K,, Weyand K . 2005. Transport of magnesium and other divalent cations: evolution of the 2-TM-GxN proteins in the MIT superfamily. Mol Genet Genomics 274 : 205 216.[CrossRef][PubMed]
189. Legatzki A,, Grass G,, Anton A,, Rensing C,, Nies DH . 2003. Interplay of the Czc system and two P-type ATPases in conferring metal resistance to Ralstonia metallidurans. J Bacteriol 185 : 4354 4361.[CrossRef][PubMed]
190. Nies DH . 2007. How cells control zinc homeostasis. Science 317 : 1695 1696.[CrossRef][PubMed]
191. Rensing C,, Mitra B,, Rosen BP . 1998. A Zn(II)-translocating P-type ATPase from Proteus mirabilis. Biochem Cell Biol 76 : 787 790.[CrossRef][PubMed]
192. Rensing C,, Ghosh M,, Rosen BP . 1999. Families of soft-metal-ion-transporting ATPases. J Bacteriol 181 : 5891 5897.[PubMed]
193. Sharma R,, Rensing C,, Rosen BP,, Mitra B . 2000. The ATP hydrolytic activity of purified ZntA, a Pb(II)/Cd(II)/Zn(II)-translocating ATPase from Escherichia coli. J Biol Chem 275 : 3873 3878.[CrossRef][PubMed]
194. Smith K,, Novick RP . 1972. Genetic studies on plasmid-linked cadmium resistance in Staphylococcus aureus. J Bacteriol 112 : 761 772.[PubMed]
195. Nucifora G,, Chu L,, Misra TK,, Silver S . 1989. Cadmium resistance from Staphylococcus aureus plasmid pI258 cadA gene results from a cadmium-efflux ATPase. Proc Natl Acad Sci USA 86 : 3544 3548.[CrossRef][PubMed]
196. Wang D,, Hosteen O,, Fierke CA . 2012. ZntR-mediated transcription of zntA responds to nanomolar intracellular free zinc. J Inorg Biochem 111 : 173 181.[CrossRef][PubMed]
197. Blattner FR,, Plunkett G III,, Bloch CA,, Perna NT,, Burland V,, Riley M,, Collado-Vides J,, Glasner JD,, Rode CK,, Mayhew GF,, Gregor J,, Davis NW,, Kirkpatrick HA,, Goeden MA,, Rose DJ,, Mau B,, Shao Y . 1997. The complete genome sequence of Escherichia coli K-12. Science 277 : 1453 1462.[CrossRef][PubMed]
198. Yoon KP,, Silver S . 1991. A second gene in the Staphylococcus aureus cadA cadmium resistance determinant of plasmid pI258. J Bacteriol 173 : 7636 7642.[CrossRef][PubMed]
199. Argudín MA,, Butaye P . 2016. Dissemination of metal resistance genes among animal methicillin-resistant coagulase-negative staphylococci. Res Vet Sci 105 : 192 194.[CrossRef][PubMed]
200. Slifierz MJ,, Park J,, Friendship RM,, Weese JS . 2014. Zinc-resistance gene CzrC identified in methicillin-resistant Staphylococcus hyicus isolated from pigs with exudative epidermitis. Can Vet J 55 : 489 490.[PubMed]
201. Vandendriessche S,, Vanderhaeghen W,, Larsen J,, de Mendonça R,, Hallin M,, Butaye P,, Hermans K,, Haesebrouck F,, Denis O . 2014. High genetic diversity of methicillin-susceptible Staphylococcus aureus (MSSA) from humans and animals on livestock farms and presence of SCCmec remnant DNA in MSSA CC398. J Antimicrob Chemother 69 : 355 362.[CrossRef][PubMed]
202. Vandendriessche S,, Vanderhaeghen W,, Soares FV,, Hallin M,, Catry B,, Hermans K,, Butaye P,, Haesebrouck F,, Struelens MJ,, Denis O . 2013. Prevalence, risk factors and genetic diversity of methicillin-resistant Staphylococcus aureus carried by humans and animals across livestock production sectors. J Antimicrob Chemother 68 : 1510 1516.[CrossRef][PubMed]
203. Agersø Y,, Hasman H,, Cavaco LM,, Pedersen K,, Aarestrup FM . 2012. Study of methicillin resistant Staphylococcus aureus (MRSA) in Danish pigs at slaughter and in imported retail meat reveals a novel MRSA type in slaughter pigs. Vet Microbiol 157 : 246 250.[CrossRef][PubMed]
204. Nair R,, Thapaliya D,, Su Y,, Smith TC . 2014. Resistance to zinc and cadmium in Staphylococcus aureus of human and animal origin. Infect Control Hosp Epidemiol 35( Suppl 3) : S32 S39.[CrossRef][PubMed]
205. Grass G,, Fan B,, Rosen BP,, Franke S,, Nies DH,, Rensing C . 2001. ZitB (YbgR), a member of the cation diffusion facilitator family, is an additional zinc transporter in Escherichia coli. J Bacteriol 183 : 4664 4667.[CrossRef][PubMed]
206. Grass G,, Otto M,, Fricke B,, Haney CJ,, Rensing C,, Nies DH,, Munkelt D . 2005. FieF (YiiP) from Escherichia coli mediates decreased cellular accumulation of iron and relieves iron stress. Arch Microbiol 183 : 9 18.[CrossRef][PubMed]
207. Xiong A,, Jayaswal RK . 1998. Molecular characterization of a chromosomal determinant conferring resistance to zinc and cobalt ions in Staphylococcus aureus. J Bacteriol 180 : 4024 4029.[PubMed]
208. Singh VK,, Xiong A,, Usgaard TR,, Chakrabarti S,, Deora R,, Misra TK,, Jayaswal RK . 1999. ZntR is an autoregulatory protein and negatively regulates the chromosomal zinc resistance operon znt of Staphylococcus aureus. Mol Microbiol 33 : 200 207.[CrossRef][PubMed]
209. Van Pham ST,, Engman H,, Dahlgren LG,, Cornvik T,, Eshaghi S . 2010. A systematic approach to isolate mono-disperse membrane proteins: purification of zinc transporter ZntB. Protein Expr Purif 72 : 48 54.[CrossRef][PubMed]
210. Papp-Wallace KM,, Maguire ME . 2007. Bacterial homologs of eukaryotic membrane proteins: the 2-TM-GxN family of Mg(2+) transporters. Mol Membr Biol 24 : 351 356.[CrossRef][PubMed]
211. Caldwell AM,, Smith RL . 2003. Membrane topology of the ZntB efflux system of Salmonella enterica serovar Typhimurium. J Bacteriol 185 : 374 376.[CrossRef][PubMed]
212. Wan Q,, Ahmad MF,, Fairman J,, Gorzelle B,, de la Fuente M,, Dealwis C,, Maguire ME . 2011. X-ray crystallography and isothermal titration calorimetry studies of the Salmonella zinc transporter ZntB. Structure 19 : 700 710.[CrossRef][PubMed]
213. Worlock AJ,, Smith RL . 2002. ZntB is a novel Zn 2+ transporter in Salmonella enterica serovar Typhimurium. J Bacteriol 184 : 4369 4373.[CrossRef][PubMed]
214. Chaoprasid P,, Nookabkaew S,, Sukchawalit R,, Mongkolsuk S . 2015. Roles of Agrobacterium tumefaciens C58 ZntA and ZntB and the transcriptional regulator ZntR in controlling Cd 2+/Zn 2+/Co 2+ resistance and the peroxide stress response. Microbiology 161 : 1730 1740.[CrossRef][PubMed]
215. Nies DH,, Silver S . 1995. Ion efflux systems involved in bacterial metal resistances. J Ind Microbiol 14 : 186 199.[CrossRef][PubMed]
216. Legatzki A,, Franke S,, Lucke S,, Hoffmann T,, Anton A,, Neumann D,, Nies DH . 2003. First step towards a quantitative model describing Czc-mediated heavy metal resistance in Ralstonia metallidurans. Biodegradation 14 : 153 168.[CrossRef][PubMed]
217. Nies DH . 2003. Efflux-mediated heavy metal resistance in prokaryotes. FEMS Microbiol Rev 27 : 313 339.[CrossRef]
218. Nies D,, Mergeay M,, Friedrich B,, Schlegel HG . 1987. Cloning of plasmid genes encoding resistance to cadmium, zinc, and cobalt in Alcaligenes eutrophus CH34. J Bacteriol 169 : 4865 4868.[CrossRef][PubMed]
219. Saier MH Jr,, Tam R,, Reizer A,, Reizer J . 1994. Two novel families of bacterial membrane proteins concerned with nodulation, cell division and transport. Mol Microbiol 11 : 841 847.[CrossRef][PubMed]
220. Diels L,, Dong Q,, van der Lelie D,, Baeyens W,, Mergeay M . 1995. The czc operon of Alcaligenes eutrophus CH34: from resistance mechanism to the removal of heavy metals. J Ind Microbiol 14 : 142 153.[CrossRef][PubMed]
221. Grosse C,, Anton A,, Hoffmann T,, Franke S,, Schleuder G,, Nies DH . 2004. Identification of a regulatory pathway that controls the heavy-metal resistance system Czc via promoter czcNp in Ralstonia metallidurans. Arch Microbiol 182 : 109 118.[CrossRef][PubMed]
222. Zoropogui A,, Gambarelli S,, Covès J . 2008. CzcE from Cupriavidus metallidurans CH34 is a copper-binding protein. Biochem Biophys Res Commun 365 : 735 739.[CrossRef][PubMed]
223. Scherer J,, Nies DH . 2009. CzcP is a novel efflux system contributing to transition metal resistance in Cupriavidus metallidurans CH34. Mol Microbiol 73 : 601 621.[CrossRef][PubMed]
224. von Rozycki T,, Nies DH . 2009. Cupriavidus metallidurans: evolution of a metal-resistant bacterium. Antonie van Leeuwenhoek 96 : 115 139.[CrossRef][PubMed]
225. Symmons MF,, Bokma E,, Koronakis E,, Hughes C,, Koronakis V . 2009. The assembled structure of a complete tripartite bacterial multidrug efflux pump. Proc Natl Acad Sci USA 106 : 7173 7178.[CrossRef][PubMed]
226. Murakami S,, Nakashima R,, Yamashita E,, Matsumoto T,, Yamaguchi A . 2006. Crystal structures of a multidrug transporter reveal a functionally rotating mechanism. Nature 443 : 173 179.[CrossRef][PubMed]
227. De Angelis F,, Lee JK,, O’Connell JD III,, Miercke LJ,, Verschueren KH,, Srinivasan V,, Bauvois C,, Govaerts C,, Robbins RA,, Ruysschaert JM,, Stroud RM,, Vandenbussche G . 2010. Metal-induced conformational changes in ZneB suggest an active role of membrane fusion proteins in efflux resistance systems. Proc Natl Acad Sci USA 107 : 11038 11043.[CrossRef][PubMed]
228. Pak JE,, Ekendé EN,, Kifle EG,, O’Connell JD III,, De Angelis F,, Tessema MB,, Derfoufi KM,, Robles-Colmenares Y,, Robbins RA,, Goormaghtigh E,, Vandenbussche G,, Stroud RM . 2013. Structures of intermediate transport states of ZneA, a Zn(II)/proton antiporter. Proc Natl Acad Sci USA 110 : 18484 18489.[CrossRef][PubMed]
229. Vaccaro BJ,, Lancaster WA,, Thorgersen MP,, Zane GM,, Younkin AD,, Kazakov AE,, Wetmore KM,, Deutschbauer A,, Arkin AP,, Novichkov PS,, Wall JD,, Adams MW . 2016. Novel metal cation resistance systems from mutant fitness analysis of denitrifying Pseudomonas stutzeri. Appl Environ Microbiol 82 : 6046 6056.[CrossRef][PubMed]
230. Djoko KY,, Ong CL,, Walker MJ,, McEwan AG . 2015. The role of copper and zinc toxicity in innate immune defense against bacterial pathogens. J Biol Chem 290 : 18954 18961.[CrossRef][PubMed]
231. 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]
232. Hao X,, Lüthje F,, Rønn R,, German NA,, Li X,, Huang F,, Kisaka J,, Huffman D,, Alwathnani HA,, Zhu YG,, Rensing C . 2016. A role for copper in protozoan grazing: two billion years selecting for bacterial copper resistance. Mol Microbiol 102 : 628 641.[CrossRef][PubMed]
233. Poole K . 2017. At the nexus of antibiotics and metals: the impact of Cu and Zn on antibiotic activity and resistance. Trends Microbiol 25 : 820 832.[CrossRef][PubMed]
234. Molmeret M,, Horn M,, Wagner M,, Santic M,, Abu Kwaik Y . 2005. Amoebae as training grounds for intracellular bacterial pathogens. Appl Environ Microbiol 71 : 20 28.[CrossRef][PubMed]