Chapter 11 : Metal Resistance Loci of Bacterial Plasmids

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This chapter provides an introduction to metallobiology, brief descriptions of the well-studied plasmidcoded metal resistances, and a short survey of the genetic and biochemical connections between metals and antibiotic resistances. Many genes in bacterial plasmid-borne metal resistance systems are homologous to those of the chromosomal homeostasis systems. Cobalt, nickel, and zinc are all essential metals, and all but zinc are redox active. Lead and cadmium have no beneficial biological functions and are both quite toxic. Operons conferring single and multiple resistances to various subsets of these four transition metals and the main group heavy metal, lead, are based on several distinct types of efflux pumps. In there are three metal resistance loci on pMOL28: a transposon conferring resistance to mercury, merTPADE, and two nontransposable loci conferring resistance to chromate and to cobalt and nickel. Although heavy metal resistances in bacteria first appeared to be largely plasmid encoded, genome sequencing has revealed that homologs of transition metal resistance genes and their regulators abound in all prokaryotic chromosomes, most likely for managing the cell’s use of their beneficial and essential metal relatives. It is a known fact that bacteria isolated from metal-impacted environments typically carry several metal resistances on large conjugative plasmids, suggesting that this genetic arrangement has selective advantage beyond that afforded by expression of related chromosomal loci.

Citation: Summers A. 2005. Metal Resistance Loci of Bacterial Plasmids, p 165-173. In White D, Alekshun M, McDermott P (ed), Frontiers in Antimicrobial Resistance. ASM Press, Washington, DC. doi: 10.1128/9781555817572.ch11
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1. Aarestrup, F. M.,, H. Hasman,, L. B. Jensen,, M. Moreno,, I. A. Herrero,, L. Dominguez,, M. Finn,, and A. Franklin. 2002. Antimicrobial resistance among enterococci from pigs in three European countries. Appl. Environ. Microbiol. 68: 4127 4129.
2. Banci, L.,, I. Bertini,, R. Del Conte,, J. Markey,, and F. J. Ruiz- Duenas. 2001. Copper trafficking: the solution structure of Bacillus subtilis CopZ. Biochemistry 40: 15660 15668.
3. Barkay, T.,, S. M. Miller,, and A. O. Summers. 2003. Bacterial mercury resistance from atoms to ecosystems. FEMS Microbiol. Rev. 27: 355 384.
4. Bender, C. L.,, and D. A. Cooksey. 1986. Indigenous plasmids in Pseudomonas syringae pv. tomato: conjugative transfer and role in copper resistance. J. Bacteriol. 165: 534 541.
5. Besnard, E.,, C. Chenu,, and M. Robert. 2001. Influence of organic amendments on copper distribution among particle-size and density fractions in Champagne vineyard soils. Environ. Pollut. 112: 329 337.
6. Borremans, B.,, J. L. Hobman,, A. Provoost,, N. L. Brown,, and D. van de Lelie. 2001. Cloning and functional analysis of the pbr lead resistance determinant of Ralstonia metallidurans CH34. J. Bacteriol. 183: 5651 5658.
7. Brown, N. L.,, J. V. Stoyanov,, S. P. Kidd,, and J. L. Hobman. 2003. The MerR family of transcriptional regulators. FEMS Microbiol. Rev. 27: 145 163.
8. Bull, P. C.,, and D. W. Cox. 1994. Wilson disease and Menkes disease: new handles on heavy-metal transport. Trends Genet. 10: 246 252.
9. Busenlehner, L. S.,, M. A. Pennella,, and D. P. Giedroc. 2003. The SmtB/ArsR family of metalloregulatory transcriptional repressors: structural insights into prokaryotic metal resistance. FEMS Microbiol. Rev. 27: 131 143.
10. Canady, R. A.,, C. S. Rabe,, and K. Gan. 1996. Toxicological Profile for Mercury (update). U.S. Dept. of Health and Human Services, Public Health Service Agency for Toxic Substances and Disease Registry, Atlanta, Ga.
11. Canovas, D.,, I. Cases,, and V. de Lorenzo. 2003. Heavy metal tolerance and metal homeostasis in Pseudomonas putida as revealed by complete genome analysis. Environ. Microbiol. 5: 1242 1256.
12. Chen, C. A.,, and J. A. Cowan. 2002. In vivo cleavage of a target RNA by copper kanamycin A. Direct observation by a fluorescence assay. Chem. Commun. (Camb): 196 197.
13. Cooksey, D. A.,, and H. R. Azad. 1992. Accumulation of copper and other metals by copper-resistant plant pathogenic and saprophytic pseudomonads. Appl. Environ. Microbiol. 58: 274 278.
14. Dyllick-Brenzinger, M.,, M. Liu,, T. L. Winstone,, D. E. Taylor,, and R. J. Turner. 2000. The role of cysteine residues in tellurite resistance mediated by the TehAB determinant. Biochem. Biophys. Res. Commun. 277: 394 400.
15. Edmonds, M. S.,, O. A. Izquierdo,, and D. H. Baker. 1985. Feed additive studies with newly weaned pigs: efficacy of supplemental copper, antibiotics and organic acids. J. Anim. Sci. 60: 462 469.
16. Finney, L. A.,, and T. V. O’Halloran. 2003. Transition metal speciation in the cell: insights from the chemistry of metal ion receptors. Science 300: 931 936.
17. Frausto de Silva, J. J. R.,, and R. J. P. Williams. 1991. The Biological Chemistry of the Elements: the Inorganic Chemistry of Life. Clarendon Press, Oxford, United Kingdom.
18. Gallagher, D. L.,, K. M. Johnston,, and A. M. Dietrich. 2001. Fate and transport of copper-based crop protectants in plasticulture runoff and the impact of sedimentation as a best management practice. Water Res. 35: 2984 2994.
19. Goldberg, M.,, T. Pribyl,, S. Juhnke,, and D. H. Nies. 1999. Energetics and topology of CzcA, a cation/proton antiporter of the resistance-nodulation-cell division protein family. J. Biol. Chem. 274: 26065 26070.
20. Hasman, H.,, and F. M. Aarestrup. 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.
21. Iqbal, M. S.,, A. R. Ahmad,, M. Sabir,, and S. M. Asad. 1999. Preparation, characterization and biological evaluation of copper( II) and zinc(II) complexes with cephalexin. J. Pharm. Pharmacol. 51: 371 375.
22. Jezowska-Bojczuk, M.,, W. Szczepanik,, W. Lesniak,, J. Ciesiolka,, J. Wrzesinski,, and W. Bal. 2002. DNA and RNA damage by Cu(II)-amikacin complex. Eur. J. Biochem. 269: 5547 5556.
23. Juhnke, S.,, N. Peitzsch,, N. Hubener,, C. Grosse,, and D. H. Nies. 2002. New genes involved in chromate resistance in Ralstonia metallidurans strain CH34. Arch. Microbiol. 179: 15 25.
24. Lehnherr, H.,, and M. Yarmolinsky. 1995. Addiction protein Phd of plasmid prophage P1 is a substrate of the ClpXp serineprotease of Escherichia coli. Proc. Natl. Acad. Sci. USA 92: 3274 3277.
25. Lesniak, W.,, W. R. Harris,, J. Y. Kravitz,, J. Schacht,, and V. L. Pecoraro. 2003. Solution chemistry of copper(II)-gentamicin complexes: relevance to metal-related aminoglycoside toxicity. Inorg. Chem. 42: 1420 1429.
26. Li, S.,, B. P. Rosen,, M. I. Borges-Walmsley,, and A. R. Walmsley. 2002. Evidence for cooperativity between the four binding sites of the dimeric ArsD, and As(III)-responsive transcriptional regulator. J. Biol. Chem. 277: 25992 256002.
27. Liebert, C. A.,, R. M. Hall,, and A. O. Summers. 1999. Transposon Tn 21, flagship of the floating genome. Microbiol. Mol. Biol. Rev. 63: 507 522.
28. Liu, M.,, R. J. Turner,, T. L. Winstone,, A. Saetre,, M. Dyllick- Brenzinger,, G. Jickling,, L. W. Tari,, J. H. Weiner,, and D. E. Taylor. 2000. Escherichia coli TehB requires S-adenosylmethionine as a cofactor to mediate tellurite resistance. J. Bacteriol. 182: 6509 6513.
29. McEwen, S. A.,, and P. J. Fedorka-Cray. 2002. Antimicrobial use and resistance in animals. Clin. Infect. Dis. 34: S93 S106.
30. Mergeay, M.,, S. Monchy,, T. Vallaeys,, V. Auquier,, A. Benotmane,, P. Bertin,, S. Taghavi,, J. Dunn,, D. van der Lelie,, and R. Wattiez. 2003. Ralstonia metallidurans, a bacterium specifically adapted to toxic metals: towards a catalogue of metal-responsive genes. FEMS Microbiol. Rev. 27: 385 410.
31. Miller, M. A.,, and S. A. Harmon. 1967. Genetic association of determinants controlling resistance to mercuric chloride, production of penicillinase and synthesis of methionine in Staphylococcus aureus. Nature 215: 531 532.
32. Moore, B. 1960. A new screen test and selective medium for the rapid detection of epidemic strains of Staphylococcus aureus. Lancet ii: 453 458.
33. Mukhopadhyay, R.,, and B. P. Rosen. 2002. Arsenate reductases in prokaryotes and eukaryotes. Environ. Health Perspect. 110: 745 748.
34. Mukhopadhyay, R.,, B. P. Rosen,, L. T. Phung,, and S. Silver. 2002. Microbial arsenic: from geocycles to genes and enzymes. FEMS Microbiol. Rev. 26: 311 325.
35. Munson, G. P.,, D. L. Lam,, F. W. Outten,, and T. V. O’Halloran. 2000. Identification of a copper-responsive two-component system on the chromosome of Escherichia coli K-12. J. Bacteriol. 182: 5864 5871.
36. Nies, D. H. 2003. Efflux-mediated heavy metal resistance in prokaryotes. FEMS Microbiol. Rev. 27: 313 339.
37. Nies, D. H., 2004. Essential and toxic effects of elements on microorganisms, p. 257 276. In K. Anke,, M. Ihnat,, and M. Stoeppler (ed.), Metals and Their Compounds in the Environment. Wiley-VCH, Weinheim, Germany.
38. Novick, R. P.,, and C. Roth. 1968. Plasmid resistance to inorganic salts in Staphylococcus aureus. J. Bacteriol. 95: 1335 1342.
39. Nucifora, G.,, L. Chu,, T. K. Misra,, and S. Silver. 1989. Cadmium resistance from Staphylococcus aureus plasmid pI258 cadA gene results from a cadmium-efflux ATPase. Proc. Natl. Acad. Sci. USA 86: 3544 3548.
40. Outten, C. E.,, and T. V. O’Halloran. 2001. Femtomolar sensitivity of metalloregulatory proteins controlling zinc homeostasis. Science 292: 2488 2492.
41. Outten, F. W.,, D. L. Huffman,, J. A. Hale,, and T. V. O’Halloran. 2001. The independent cue and cus systems confer copper tolerance during aerobic and anaerobic growth in Escherichia coli. J. Biol. Chem. 276: 30670 30677.
42. Outten, F. W.,, C. E. Outten,, J. Hale,, and T. V. O’Halloran. 2000. Transcriptional activation of an Escherichia coli copper efflux regulon by the chromosomal MerR homolog, CueR. J. Biol. Chem. 275: 31024 31029.
43. Randall, L. P.,, and M. J. Woodward. 2002. The multiple antibiotic resistance (mar) locus and its significance. Res. Vet. Sci. 72: 87 93.
44. Rensing, C.,, and G. Grass. 2003. Escherichia coli mechanisms of copper homeostasis in a changing environment. FEMS Microbiol. Rev. 27: 197 213.
45. Richmond, M. H.,, and M. John. 1964. Co-transduction by a staphylococcal phage of the genes responsible for penicillinase synthesis and resistance to mercury salts. Nature 202: 1360 1361.
46. Saltikov, C. W.,, A. Cifuentes,, K. Venkateswaran,, and D. K. Newman. 2003. The ars detoxification system is advantageous but not required for As(V) respiration by the genetically tractable Shewanella species strain ANA-3. Appl. Environ. Microbiol. 69: 2800 2809.
47. Saltikov, C. W.,, and D. K. Newman. 2003. Genetic identification of a respiratory arsenate reductase. Proc. Natl. Acad. Sci. USA 100: 10983 10988.
48. Schluter, A.,, H. Heuer,, R. Szczepanowski,, L. J. Forney,, C. M. Thomas,, A. Puhler,, and E. M. Top. 2003. The 64,508 bp IncP- 1β antibiotic multiresistance plasmid pB10 isolated from a waste-water treatment plant provides evidence for recombination between members of different branches of the IncP-1β group. Microbiology 149: 3139 3153.
49. Silver, S. 2003. Bacterial silver resistance: molecular biology and uses and misuses of silver compounds. FEMS Microbiol. Rev. 27: 341 353.
50. Solioz, M.,, and J. V. Stoyanov. 2003. Copper homeostasis in Enterococcus hirae. FEMS Microbiol. Rev. 27: 183 195.
51. Szczepanik, W.,, E. Dworniczek,, J. Ciesiolka,, J. Wrzesinski,, J. Skala,, and M. Jezowska-Bojczuk. 2003. In vitro oxidative activity of cupric complexes of kanamycin A in comparison to in vivo bactericidal efficacy. J. Inorg. Biochem. 94: 355 364.
52. Taylor, D. E. 1999. Bacterial tellurite resistance. Trends Microbiol. 7: 111 115.
53. Taylor, D. E.,, M. Rooker,, M. Keelan,, L. K. Ng,, I. Martin,, N. T. Perna,, N. T. Burland,, and F. R. Blattner. 2002. Genomic variability of O islands encoding tellurite resistance in enterohemorrhagic Escherichia coli O157:H7 isolates. J. Bacteriol. 184: 4690 4698.
54. Thorburn, A. L. 1983. Paul Ehrlich: pioneer of chemotherapy and cure by arsenic (1854-1915). Br. J. Vener. Dis. 59: 404 405.
55. Tsai, K. J.,, Y. F. Lin,, M. D. Wong,, H. H. C. Yang,, H. L. Fu,, and B. P. Rosen. 2002. Membrane topolocy of the pI258 CadA Cd(II)/Pb(II)/Zn(II)-translocating P-type ATPase. J. Bionerg. Biomembr. 34: 147 156.
56. Vidaver, A. K. 2002. Uses of antimicrobials in plant agriculture. Clin. Infect. Dis. 34: S107 S110.
57. Williams, J. R.,, A. G. Morgan,, D. A. Rouch,, N. L. Brown,, and B. T. Lee. 1993. Copper-resistant enteric bacteria from United Kingdom and Australian piggeries. Appl. Environ. Microbiol. 59: 2531 2537.
58. Wong, M. D.,, B. Fan,, and B. P. Rosen,. 2003. Bacterial transport ATPases for monovalent, divalent and trivalent soft metal ions, p. 159 178. In J. Kaplan,, Y. Wada,, and M. Futai (ed.), Ion- Pumping ATPases: Biochemisry, Cell Biology and Pathophysiology. Wiley-VCH, Weinhein, Germany.


Generic image for table
Table 1

Biologically useful heavy metal and metalloid elements

Data from references and .

Vanadium and tungsten are also essential for nitrogen fixation in some bacteria.

Citation: Summers A. 2005. Metal Resistance Loci of Bacterial Plasmids, p 165-173. In White D, Alekshun M, McDermott P (ed), Frontiers in Antimicrobial Resistance. ASM Press, Washington, DC. doi: 10.1128/9781555817572.ch11
Generic image for table
Table 2

Plasmid-determined heavy metal and metalloid resistance systems

Citation: Summers A. 2005. Metal Resistance Loci of Bacterial Plasmids, p 165-173. In White D, Alekshun M, McDermott P (ed), Frontiers in Antimicrobial Resistance. ASM Press, Washington, DC. doi: 10.1128/9781555817572.ch11

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