Skip to main content
Log in

Ion efflux systems involved in bacterial metal resistances

  • Published:
Journal of Industrial Microbiology

Summary

Studying metal ion resistances gives us important insights into environmental processes and provides an understanding of basic living processes. This review concentrates on bacterial efflux systems for inorganic metal cations and anions, which have generally been found as resistance systems from bacteria isolated from metal-polluted environments. The protein products of the genes involved are sometimes prototypes of new families of proteins or of important new branches of known families. Sometimes, a group of related proteins (and presumedly the underlying physiological function) has still to be defined. For example, the efflux of the inorganic metal anion arsenite is mediated by a membrane protein which functions alone in Gram-positive bacteria, but which requires an additional ATPase subunit in some Gram-negative bacteria. Resistance to Cd2+ and Zn2+ in Gram-positive bacteria is the result of a P-type efflux ATPase which is related to the copper transport P-type ATPases of bacteria and humans (defective in the human hereditary diseases Menkes' syndrome and Wilson's disease). In contrast, resistance to Zn2+, Ni2+, Co2+ and Cd2+ in Gram-negative bacteria is based on the action of proton-cation antiporters, members of a newly-recognized protein family that has been implicated in diverse functions such as metal resistance/nodulation of legumes/cell division (therefore, the family is called RND). Another new protein family, named CDF for ‘cation diffusion facilitator’ has as prototype the protein CzcD, which is a regulatory component of a cobalt-zinc-cadmium resistance determinant in the Gram-negative bacteriumAlcaligenes eutrophus. A family for the ChrA chromate resistance system in Gram-negative bacteria has still to be defined.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Bairoch, A. 1993. A possible mechanism for metal-ion induced DNA-protein dissociation in a family of prokaryotic transcriptional regulators. Nucl. Acids Res. 21: 2515.

    PubMed  Google Scholar 

  2. Bennett, R.L. and M.H. Malamy. 1970. Arsenate-resistant mutants ofEscherichia coli and phosphate transport. Biochem. Biophys. Res. Comm. 40: 490–503.

    Google Scholar 

  3. Bröer, S., G. Ji, A. Bröer and S. Silver. 1993. Arsenic efflux governed by the arsenic resistance determinant ofStaphylococcus aureus plasmid p1258. J. Bacteriol. 175: 3480–3485.

    PubMed  Google Scholar 

  4. Bucheder, F. and E. Broda. 1974. Energy-dependent zinc transport byEscherichia coli. Eur. J. Biochem. 45: 555–559.

    PubMed  Google Scholar 

  5. Bull, P.C. and D.W. Cox. 1994. Wilson disease and Menkes disease: new handles on heavy metal transport. Trends Genet. 10: 246–252.

    PubMed  Google Scholar 

  6. Bull, P.C., G.R. Thomas, J.M. Rommens, J.R. Forbes and D.W. Cox. 1993. The Wilson Disease gene is a putative copper transporting P-type ATPase similar to the Menkes gene. Nature (Genetics) 5: 327–337.

    Google Scholar 

  7. Cervantes, C., H. Ohtake, L. Chu, T.K. Misra and S. Silver. 1990. Cloning, nucleotide sequence, and expression of the chromate resistance determinant ofPseudomonas aeruginosa plasmid pUM505. J. Bacteriol. 172: 287–291.

    Google Scholar 

  8. Chelly, J., Z. Tumer, T. Tonnesen, A. Petterson, Y. Ishikawabrush, N. Tommerup, N. Horn and A.P. Monaco. 1993. Isolation of a candidate gene for Menkes' disease that encodes a potential heavy metal binding protein. Nature (Genetics) 3: 14–19.

    Google Scholar 

  9. Chen, C.-M., T.P. Misra, S. Silver and B.P. Rosen. 1986. Nucleotide sequence of the structural genes for an anion pump. J. Biol. Chem. 261: 15030–15038.

    PubMed  Google Scholar 

  10. Collard, J.-M., A. Provoost, S. Taghavi and M. Mergeay. 1993. A new type ofAlcaligenes eutrophus CH34 zinc resistance generated by mutations affecting regulation of thecnr cobalt-nickel resistance system. J. Bacteriol. 175: 779–794.

    PubMed  Google Scholar 

  11. Conklin, D.S., J.A. McMaster, M.R. Culbertson and C. Kung. 1992. COT1, a gene involved in cobalt accumulation inSaccharomyces cerevisiae. Mol. Cell Biol. 12: 3678–3688.

    PubMed  Google Scholar 

  12. Corbisier, P., G. Nuyts, G. Ji, M. Mergeay and S. Silver. 1993.luxAB gene fusions with the arsenic and cadmium resistance operons ofStaphylococcus aureus plasmid pl258. FEMS Microbiol. Lett. 110: 231–238.

    PubMed  Google Scholar 

  13. Dressler, C., U. Kues, D.H. Nies and B. Friedrich. 1991. Determinants encoding multiple metal resistance in newly isolated copper-resistant bacteria. Appl. Environ. Microbiol. 57: 3079–3085.

    Google Scholar 

  14. Elvin, C.M., C.M. Hardy and H. Rosenberg. 1987. Molecular studies on the phosphate inorganic transport system ofEscherichia coli. In: Phosphate Metabolism and Cellular Regulation in Micro-organisms (Torriani-Gorini, A., F.G. Rothmann, S. Silver, A. Wright and E. Yagil, eds), pp. 156–158, American Society for Microbiology, Washington, DC.

    Google Scholar 

  15. Eriksson, P.-O. and L. Sahlman. 1993.1H NMR studies of the mercuric ion binding protein MerP: sequential assignment secondary structure and global fold of oxidized MerP. J. Biomolec. NMR 3: 613–626.

    Google Scholar 

  16. Fagan, M.J. and M.H. Saier, Jr. 1994. P-type ATPases of eukaryotes and bacteria: sequence comparisons and construction of phylogenetic trees. J. Mol. Evol. 38: 57–99.

    PubMed  Google Scholar 

  17. Fath, M.J. and R. Kolter. 1993. ABC transporters: bacterial exporters. Microbiol. Rev. 57: 995–1017.

    PubMed  Google Scholar 

  18. Gladysheva, T.B., K.L. Oden and B.P. Rosen. 1994. The ArsC arsenate reductase of plasmid R773. Biochemistry 33: 7288–7293.

    PubMed  Google Scholar 

  19. Harold, F.M. and J.R. Baarda. 1966. Interaction of arsenate with phosphate-transport systems in wild type and mutantStreptococcus faecalis. J. Bacteriol. 91: 2257–2262.

    PubMed  Google Scholar 

  20. Hsu, C. M., P. Kaur, R.F. Steiner and B.P. Rosen. 1991. Substrate-induced dimerization of the ArsA protein, the catalytic component of an anion-translocating ATPase. J. Biol. Chem. 266: 2327–2332.

    PubMed  Google Scholar 

  21. Ji, G., E.A.E. Garber, L.G. Armes, C.-M. Chen, J.A. Fuchs and S. Silver. 1994. Arsenate reductase ofStaphylococcus aureus plasmid pl258: kinetics and spectroscopy. Biochemistry 33: 7294–7299.

    PubMed  Google Scholar 

  22. Ji, G. and S. Silver. 1992. Regulation and expression of the arsenic resistance operon fromStaphylococcus aureus plasmid pl258. J. Bacteriol. 174: 3684–3694.

    PubMed  Google Scholar 

  23. Ji, G. and S. Silver. 1992. Reduction of arsenate to arsenite by the ArsC protein of the arsenic resistance operon ofStaphylococcus aureus plasmid pl258. Proc. Natl. Acad. Sci. USA 89: 7974–7978.

    Google Scholar 

  24. Kaback, H.R. 1988. Site-directed mutagenesis and ion-gradient driven active transport: on the path of the proton. Annu. Rev. Physiol. 50:243–256.

    PubMed  Google Scholar 

  25. Kamizomo, A., M. Nishizawa, Y. Teranishi, K. Murata and A. Kimura. 1989. Identification of a gene conferring resistance to zinc and cadmium in the yeastSaccharomyces cerevisiae. Mol. Gen. Genet. 219: 161–167.

    PubMed  Google Scholar 

  26. Karkaria, C.E. and B.P. Rosen. 1991. Trinitrophenyl-ATP binding to the ArsA protein—the catalytic subunit of an anion pump. Arch. Biochem. Biophys. 288: 107–111.

    PubMed  Google Scholar 

  27. Kaur, P. and B.P. Rosen. 1992. Mutagenesis of the C-Terminal nucleotide-binding site of an anion-translocating ATPase. J. Biol. Chem. 267: 19272–19277.

    PubMed  Google Scholar 

  28. Kaur, P. and B.P. Rosen. 1993. Complementation between nucleotide binding domains in an anion-translocating ATPase. J. Bacteriol. 175: 351–357.

    PubMed  Google Scholar 

  29. Kaur, P. and B.P. Rosen. 1994.in vitro assembly of an anionstimulated ATPase from peptide fragments.

  30. Kiel, J.A.K.W., J.M. Boels, G. Beldman and G. Venema. 1991. TheglgB gene from the thermophileBacillus caldolyticus encodes a thermolabile branching enzyme. J. DNA Seq. Map 3: 221–232.

    Google Scholar 

  31. Kiel, J.A.K.W., J. M. Boels, G. Beldman and G. Venema. 1992. Molecular cloning and nucleotide sequence of the glycogen branching enzyme gene (glgB) fromBacillus stearothermophilus and expression inEscherichia coli andBacillus subtilis. Mol. Gen. Genet. 230: 136–144.

    Google Scholar 

  32. Krebs, M.P. and H.G. Khorana. 1993. Mechanism of light-dependent proton translocation by bacteriorhodopsin. J. Bacteriol. 175: 1555–1560.

    PubMed  Google Scholar 

  33. Lebrun, M., A. Audurier and P. Cossart. 1994a. Plasmid-borne cadmium resistance genes inListeria monocytogenes are similar tocadA andcadC ofStaphylococcus aureus and are induced by cadmium. J. Bacteriol. 176: 3040–3048.

    PubMed  Google Scholar 

  34. Lebrun, M., A. Audurier and P. Cossart. 1994b. Plasmid-borne cadmium resistance genes inListeria monocytogenes are present on Tn5422 a novel transposon closely related to Tn917. J Bacteriol. 176:3049–3061.

    PubMed  Google Scholar 

  35. Lewis, K. 1994. Multidrug resistance pumps in bacteria: variations on a theme. Trends Biochem. Sci. 19: 119–123.

    PubMed  Google Scholar 

  36. Liesegang, H., K. Lemke, R.A. Siddiqui and H.-G. Schlegel. 1993. Characterization of the inducible nickel and cobalt resistance determinant cnr from pMOL28 ofAlcaligenes eutrophus CH34. J. Bacteriol. 175: 767–778.

    PubMed  Google Scholar 

  37. Luecke, H. and F.A. Quiocho. 1990. High specificity of a phosphate transport protein determined by hydrogen bonds. Nature Lond. 347: 402–406.

    PubMed  Google Scholar 

  38. Ma, D., D.N. Cook, M. Albertie, N.G. Pon, H. Nikaido and J.E. Hearst. 1993. Molecular cloning ofacrA andacrE genes ofEscherichia coli. J. Bacteriol. 175: 6299–6313.

    PubMed  Google Scholar 

  39. Maloney, P.C., S.V. Ambudkar, V. Anantharam, L.A. Sonna and Varadhachary. 1990. Anion-exchange mechanisms in bacteria. Microbiol. Rev. 54: 1–17.

    PubMed  Google Scholar 

  40. Marger, M.D. and Saier, M.H. 1993. A major superfamily of transmembrane facilitators catalyzing uniport, symport and antiport. Trends Biochem. Sci. 18: 13–20.

    PubMed  Google Scholar 

  41. Mercer, J.F.B., J. Livingston, B. Hall, J.A. Paynter, C. Begy, S. Chandrasekharappa, P. Lockhart, A. Grimes, M. Bhave, D. Siemieniak and T.W. Glover. 1993. Isolation of a partial candidate gene for Menkes disease by positional cloning. Nature (Genetics) 3: 20–25.

    Google Scholar 

  42. Mercer, J.F.B., A. Grimes, L. Ambrosini, P. Lockhart, J.A. Paynter, H. Dierick and T.W. Glover. 1994. Mutations in the murine homologue of the Menkes gene in dappled and blotchy mice. Nature (Genetics) 6: 374–378.

    Google Scholar 

  43. Mergeay, M., D. Nies, H.G. Schlegel, J. Gerits, P. Charles and F. VanGijsegem. 1985.Alcaligenes eutrophus CH34 is a facultative chemolithotroph with plasmid-bound resistance to heavy metals. J. Bacteriol. 162: 328–334.

    PubMed  Google Scholar 

  44. Mobley, H.L.T. and B.P. Rosen. 1982. Energetics of plasmidmediated arsenate resistance inEscherichia coli. Proc. Natl Acad. Sci. USA 79: 6119–6122.

    PubMed  Google Scholar 

  45. Nakata, A.M., M. Amemura, K. Makimo and H. Shinegawa. 1987. Genetic and biochemical analysis of the phosphate-specific transport system inEscherichia coli. In: Phosphate Metabolism and Cellular Regulation in Microorganisms (Torriani-Gorini, A., F.G. Rothmann, S. Silver, A. Wright and E. Yagil, eds), pp. 150–155, American Society for Microbiology, Washington, DC.

    Google Scholar 

  46. Nies, A., D.H. Nies and S. Silver. 1989. Cloning and expression of plasmid genes encoding resistances to chromate and cobalt inAlcaligenes eutrophus. J. Bacteriol. 171: 5065–5070.

    PubMed  Google Scholar 

  47. Nies, A., D.H. Nies and S. Silver. 1990. Nucelotide sequence and expression of a plasmid-encoded chromate resistance determinant fromAlcaligenes eutrophus. J. Biol. Chem. 265: 5648–5653.

    PubMed  Google Scholar 

  48. Nies, D.H. 1992a. Resistance to cadmium, cobalt, zinc, and nickel in microbes. Plasmid 27: 17–28.

    PubMed  Google Scholar 

  49. Nies D.H. 1992b. CzcR and CzcD, gene products affecting regulation of resistance to cobalt, zinc and cadmium (czc system) inAlcaligenes eutrophus. J. Bacteriol. 174: 8102–8110.

    PubMed  Google Scholar 

  50. (Reference deleted in proof.)

  51. Nies, D.H., M. Mergeay, B. Friedrich and H.G. Schlegel. 1987. Cloning of the plasmid coded resistance to cobalt, zinc, and cadmium fromAlcaligenes eutrophus CH34. J. Bacteriol. 167: 4865–4868.

    Google Scholar 

  52. Nies, D.H., A. Nies, L. Chu and S. Silver. 1989. Expression and nucelotide sequence of a plasmid-determined divalent cation efflux system fromAlcaligenes eutrophus. Proc. Natl Acad. Sci. USA 86: 7351–7355.

    PubMed  Google Scholar 

  53. Nies, D.H. and S. Silver. 1989. Metal ion uptake by plasmidfree metal-sensitiveAlcaligenes eutrophus strain. J. Bacteriol. 171: 4073–4075.

    PubMed  Google Scholar 

  54. Nies, D.H. and S. Silver. 1989. Plasmid-determined inducible efflux is responsible for resistance to cadmium, zinc and cobalt inAlcaligenes eutrophus. J. Bacteriol. 171: 896–900.

    PubMed  Google Scholar 

  55. Novick, R.P. and C. Roth. 1968. Plasmid-linked resistance to inorganic salts inStaphylococcus aureus. J. Bacteriol. 95: 1335–1342.

    PubMed  Google Scholar 

  56. Novick, R.P., R.P. Murphy, T.J. Gryczan, E. Barone and I. Edelman. 1979. Penicillinase plasmids ofStaphylococcus aureus: restriction-deletion maps. Plasmid 2: 109–129.

    PubMed  Google Scholar 

  57. Nucifora, G., L. Chu, T.K. Misra and S. Silver. 1989. Cadmium resistance fromStaphylococcus aureus plasmid, pl258cadA results from a cadmium-efflux ATPase. Proc. Natl Acad. Sci. USA 86: 3544–3548.

    PubMed  Google Scholar 

  58. Oden, K.L., T.B. Gladysheva and B.P. Rosen. 1994. Arsenate reduction by the plasmid-encoded ArsC protein is coupled to glutathione. Mol. Microbiol. 12: 301–306.

    PubMed  Google Scholar 

  59. Odermatt, A., H. Suter, R. Krapf and M. Solioz. 1993. Primary structure of two P-type ATPases involved in copper homeostasis inEnterococcus hirae. J. Biol. Chem. 268: 12775–12777.

    PubMed  Google Scholar 

  60. Ohtake, H., C. Cervantes and S. Silver. 1987. Decreased chromate uptake inPseudomonas fluorescens carrying a chromate resistance plasmid. J. Bacteriol. 169: 3853–3856.

    PubMed  Google Scholar 

  61. Perry, R.D. and S. Silver. 1982. Cadmium and manganese transport inStaphylococcus aureus membrane vesicles. J. Bacteriol. 150: 973–976.

    PubMed  Google Scholar 

  62. Poole, K. and R.E.W. Hancock. 1984. Phosphate transport inPseudomonas aeruginosa. Eur. J. Biochem. 144: 607–612.

    PubMed  Google Scholar 

  63. Poole, K., K. Krebes, C. McNally and S. Neshat. 1993. Multiple antibiotic resistance inPseudomonas aeruginosa: evidence for involvement of an efflux operon. J. Bacteriol. 175: 7363–7372.

    PubMed  Google Scholar 

  64. Rao, N.N. and A. Torriani. 1990. Molecular aspects of phosphate transport inEscherichia coli. Mol. Microbiol. 4: 1083–1090.

    PubMed  Google Scholar 

  65. Rosen, B.P. and M.G. Borbolla. 1984. A plasmid-encoded arsenite pump produces arsenite resistance inEscherichia coli. Biochem. Biophys. Res. Comm. 124: 760–765.

    PubMed  Google Scholar 

  66. Rosen, B.P., U. Weigel, C. Karkaria and P. Gangola. 1988. Molecular characterization of an anion pump. The arsA gene product is an arsenite (antimonate)-stimulated ATPase. J. Biol. Chem. 263: 3067–3070.

    PubMed  Google Scholar 

  67. Rosenberg, H. 1987. Phosphate transport in prokaryotes. In: Ion Transport in Prokaryotes (Rosen, B.P. and S. Silver, eds.), pp. 205–248, Academic Press, San Diego.

    Google Scholar 

  68. Rosenberg, H., R. G. Gerdes and K. Chegwidden. 1977. Two systems for the uptake of phosphate inEscherichia coli. J. Bacteriol. 131: 505–511.

    PubMed  Google Scholar 

  69. Rosenstein, R., A. Perschel, B. Wieland and F. Götz. 1992. Expression and regulation of the antimonite, arsenite and arsenate resistance operon ofStaphylococcus xylosus plasmid pSX267. J. Bacteriol. 174: 3676–3683.

    PubMed  Google Scholar 

  70. Sahlman, L. and E.G. Skärfstad. 1993. Mercuric ion binding abilities of MerP variants containing only one cysteine. Biochem. Biophys. Res. Commun. 196: 583–588.

    PubMed  Google Scholar 

  71. Saier, M. H., Jr. 1994. Computer-aided analysis of transport protein sequences: gleaning evidence concerning function, structure, biogenesis, and evolution Microbiol. Rev. 58: 71–93.

    PubMed  Google Scholar 

  72. Saier, M.H., Jr., R. Tam, A. Reizer and J. Reizer. 1994. Two novel families of bacterial membrane proteins concerned with nodulation, cell division and transport. Mol. Microbiol. 11: 841–847.

    PubMed  Google Scholar 

  73. San Francisco, M.J.D., L.S. Tisa and B.P. Rosen. 1989. Identification of the membrane component of the anion pump encoded by the arsenical resistance operon of R-factor R773. Mol. Microbiol. 3: 15–21.

    PubMed  Google Scholar 

  74. Schmidt, T. and H.G. Schlegel. 1994. Combined nickel-cobaltcadmium resistance encoded by thencc locus ofAlcaligenes xylosoxidans 31A. J. Bacteriol. 176: 7045–7054.

    PubMed  Google Scholar 

  75. Sensfuss, C. and H.G. Schlegel. 1988. Plasmid pMOL28-encoded resistance to nickel is due to specific efflux. FEMS Microbiol. Lett. 55: 295–298.

    Google Scholar 

  76. Siddiqui, R.A. and H.G. Schlegel. 1987. Plasmid pMOL28 mediated inducible nickel resistance inAlcaligenes eutrophus CH34. FEMS Microbiol. Lett. 43: 9–13.

    Google Scholar 

  77. Siddiqui, R.A., K. Benthin and H.G. Schlegel. 1989. Cloning of pMOL28-encoded nickel resistance genes and expression of the genes inAlcaligenes eutrophus andPseudomonas spp. J. Bacteriol. 171: 5071–5078.

    PubMed  Google Scholar 

  78. Silver, S., K. Budd, K.M. Leahy, W.V. Shaw, D. Hammond, R.P. Novick, G.R. Willsky, M.H. Malamy and H. Rosenberg. 1981. Inducible plasmid-determined resistance to arsenate, arsenite, and antimony (III) inEscherichia coli andStaphylococcus aureus. J. Bacteriol. 146: 983–996.

    PubMed  Google Scholar 

  79. Silver, S., G. Ji, S. Bröer, S. Dey, D. Dou and B.P. Rosen. 1993. Orphan enzyme or patriarch of a new tribe: the arsenic resistance ATPase of bacterial plasmids. Mol. Microbiol. 8: 637–642.

    PubMed  Google Scholar 

  80. Silver, S. and D. Keach. 1982. Energy-dependent arsenate efflux: the mechanism of plasmid-mediated resistance. Proc. Natl Acad. Sci. USA 79: 6114–6118.

    PubMed  Google Scholar 

  81. Silver, S., G. Nucifora, L. Chu and T.K. Misra. 1989. Bacterial resistance ATPases: primary pumps for exporting toxic cations and anions. Trends Biochem. Sci. 14: 76–80.

    PubMed  Google Scholar 

  82. Silver, S., G. Nucifora and L.T. Phung. 1993. Human Menkes X-chromosome disease and the staphylococcal cadmium-resistance ATPase: a remarkable similarity in protein sequences. Mol. Microbiol. 10: 7–12.

    PubMed  Google Scholar 

  83. Silver, S. and M. Walderhaug. 1992. Gene regulation of plasmid-and chromosomal-determined inorganic ion transport in bacteria. Microbiol. Rev. 56: 195–228.

    PubMed  Google Scholar 

  84. Surin, B.P., G.B. Cox and H. Rosenberg 1987. Molecular studies on the phosphate-specific transport system ofEscherichia coli In: Phosphate Metabolism and Cellular Regulation in Microorganisms (Torriani-Gorini, A., F.G. Rothmann, S. Silver, A. Wright and E. Yagil, eds), pp. 145–149, American Society for Microbiology, Washington, DC.

    Google Scholar 

  85. Tisa, L.S. and B.P. Rosen. 1900. Molecular characterization of an anion pump. The ArsB protein is the membrane anchor for the ArsA protein. J. Biol. Chem. 265: 190–194.

    Google Scholar 

  86. Torriani, A. 1990. From cell membranes to nucleotides: the phosphate regulon inEscherichia coli. Bioessays 12: 493–507.

    PubMed  Google Scholar 

  87. Tsai, K.-J. and A.L. Linet. 1993. Formation of a phosphorylated enzyme intermediate by thecadA Cd2+-ATPase. Arch. Biochem. Biophys. 305: 267–270.

    PubMed  Google Scholar 

  88. Tsai, K.-J., K.P. Yoon and A.R. Lynn. 1992. ATP-dependent cadmium transport by thecadA cadmium resistance determinant in everted membrane vesicles ofBacillus subtilis. J. Bacteriol. 174: 116–121.

    PubMed  Google Scholar 

  89. Turner, R.J., Y. Hou, J.H. Weiner and D.E. Taylor. 1992. The arsenical ATPase efflux pump mediates tellurite resistance. J. Bacteriol. 174: 3092–3094.

    PubMed  Google Scholar 

  90. Tynecka, Z., Z. Gos and J. Zajac. 1981a. Reduced cadmium transport determined by a plasmid inStaphylococcus aureus. J. Bacteriol. 147: 305–312.

    PubMed  Google Scholar 

  91. Tynecka, Z., Z. Gos and J. Zajac. 1981b. Energy-dependent efflux of cadmium coded by a plasmid resistance determinant inStaphylococcus aureus. J. Bacteriol. 147: 313–319.

    PubMed  Google Scholar 

  92. Vulpe, C., B. Levinson, S. Whitney, S. Packman and J. Gitschier. 1993. Isolation of a candidate gene for Menkes disease and evidence that it encodes a copper-transporting ATPase. Nature (Genetics) 3: 7–13.

    Google Scholar 

  93. Wanner, B.L. 1990. Phosphate assimilation and its control of gene expression inEscherichia coli. In: The Molecular Basis of Bacterial Metabolism (Hauska, G. and R. Thauer, eds), pp. 152–163, Springer Verlag, Heidelberg.

    Google Scholar 

  94. Weiss, A.A., S. Silver and T.G. Kinscherf. 1978. Cation transport alteration associated with plasmid-determined resistance to cadmium inStaphylococcus aureus. Antimicrob. Agents Chemother. 14: 856–865.

    PubMed  Google Scholar 

  95. Willksy, G.R. and M.H. Malamy. 1980a. Characterization of two genetically separable inorganic phosphate transport systems inEscherichia coli. J. Bacteriol. 144: 356–365.

    PubMed  Google Scholar 

  96. Willsky, G.R. and M.H. Malamy. 1980b. Effect of arsenate on inorganic phosphate transport inEscherichia coli. J. Bacteriol. 144: 366–374.

    PubMed  Google Scholar 

  97. Wu, J. and B.P. Rosen. 1991. The ArsR protein is a trans-acting regulatory protein. Molec. Microbiol. 5: 1331–1336.

    Google Scholar 

  98. Wu, J. and B.P. Rosen. 1993a. The arsD gene encodes a second trans-acting regulatory protein of the plasmid-encoded arsenical resistance operon. Mol. Microbiol. 8: 615–623.

    PubMed  Google Scholar 

  99. Wu, J. and B.P. Rosen. 1993b. Metalloregulated expression of thears operon. J. Biol. Chem. 268: 52–58.

    PubMed  Google Scholar 

  100. Wu, J., L.S. Tisa and B.P. Rosen. 1992. Membrane topology of the ArsB protein, the membrane subunit of an anion-translocating ATPase. J. Biol. Chem. 267: 12570–12576.

    PubMed  Google Scholar 

  101. Yoon, K.P., T.K. Misra and S. Silver. 1991. Regulation of the cadA cadmium resistance determinant ofStaphylococcus aureus. J. Bacteriol. 173: 7643–7649.

    PubMed  Google Scholar 

  102. Yoon, K.P. and S. Silver. 1991. A second gene in theStaphylococcus aureus cadA cadmium resistance determinant. J. Bacteriol. 173: 7636–7642.

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Nies, D.H., Silver, S. Ion efflux systems involved in bacterial metal resistances. Journal of Industrial Microbiology 14, 186–199 (1995). https://doi.org/10.1007/BF01569902

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01569902

Key words

Navigation