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Bacterial zinc transporters and regulators

  • Klaus Hantke
Chapter

Abstract

Zn2+ homeostasis in bacteria is achieved by export systems and uptake systems which are separately regulated by their own regulators. Three types of Zn2+ export systems that protect cells from high toxic concentrations of Zn2+ have been identified: RND multi-drug efflux transporters, P-type ATPases, and cation-diffusion facilitators. The RND type exporters for Zn2+ are only found in a few gram-negative bacteria; they allow a very efficient export across the cytoplasmic membrane and the outer membrane of the cell. P-type ATPases and cation-diffusion facilitators belong to protein families that are also found in eukaryotes. The exporters are regulated in bacteria by MerR-like repressor/activators or by ArsR-like repressors. For the high-affinity uptake of Zn2+, several bindingprotein-dependent ABC transporters belonging to one class have been identified in different bacteria. Zn2+ ABC transporters are regulated by Zur repressors, which belong to the Fur protein family of iron regulators. Little is known about low-affinity Zn2+ uptake under zinc-replete conditions. One known example is the phosphate uptake system Pit, which may cotransport Zn2+ in Escherichia coli. Similarly, the citrate—metal cotransporter CitM in Bacillus subtilis may help to supply Zn2+.

Key words

zinc transporter regulator RND type exporter P-type ATPase ABC transporter 

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References

  1. Alonso A, Sanchez P, Martinez JL. 2000 Stenotrophomonas maltophila D457R contains a cluster of genes from gram-positive bacteria involved in antibiotic and heavy metal resistance. Antimicrob Agents Chemother 44, 1778–1782.Google Scholar
  2. Anton A, Grosse C, Reissmann J, Pribyl T, Nies DH. 1999 CzcD is a heavy metal ion transporter involved in regulation of heavy metal resistance in Ralstonia sp. strain CH34. J Bacteriol 181, 6876–6881.PubMedGoogle Scholar
  3. 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.CrossRefGoogle Scholar
  4. Bearden SW, Perry RD. 1999 The Yfe system of Yersinia pestis transports iron and manganese and is required for full virulence of plague. Mol Microbiol 32, 403–414.PubMedCrossRefGoogle Scholar
  5. Binet MR, Poole RK. 2000 Cd(II), Pb(II) and Zn(II) ions regulate expression of the metal-transporting P-type ATPase ZntA in Escherichia coli. FEBS Lett 473, 67–70.CrossRefGoogle Scholar
  6. Braun V, Hantke K, Köster W. 1998 Bacterial iron transport: mechanisms, genetics, and regulation. Met Ions Biol Syst 35, 67–145.PubMedGoogle Scholar
  7. Bsat N, Herbig A, Casillas-Martinez L, Setlow P, Heimann JD. 1998 Bacillus subtilis contains multiple Fur homologues: identification of the iron uptake (Fur) and peroxide regulon (PerR) repressors. Mol Microbiol 29, 189–198.Google Scholar
  8. Bucheder F, Broda E. 1974 Energy-dependent zinc transport by Escherichia coli. Eur J Biochem 45, 555–559.CrossRefGoogle Scholar
  9. Caguiat JJ, Watson AL, Summers AO. 1999 Cd(II)-responsive and constitutive mutants implicate a novel domain in MerR. J Bacteriol 181, 3462–3471.PubMedGoogle Scholar
  10. Clarke ND, Berg JM. 1998 Zinc fingers in Caenorhabditis elegans: finding families and probing pathways. Science 282, 2018–2022.PubMedCrossRefGoogle Scholar
  11. Claverys J-P. 2001 A new family of high affinity ABC manganese and zinc permeases. Res Microbiol 152, 231–243.PubMedCrossRefGoogle Scholar
  12. Cook WJ, Kar SR, Taylor KB, Hall LM. 1998 Crystal structure of the cyanobacterial metallothionein repressor SmtB: a model for metalloregulatory proteins. J Mol Biol 275, 337–346.PubMedCrossRefGoogle Scholar
  13. Dalet K, Gouin E, Cenatiempo Y, Cossart P, Hechard Y. 1999 Characterisation of a new operon encoding a Zur-like protein and an associated ABC zinc permease in Listeria monocvtogenes. FEMS Microbiol Lett 174, 111–116.CrossRefGoogle Scholar
  14. Deka RK, Lee YH, Hagman KE, Shevchenko D, Lingwood CA, Hasemann CA, Norgard MV, Radolf JD. 1999 Physicochemical evidence that Treponema pallidum TroA is a zinc-containing metalloprotein that lacks porin-like structure. J Bacteriol 181, 4420–4423.PubMedGoogle Scholar
  15. Dinthilhac A, Alloing G, Granadel C, Claverys J-P. 1997 Competence and virulence of Streptococcus pneumoniae: AdcA and PsaA mutants exhibit a requirement for Zn and Mn resulting from inactivation of putative ABC metal permeases. Mol Microbiol 25, 727–739.CrossRefGoogle Scholar
  16. Gaballa A, Heimann JD. 1998 Identification of a zinc-specific metalloregulatory protein, Zur, controlling zinc transport operons in Bacillus subtilis. J Bacteriol 180, 5815–5821.Google Scholar
  17. Gatti D, Mitra B, Rosen BP. 2000 Escherichia coli soft metal iontranslocating ATPases. J Biol Chem 275, 34009–34012.Google Scholar
  18. Gilbert HF. 1990 Molecular and cellular aspects of thiol-disulfide exchange. Adv Enzymol Relat Areas Mol Biol 63, 69–172.PubMedGoogle Scholar
  19. Grosse C, Grass G, Anton A, Franke S, Santos AN, Lawley B, Brown NL, Nies DH. 1999 Transcriptional organization of the czc heavy-metal homeostasis determinant from Alcaligenes eutrophus. J Bacteriol 181, 2385–2393.Google Scholar
  20. Hantke K, Braun V. 2000 The art of keeping low and high iron concentrations in balance. In: Storz G, Hengge-Aronis R. eds. Bacterial stress responses. Washington, D.C.: ASM Press: 275–288.Google Scholar
  21. Heidrich C, Hantke K, Bierbaum G, Sahl HG. 1996 Identification and analysis of a gene encoding a Fur-like protein of Staphylococcus epidermidis. FEMS Microbiol Lett 140, 253–259.CrossRefGoogle Scholar
  22. Jacquamet L, Aberdam D, Adrait A, Hazemann JL, Latour JM, Michaud-Soret I. 1998 X-ray absorption spectroscopy of a new zinc site in the Fur protein from Escherichia coli. Biochemistry 37, 2564–2571.Google Scholar
  23. Janulczyk R, Pallon J, Bjorck L. 1999 Identification and characterization of a Streptococcus pyogenes ABC transporter with multiple specificity for metal cations. Mol Microbiol 34, 596–606.PubMedCrossRefGoogle Scholar
  24. Jordan SR, Pabo CO. 1988 Structure of the lambda complex at 2.5 A resolution: details of the repressor-operator interactions. Science 242, 893–899.PubMedCrossRefGoogle Scholar
  25. Krom BP, Warner JB, Konings WN, Lolkema JS. 2000 Complementary metal ion specificity of the metal-citrate transporters CitM and CitH of Bacillus subtilis. J Bacteriol 182, 6374–6381.CrossRefGoogle Scholar
  26. Lai HC, Gygi D, Fraser GM, Hughes C. 1998 A swarming-defective mutant of Proteus mirabilis lacking a putative cation-transporting membrane P-type ATPase. Microbiology 144, 1957–1961.PubMedCrossRefGoogle Scholar
  27. Lawrence MC, Pilling PA, Epa VC, Berry AM, Ogunniyi AD, Paton JC. 1998 The crystal structure of pneumococcal surface antigen PsaA reveals a metal-binding site and a novel structure for a putative ABC-type binding protein. Structure 6, 1553–1561.PubMedCrossRefGoogle Scholar
  28. Lebrun M, Audurier A, Cossart P. 1994 Plasmid-borne cadmium resistance genes in Listeria monocytogenes are similar to cadA and cadC of Staphylococcus aureus and are induced by cadmium. J Bacteriol 176, 3040–3048.PubMedGoogle Scholar
  29. Lee YH, Deka RK, Norgard MV, Radolf JD, Hasemann CA. 1999 Treponema pallidum TroA is a periplasmic zinc-binding protein with a helical backbone. Nat Struct Biol 6, 628–633.Google Scholar
  30. Leonhartsberger S, Huber A, Lottspeich F, Bock A. 2001 The hydH/G genes from Escherichia coli code for a zinc and lead responsive two-component regulatory system. J Mol Biol 307, 93–105.PubMedCrossRefGoogle Scholar
  31. Lewis DA, Klesney-Tait J, Lumbley SR, Ward CK, Latimer JL, Ison CA, Hansen EJ. 1999 Identification of the znuA-encoded periplasmic zinc transport protein of Haemophilus ducreyi. Infect Immun 67, 5060–5068.Google Scholar
  32. Lu D, Boyd B, Lingwood CA. 1997 Identification of the key protein for zinc uptake in Haemophilus influenzae. J Biol Chem 272, 29033–29038.CrossRefGoogle Scholar
  33. Noll M, Lutsenko S. 2000 Expression of ZntA, a zinc-transporting PI-type ATPase, is specifically regulated by zinc and cadmium. IUBMB Life 49, 297–302.PubMedCrossRefGoogle Scholar
  34. Okkeri J, Haltia T. 1999 Expression and mutagenesis of ZntA, a zinc-transporting P-type ATPase from Escherichia coli. Biochemistry 38, 14109–14116.Google Scholar
  35. Outten CE, Outten FW, O’Halloran TV. 1999 DNA distortion mechanism for transcriptional activation by ZntR, a Zn(II)-responsive MerR homologue in Escherichia coli. J Biol Chem 274, 37517–37524.CrossRefGoogle Scholar
  36. Palmiter RD, Findley SD. 1995 Cloning and functional characterization of a mammalian zinc transporter that confers resistance to zinc. EMBO J 14, 639–649.PubMedGoogle Scholar
  37. Palmiter RD, Cole TB, Findley SD. 1996 ZnT-2, a mammalian protein that confers resistance to zinc by facilitating vesicular sequestration. EMBO J 15, 1784–1791.PubMedGoogle Scholar
  38. Patzer SI, Hantke K. 1998 The ZnuABC high-affinity zinc uptake system and its regulator Zur in Escherichia coli. Mol Microbiol 28, 1199–1210.CrossRefGoogle Scholar
  39. 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.CrossRefGoogle Scholar
  40. Paulsen IT, Saier MHJ. 1997 A novel family of ubiquitous heavy metal ion transport proteins. J Membr Biol 156, 99–103.PubMedCrossRefGoogle Scholar
  41. Posey JE, Hardham JM, Norris SJ, Gherardini FC. 1999 Characterization of a manganese-dependent regulatory protein, TroR, from Treponema pallidum. Proc Nat! Acad Sci USA 96, 10887–10892.CrossRefGoogle Scholar
  42. Rensing C, Pribyl T, Nies DH. 1997a New functions for the three subunits of the CzcCBA cation-proton antiporter. J Bacteriol 179, 6871–6879.PubMedGoogle Scholar
  43. Rensing C, Mitra B, Rosen BP. I997b The zntA gene of Escherichia coli encodes a Zn(II)-translocating P-type ATPase. Proc Nat! Acad Sci USA 94, 14326–14331.Google Scholar
  44. Rensing C, Mitra B, Rosen BP. 1998 A Zn(II)-translocating P-type ATPase from Proteus mirabilis. Biochem Cell Biol 76, 787–790.Google Scholar
  45. Robinson NJ, Bird AJ, Turner JS. 1998 Metallothionein gene regulation in cyanobacteria. In: Silver S, Walden W. eds. Metal ions in gene regulation. New York: ITP: 372–397.CrossRefGoogle Scholar
  46. Rosenstein R, Nikoleit K, Götz F. 1994 Binding of ArsR, the repressor of the Staphylococcus xylosus (pSX267) arsenic resistance operon to a sequence with dyad symmetry within the ars promoter. Mol Gen Genet 242, 566–572.PubMedCrossRefGoogle Scholar
  47. 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.CrossRefGoogle Scholar
  48. Shi W, Wu J, Rosen BP. 1994 Identification of a putative metal binding site in a new family of metalloregulatory proteins. J Biol Chem 269, 19826–19829.PubMedGoogle Scholar
  49. Tam R, Saier Jr. MH. 1993 Structural, functional, evolutionary relationships among extracellular solute-binding receptors of bacteria. Microbiol Rev 57, 320–346.PubMedGoogle Scholar
  50. Tsai KJ, Yoon KP, Lynn AR. 1992 ATP-dependent cadmium transport by the cadA cadmium resistance determinant in everted membrane vesicles of Bacillus subtilis. J Bacterial 174, 116–121.Google Scholar
  51. Tseng TT, Gratwick KS, Kollman J, Park D, Nies DH, Goffeau A, Saier MHJ. 1999 The RND permease superfamily: an ancient, ubiquitous and diverse family that includes human disease and development proteins. J Mol Microbiol Biotechnol 1, 107–125.PubMedGoogle Scholar
  52. van Veen HW, Abee T, Kortstee GJ, Konings WN, Zehnder AJ. 1994 Translocation of metal phosphate via the phosphate inorganic transport system of Escherichia coli. Biochemistry 33, 1766–1770.Google Scholar
  53. Xiong A, Jayaswal RK. 1998 Molecular characterization of a chromosomal determinant conferring resistance to zinc and cobalt ions in Staphylococcus aureus. J Bacterial 180, 4024–4029.Google Scholar
  54. Yoon KP, Silver S. 1991 A second gene in the Staphylococcus aureus cadA cadmium resistance determinant of plasmid pI258. J Bacteriol 173, 7636–7642.PubMedGoogle Scholar
  55. Zwicker N, Theobald U, Zähner H, Fiedler H-R. 1997 Optimization of fermentation conditions for the production of ethylenediamine-disuccinic acid by Amycolatopsis orientalis. J Ind Microbial Biotechnol 19, 280–285.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2001

Authors and Affiliations

  • Klaus Hantke
    • 1
  1. 1.Mikrobiologie/MembranphysiologieUniversität TübingenTübingenGermany

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