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A bacterial view of the periodic table: genes and proteins for toxic inorganic ions

  • Environmental Biotechnology
  • Published:
Journal of Industrial Microbiology and Biotechnology

Abstract

Essentially all bacteria have genes for toxic metal ion resistances and these include those for Ag+, AsO −2 , AsO 3−4 , Cd2+, Co2+, CrO 2−4 , Cu2+, Hg2+, Ni2+, Pb2+, TeO 2−3 , Tl+ and Zn2+. The largest group of resistance systems functions by energy-dependent efflux of toxic ions. Fewer involve enzymatic transformations (oxidation, reduction, methylation, and demethylation) or metal-binding proteins (for example, metallothionein SmtA, chaperone CopZ and periplasmic silver binding protein SilE). Some of the efflux resistance systems are ATPases and others are chemiosmotic ion/proton exchangers. For example, Cd2+-efflux pumps of bacteria are either inner membrane P-type ATPases or three polypeptide RND chemiosmotic complexes consisting of an inner membrane pump, a periplasmic-bridging protein and an outer membrane channel. In addition to the best studied three-polypeptide chemiosmotic system, Czc (Cd2+, Zn2+, and Co2), others are known that efflux Ag+, Cu+, Ni2+, and Zn2+. Resistance to inorganic mercury, Hg2+ (and to organomercurials, such as CH3Hg+ and phenylmercury) involve a series of metal-binding and membrane transport proteins as well as the enzymes mercuric reductase and organomercurial lyase, which overall convert more toxic to less toxic forms. Arsenic resistance and metabolizing systems occur in three patterns, the widely-found ars operon that is present in most bacterial genomes and many plasmids, the more recently recognized arr genes for the periplasmic arsenate reductase that functions in anaerobic respiration as a terminal electron acceptor, and the aso genes for the periplasmic arsenite oxidase that functions as an initial electron donor in aerobic resistance to arsenite.

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References

  1. Aguilera S, Aguilar ME, Chavez MP, Lopez-Meza JE, Pedraza-Reyes M, Campos-Garcia J, Cervantes C (2004) Essential residues in the chromate transporter ChrA of Pseudomonas aeruginosa. FEMS Microbiol Lett 232:107–112

    Article  PubMed  CAS  Google Scholar 

  2. Ahmann D, Roberts AL, Krumholz LR, Morel FMM (1994) Microbe grows by reducing arsenic. Nature 371:750

    Article  PubMed  CAS  Google Scholar 

  3. Alkorta I, Hernandez-Allica J, Garbisu C (2004) Plants against the global epidemic of arsenic poisoning. Environ Int 30:949–951

    CAS  Google Scholar 

  4. Anderson GL, Ellis PJ, Kuhn P, Hille R (2001) Oxidation of arsenite by Alcaligenes faecalis. In: Frankenberger WT Jr (ed) Environmental chemistry of arsenic. Marcel Dekker, New York, pp 343–361

    Google Scholar 

  5. Anderson GL, Williams J, Hille R (1992) The purification and characterization of arsenite oxidase from Alcaligenes faecalis, a molybdenum-containing hydroxylase. J Biol Chem 267:23674–23682

    PubMed  CAS  Google Scholar 

  6. Anton A, Weltrowski A, Haney CJ, Franke S, Grass G, Rensing C, Nies DH (2004) Characteristics of zinc transport by two bacterial cation diffusion facilitators from Ralstonia metallidurans CH34 and Escherichia coli. J Bacteriol 186:7499–7507

    Article  PubMed  CAS  Google Scholar 

  7. Arguello JM (2003) Identification of ion-selectivity determinants in heavy-metal transport P1B-type ATPases. J Membr Biol 195:93–108

    Article  PubMed  CAS  Google Scholar 

  8. Bang SW, Clark DS, Keasling JD (2000) Engineering hydrogen sulfide production and cadmium removal by expression of the thiosulfate reductase gene (phsABC) from Salmonella enterica serovar typhimurium in Escherichia coli. Appl Environ Microbiol 66:3939–3944

    CAS  Google Scholar 

  9. Barkay T, Miller SM, Summers AO (2003) Bacterial mercury resistance from atoms to ecosystems. FEMS Microbiol Rev 27:355–384

    Article  PubMed  CAS  Google Scholar 

  10. Begley TP, Ealick SE (2004) Enzymatic reactions involving novel mechanisms of carbanion stabilization. Curr Opin Chem Biol 8:508–515

    Article  PubMed  CAS  Google Scholar 

  11. Benison GC, Di Lello P, Shokes JE, Cosper NJ, Scott RA, Legault P, Omichinski JG (2004) A stable mercury-containing complex of the organomercurial lyase MerB: catalysis, product release, and direct transfer to MerA. Biochemistry 43:8333–8345

    Article  PubMed  CAS  Google Scholar 

  12. Bizily SP, Kim T, Kandasamy MK, Meagher RB (2003) Subcellular targeting of methylmercury lyase enhances its specific activity for organic mercury detoxification in plants. Plant Physiol 131:463–471

    Article  PubMed  CAS  Google Scholar 

  13. Blencowe DK, Morby AP (2003) Zn(II) metabolism in prokaryotes. FEMS Microbiol Rev 27:291–311

    Article  PubMed  CAS  Google Scholar 

  14. Blindauer CA, Harrison MD, Robinson AK, Parkinson JA, Bowness PW, Sadler PJ, Robinson NJ (2002) Multiple bacteria encode metallothioneins and SmtA-like zinc fingers. Mol Microbiol 45:1421–1432

    Article  PubMed  CAS  Google Scholar 

  15. Borremans B, Hobman JL, Provoost A, Brown NL, van der Lelie D (2001) Cloning and functional analysis of the pbr lead resistance determinant of Ralstonia metallidurans CH34. J Bacteriol 183:5651–5658

    Article  PubMed  CAS  Google Scholar 

  16. 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

    Article  PubMed  CAS  Google Scholar 

  17. Brown NL, Morby AP, Robinson NJ (2003) Thematic issue. Interactions of bacteria with metals. FEMS Microbiol Rev 27:129–447

    Article  CAS  Google Scholar 

  18. Brown NL, Stoyanov JV, Kidd SP, Hobman JL (2003) The MerR family of transcriptional regulators. FEMS Microbiol Rev 27:145–163

    Article  PubMed  CAS  Google Scholar 

  19. Busenlehner LS, Pennella MA, Giedroc DP (2003) The SmtB/ArsR family of metalloregulatory transcriptional repressors: Structural insights into prokaryotic metal resistance. FEMS Microbiol Rev 27:131–143

    Article  PubMed  CAS  Google Scholar 

  20. Carlin A, Shi W, Dey S, Rosen BP (1995) The ars operon of Escherichia coli confers arsenical and antimonial resistance. J Bacteriol 177:981–986

    PubMed  CAS  Google Scholar 

  21. Cavet JS, Borrelly GP, Robinson NJ (2003) Zn, Cu and Co in cyanobacteria: selective control of metal availability. FEMS Microbiol Rev 27:165–181

    Article  PubMed  CAS  Google Scholar 

  22. Cervantes C, Campos-Garcia J, Devars S, Gutierrez-Corona F, Loza-Tavera H, Torres-Guzman JC, Moreno-Sanchez R (2001) Interactions of chromium with microorganisms and plants. FEMS Microbiol Rev 25:335–347

    Article  PubMed  CAS  Google Scholar 

  23. Chao Y, Fu D (2004a) Kinetic study of the antiport mechanism of an Escherichia coli zinc transporter, ZitB. J Biol Chem 279:12043–12050

    Article  CAS  Google Scholar 

  24. Chao Y, Fu D (2004b) Thermodynamic studies of the mechanism of metal binding to the Escherichia coli zinc transporter YiiP. J Biol Chem 279:17173–17180

    Article  CAS  Google Scholar 

  25. Chau YK, Zhang S, Maguire RJ (1992) Occurrence of butyltin species in sewage and sludge in Canada. Sci Total Environ 121:271–281

    Article  PubMed  CAS  Google Scholar 

  26. Chen P, Greenberg B, Taghavi S, Romano C, van der Lelie D, He C (2005) An exceptionally selective lead(II)-regulatory protein from Ralstonia metallidurans: development of a fluorescent lead(II) probe. Angew Chem Int Ed Engl 44:2715–2719

    Article  PubMed  CAS  Google Scholar 

  27. Cooksey DA (1994) Molecular mechanisms of copper resistance and accumulation in bacteria. FEMS Microbiol Rev 14:381–386

    Article  PubMed  CAS  Google Scholar 

  28. Cooney JJ, Wuertz S (1989) Toxic effects of tin compounds on microorganisms. J Ind Microbiol 4:375–402

    Article  CAS  Google Scholar 

  29. Degen O, Eitinger T (2002) Substrate specificity of nickel/cobalt permeases: insights from mutants altered in transmembrane domains I and II. J Bacteriol 184:3569–3577

    Article  PubMed  CAS  Google Scholar 

  30. DeSilva TM, Veglia G, Porcelli F, Prantner AM, Opella SJ (2002) Selectivity in heavy metal-binding to peptides and proteins. Biopolymers 64:189–197

    Article  PubMed  CAS  Google Scholar 

  31. Di Lello P, Benison GC, Omichinski JG, Legault P (2004a) 1 H, 15 N, and 13 C resonance assignment of the 23 kDa organomercurial lyase MerB in its free and mercury-bound forms. J Biomol NMR 29:457–458

    Article  CAS  Google Scholar 

  32. Di Lello P, Benison GC, Valafar H, Pitts KE, Summers AO, Legault P, Omichinski JG (2004b) NMR structural studies reveal a novel protein fold for MerB, the organomercurial lyase involved in the bacterial mercury resistance system. Biochemistry 43:8322–8332

    Article  CAS  Google Scholar 

  33. Diels L, De Smet M, Hooyberghs L, Corbisier P (1999) Heavy metals bioremediation of soil. Mol Biotechnol 12:149–158. Erratum in Mol Biotechnol 113:171

    Google Scholar 

  34. Eicken C, Pennella MA, Chen X, Koshlap KM, VanZile ML, Sacchettini JC, Giedroc DP (2003) A metal-ligand-mediated intersubunit allosteric switch in related SmtB/ArsR zinc sensor proteins. J Mol Biol 333:683–695

    Article  PubMed  CAS  Google Scholar 

  35. Ellis PJ, Conrads T, Hille R, Kuhn P (2001) Crystal structure of the 100 kDa arsenite oxidase from Alcaligenes faecalis in two crystal forms at 1.64 A and 2.03 A. Struct (Camb) 9:125–132

    Article  CAS  Google Scholar 

  36. Engst S, Miller SM (1998) Rapid reduction of Hg(II) by mercuric ion reductase does not require the conserved C-terminal cysteine pair using HgBr2 as the substrate. Biochemistry 37:11496–11507

    CAS  Google Scholar 

  37. Engst S, Miller SM (1999) Alternative routes for entry of HgX2 into the active site of mercuric ion reductase depend on the nature of the X ligands. Biochemistry 38:3519–3529

    Article  PubMed  CAS  Google Scholar 

  38. Eswaran J, Koronakis E, Higgins MK, Hughes C, Koronakis V (2004) Three’s company: component structures bring a closer view of tripartite drug efflux pumps. Curr Opin Struct Biol 14:741–747

    Article  PubMed  CAS  Google Scholar 

  39. 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

    Article  PubMed  CAS  Google Scholar 

  40. Frankenberger WT Jr (ed) (2001) Environmental chemistry of arsenic. Marcel Dekker, New York

    Google Scholar 

  41. Frausto Da Silva JJR, Williams RJP (2001) The biological chemistry of the elements: the inorganic chemistry of life. Oxford University Press, Oxford

    Google Scholar 

  42. Goldberg M, Pribyl T, Juhnke S, Nies DH (1999) Energetics and topology of CzcA, a cation/proton antiporter of the resistance-nodulation-cell division protein family. J Biol Chem 274:26065–26070

    Article  PubMed  CAS  Google Scholar 

  43. Grass G, Franke S, Taudte N, Nies DH, Kucharski LM, Maguire ME, Rensing C (2005a) The metal permease ZupT from Escherichia coli is a transporter with a broad substrate spectrum. J Bacteriol 187:1604–1611

    Article  CAS  Google Scholar 

  44. Grass G, Otto M, Fricke B, Haney CJ, Rensing C, Nies DH, Munkelt D (2005b) FieF (YiiP) from Escherichia coli mediates decreased cellular accumulation of iron and relieves iron stress. Arch Microbiol 183:9–18

    Article  CAS  Google Scholar 

  45. Gupta A, Matsui K, Lo JF, Silver S (1999) Molecular basis for resistance to silver cations in Salmonella. Nat Med 5:183–188

    Article  PubMed  CAS  Google Scholar 

  46. Gupta A, Phung LT, Taylor DE, Silver S (2001) Diversity of silver resistance genes in IncH incompatibility group plasmids. Microbiology 147:3393–3402

    PubMed  CAS  Google Scholar 

  47. Haney CJ, Grass G, Franke S, Rensing C (2005) New developments in the understanding of the cation diffusion facilitator family. J Ind Microbiol Biotechnol 32:215–226

    Article  PubMed  CAS  Google Scholar 

  48. Hassan MT, van der Lelie D, Springael D, Romling U, Ahmed N, Mergeay M (1999) Identification of a gene cluster, czr, involved in cadmium and zinc resistance in Pseudomonas aeruginosa. Gene 238:417–425

    Article  PubMed  CAS  Google Scholar 

  49. Hebbeln P, Eitinger T (2004) Heterologous production and characterization of bacterial nickel/cobalt permeases. FEMS Microbiol Lett 230:129–135

    Article  PubMed  CAS  Google Scholar 

  50. Higgins MK, Bokma E, Koronakis E, Hughes C, Koronakis V (2004) Structure of the periplasmic component of a acterial drug efflux pump. Proc Natl Acad Sci USA 101:9994–9999

    Article  PubMed  CAS  Google Scholar 

  51. Hoke KR, Cobb N, Armstrong FA, Hille R (2004) Electrochemical studies of arsenite oxidase: an unusual example of a highly cooperative two-electron molybdenum center. Biochemistry 43:1667–1674

    Article  PubMed  CAS  Google Scholar 

  52. Husain F, Humbard M, Misra R (2004) Interaction between the TolC and AcrA proteins of a multidrug efflux system of Escherichia coli. J Bacteriol 186:8533–8536

    Article  PubMed  CAS  Google Scholar 

  53. Jude F, Arpin C, Brachet-Castang C, Capdepuy M, Caumette P, Quentin C (2004) TbtABM, a multidrug efflux pump associated with tributyltin resistance in Pseudomonas stutzeri. FEMS Microbiol Lett 232:7–14

    Article  PubMed  CAS  Google Scholar 

  54. Karenlampi S, Schat H, Vangronsveld J, Verkleij JA, van der Lelie D, Mergeay M, Tervahauta AI (2000) Genetic engineering in the improvement of plants for phytoremediation of metal polluted soils. Environ Pollut 107:225–231

    CAS  Google Scholar 

  55. Koch AL, Silver S (2005) The first cell. Adv Microb Physiol 50 (in press)

  56. Lancaster CRD (2004) Structural biology: ion pump in the movies. Nature 432:286–287

    Article  PubMed  CAS  Google Scholar 

  57. Lebrun E, Brugna M, Baymann F, Muller D, Lievremont D, Lett MC, Nitschke W (2003) Arsenite oxidase, an ancient bioenergetic enzyme. Mol Biol Evol 20:686–693

    Article  PubMed  CAS  Google Scholar 

  58. LeDuc DL, Terry N (2005) Phytoremediation of toxic trace elements in soil and water. J Ind Microbiol Biotechnol 32 (in press)

  59. 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

    Article  PubMed  CAS  Google Scholar 

  60. Levi P (1984) Sistema periodico. English title: the periodic table, translated by Raymond Rosenthal. Schocken, New York

    Google Scholar 

  61. Levinson HS, Mahler I, Blackwelder P, Hood T (1996) Lead resistance and sensitivity in Staphylococcus aureus. FEMS Microbiol Lett 145:421–425

    Article  PubMed  CAS  Google Scholar 

  62. Li S, Rosen BP, Borges-Walmsley MI, Walmsley AR (2002) Evidence for cooperativity between the four binding sites of dimeric ArsD, an As(III)-responsive transcriptional regulator. J Biol Chem 277:25992–26002

    Article  PubMed  CAS  Google Scholar 

  63. Li XZ, Nikaido H (2004) Efflux-mediated drug resistance in bacteria. Drugs 64:159–204

    Article  PubMed  CAS  Google Scholar 

  64. Lippard SJ, Berg JM (1994) Principles of bioinorganic chemistry. University Science Books, Mill Valley

    Google Scholar 

  65. Lodewyckx C, Taghavi S, Mergeay M, Vangronsveld J, Clijsters H, van der Lelie D (2001) The effect of recombinant heavy metal-resistant endophytic bacteria on heavy metal uptake by their host plant. Int J Phytoremediation 3:173–187

    CAS  Google Scholar 

  66. Makkar NS, Cooney JJ (1990) Methylation of monomethyltin by a bacterial coculture. Geomicrobiol J 8:101–107

    Article  CAS  Google Scholar 

  67. Mandal AK, Yang Y, Kertesz TM, Arguello JM (2004) Identification of the transmembrane metal binding site in Cu+-transporting PIB-type ATPases. J Biol Chem 279:54802–54807

    Article  PubMed  CAS  Google Scholar 

  68. Meagher RB (2005) Strategies for the engineered phytoremediation of toxic element pollution: mercury and arsenic. J Ind Microbiol Bioechnol 32 (in press)

  69. Mergeay M, Monchy S, Vallaeys T, Auquier V, Benotmane A, Bertin P, Taghavi S, Dunn J, van der Lelie D, Wattiez R (2003) Ralstonia metallidurans, a bacterium specifically adapted to toxic metals: towards a catalogue of metal-responsive genes. FEMS Microbiol Rev 27:385–410

    Article  PubMed  CAS  Google Scholar 

  70. Messens J, Van Molle I, Vanhaesebrouck P, Van Belle K, Wahni K, Martins JC, Wyns L, Loris R (2004) The structure of a triple mutant of pI258 arsenate reductase from Staphylococcus aureus and its 5-thio-2-nitrobenzoic acid adduct. Acta Crystallogr D Biol Crystallogr 60:1180–1184

    Article  PubMed  CAS  Google Scholar 

  71. Miller CE, Wuertz S, Cooney JJ, Pfister RM (1995) Plasmids in tributyltin-resistant bacteria from fresh and estuarine waters. J Ind Microbiol 14:337–342

    Article  CAS  Google Scholar 

  72. Miller SM (1999) Bacterial detoxification of Hg(II) and organomercurials. Essays Biochem 34:17–30

    PubMed  CAS  Google Scholar 

  73. Mukhopadhyay R, Rosen BP, Phung LT, Silver S (2002) Microbial arsenic: from geocycles to genes and enzymes. FEMS Microbiol Rev 26:311–325

    Article  PubMed  CAS  Google Scholar 

  74. Muller D, Lievremont D, Simeonova DD, Hubert JC, Lett MC (2003) Arsenite oxidase aox genes from a metal-resistant beta-proteobacterium. J Bacteriol 185:135–141

    Article  PubMed  CAS  Google Scholar 

  75. Mulrooney SB, Hausinger RP (2003) Nickel uptake and utilization by microorganisms. FEMS Microbiol Rev 27:239–261

    Article  PubMed  CAS  Google Scholar 

  76. Munkelt D, Grass G, Nies DH (2004) The chromosomally encoded cation diffusion facilitator proteins DmeF and FieF from Wautersia metallidurans CH34 are transporters of broad metal specificity. J Bacteriol 186:8036–8043

    Article  PubMed  CAS  Google Scholar 

  77. Murakami S, Nakashima R, Yamashita E, Yamaguchi A (2002) Crystal structure of bacterial multidrug efflux transporter AcrB. Nature 419:587–593

    Article  PubMed  CAS  Google Scholar 

  78. Murakami S, Tamura N, Saito A, Hirata T, Yamaguchi A (2004) Extramembrane central pore of multidrug exporter AcrB in Escherichia coli plays an important role in drug transport. J Biol Chem 279:3743–3748

    Article  PubMed  CAS  Google Scholar 

  79. Murakami S, Yamaguchi A (2003) Multidrug-exporting secondary transporters. Curr Opin Struct Biol 13:443–452

    Article  PubMed  CAS  Google Scholar 

  80. Narita M, Chiba K, Nishizawa H, Ishii H, Huang CC, Kawabata Z, Silver S, Endo G (2003) Diversity of mercury resistance determinants among Bacillus strains isolated from sediment of Minamata Bay. FEMS Microbiol Lett 223:73–82. Erratum in FEMS Microbiol Lett 226:415

    Google Scholar 

  81. Nies DH (1995) The cobalt, zinc, and cadmium efflux system CzcABC from Alcaligenes eutrophus functions as a cation-proton antiporter in Escherichia coli. J Bacteriol 177:2707–2712

    PubMed  CAS  Google Scholar 

  82. Nies DH (2003) Efflux-mediated heavy metal resistance in prokaryotes. FEMS Microbiol Rev 27:313–339

    Article  PubMed  CAS  Google Scholar 

  83. Ohtake H, Silver S (1994) Bacterial detoxification of toxic chromate. In: Chaudhry GR (ed) Biological degradation and bioremediation of toxic chemicals. Chapman and Hall, London, pp 403–415

    Google Scholar 

  84. Opella SJ, DeSilva TM, Veglia G (2002) Structural biology of metal-binding sequences. Curr Opin Chem Biol 6:217–223

    Article  PubMed  CAS  Google Scholar 

  85. Oremland RS, Stolz JF (2005) Arsenic, microbes and contaminated aquifers. Trends Microbiol 13:45–49

    Article  PubMed  CAS  Google Scholar 

  86. Pilon-Smits E (2005) Phytoremediation. Annu Rev Plant Biol 56:15–39

    Article  PubMed  CAS  Google Scholar 

  87. Pitts KE, Summers AO (2002) The roles of thiols in the bacterial organomercurial lyase (MerB). Biochemistry 41:10287–10296

    Article  PubMed  CAS  Google Scholar 

  88. Rensing C, Grass G (2003) Escherichia coli mechanisms of copper homeostasis in a changing environment. FEMS Microbiol Rev 27:197–213

    Article  PubMed  CAS  Google Scholar 

  89. 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

    Article  PubMed  CAS  Google Scholar 

  90. Rodrigue A, Effantin G, Mandrand-Berthelot MA (2005) Identification of rcnA (yohM), a nickel and cobalt resistance gene in Escherichia coli. J Bacteriol 187:2912–2916

    Article  PubMed  CAS  Google Scholar 

  91. Rossbach S, Kukuk ML, Wilson TL, Feng SF, Pearson MM, Fisher MA (2000) Cadmium-regulated gene fusions in Pseudomonas fluorescens. Environ Microbiol 2:373–382

    CAS  Google Scholar 

  92. Rugh CL, Senecoff JF, Meagher RB, Merkle SA (1998) Development of transgenic yellow poplar for mercury phytoremediation. Nat Biotechnol 16:925–928

    Article  PubMed  CAS  Google Scholar 

  93. Ruiz ON, Hussein HS, Terry N, Daniell H (2003) Phytoremediation of organomercurial compounds via chloroplast genetic engineering. Plant Physiol 132:1344–1352

    Article  PubMed  CAS  Google Scholar 

  94. Saier MH Jr, Beatty JT, Goffeau A, Harley KT, Heijne WH, Huang SC, Jack DL, Jahn PS, Lew K, Liu J, Pao SS, Paulsen IT, Tseng TT, Virk PS (1999) The major facilitator superfamily. J Mol Microbiol Biotechnol 1:257–279. Erratum in J Mol Microbiol Biotechnol 252:255

    Google Scholar 

  95. Schiering N, Kabsch W, Moore MJ, Distefano MD, Walsh CT, Pai EF (1991) Structure of the detoxification catalyst mercuric ion reductase from Bacillus sp. strain RC607. Nature 352:168–172

    Article  PubMed  CAS  Google Scholar 

  96. Sigel A, Sigel H, Sigel RKO (eds) (2005) Biogeochemical cycles of elements, vol 43. Taylor & Francis Group, Boca Raton

  97. Silver S (1996) Bacterial resistances to toxic metal ions—a review. Gene 179:9–19

    Article  PubMed  CAS  Google Scholar 

  98. Silver S (1996) Transport of inorganic cations. In: Neidhardt FC et al (ed) Escherichia coli and Salmonella typhimurium: cellular and molecular biology, vol 1. ASM, Washington, pp 1091–1102

  99. Silver S (1998) Genes for all metals–a bacterial view of the periodic table. The 1996 Thom Award Lecture. J Ind Microbiol Biotechnol 20:1–12

    Article  PubMed  CAS  Google Scholar 

  100. Silver S (2003) Bacterial silver resistance: molecular biology and uses and misuses of silver compounds. FEMS Microbiol Rev 27:341–353

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  102. Silver S, Phung LT (1996) Bacterial heavy metal resistance: new surprises. Annu Rev Microbiol 50:753–789

    Article  PubMed  CAS  Google Scholar 

  103. Silver S, Phung LT (2005) Genes and enzymes involved in bacterial oxidation and reduction of inorganic arsenic. Appl Environ Microbiol 71:599–608

    CAS  Google Scholar 

  104. Silver S, Phung LT, Rosen BP (2001) Arsenic metabolism: resistance, reduction, and oxidation. In: Frankenberger WT Jr (ed) Environmental chemistry of arsenic. Marcel Dekker, New York, pp 247–272

    Google Scholar 

  105. Singh SK, Grass G, Rensing C, Montfort WR (2004) Cuprous oxidase activity of CueO from Escherichia coli. J Bacteriol 186:7815–7817

    Article  PubMed  CAS  Google Scholar 

  106. Solioz M, Odermatt A (1995) Copper and silver transport by CopB-ATPase in membrane vesicles of Enterococcus hirae. J Biol Chem 270:9217–9221

    Article  PubMed  CAS  Google Scholar 

  107. Solioz M, Stoyanov J (2003) Copper homeostasis in Enterococcus hirae. FEMS Microbiol Rev 27:183–195

    Article  PubMed  CAS  Google Scholar 

  108. Solioz M, Vulpe C (1996) CPX-type ATPases: a class of P-type ATPases that pump heavy metals. Trends Biochem Sci 21:237–241

    Article  PubMed  CAS  Google Scholar 

  109. Steele RA, Opella SJ (1997) Structures of the reduced and mercury-bound forms of MerP, the periplasmic protein from the bacterial mercury detoxification system. Biochemistry 36:6885–6895

    Article  PubMed  CAS  Google Scholar 

  110. Thomas DJ, Waters SB, Styblo M (2004) Elucidating the pathway for arsenic methylation. Toxicol Appl Pharmacol 198:319–326

    Article  PubMed  CAS  Google Scholar 

  111. Tisa LS, Rosen BP (1990) Molecular characterization of an anion pump. The ArsB protein is the membrane anchor for the ArsA protein. J Biol Chem 265:190–194

    PubMed  CAS  Google Scholar 

  112. Touze T, Eswaran J, Bokma E, Koronakis E, Hughes C, Koronakis V (2004) Interactions underlying assembly of the Escherichia coli AcrAB-TolC multidrug efflux system. Mol Microbiol 53:697–706

    Article  PubMed  CAS  Google Scholar 

  113. Toyoshima C, Inesi G (2004) Structural basis of ion pumping by Ca2+ -ATPase of the sarcoplasmic reticulum. Annu Rev Biochem 73:269–292

    Article  PubMed  CAS  Google Scholar 

  114. Toyoshima C, Mizutani T (2004) Crystal structure of the calcium pump with a bound ATP analogue. Nature 430:529–535

    Article  PubMed  CAS  Google Scholar 

  115. Toyoshima C, Nomura H, Tsuda T (2004) Lumenal gating mechanism revealed in calcium pump crystal structures with phosphate analogues. Nature 432:361–368

    Article  PubMed  CAS  Google Scholar 

  116. Tseng TT, Gratwick KS, Kollman J, Park D, Nies DH, Goffeau A, Saier MH, Jr. (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

    PubMed  CAS  Google Scholar 

  117. Wang CL, Clark DS, Keasling JD (2001) Analysis of an engineered sulfate reduction pathway and cadmium precipitation on the cell surface. Biotechnol Bioeng 75:285–291

    Article  PubMed  CAS  Google Scholar 

  118. Wei Y, Li H, Fu D (2004) Oligomeric state of the Escherichia coli metal transporter YiiP. J Biol Chem 279:39251–39259

    Article  PubMed  CAS  Google Scholar 

  119. White JS, Tobin JM, Cooney JJ (1999) Organotin compounds and their interactions with microorganisms. Can J Microbiol 45:541–554

    Article  PubMed  CAS  Google Scholar 

  120. Wilson JR, Leang C, Morby AP, Hobman JL, Brown NL (2000) MerF is a mercury transport protein: different structures but a common mechanism for mercuric ion transporters? FEBS Lett 472:78–82

    Article  PubMed  CAS  Google Scholar 

  121. Wuertz S, Miller CE, Pfister RM, Cooney JJ (1991) Tributyltin-resistant bacteria from estuarine and freshwater sediments. Appl Environ Microbiol 57:2783–2789

    CAS  Google Scholar 

  122. Yu EW, Aires JR, Nikaido H (2003a) AcrB multidrug efflux pump of Escherichia coli: composite substrate-binding cavity of exceptional flexibility generates its extremely wide substrate specificity. J Bacteriol 185:5657–5664

    Article  CAS  Google Scholar 

  123. Yu EW, McDermott G, Zgurskaya HI, Nikaido H, Koshland DE Jr (2003b) Structural basis of multiple drug-binding capacity of the AcrB multidrug efflux pump. Science 300:976–980

    Article  CAS  Google Scholar 

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  1. Department of Microbiology and Immunology, University of Illinois, Chicago, IL, 60612, USA

    Simon Silver & Le T. Phung

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  1. Simon Silver
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  2. Le T. Phung
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Correspondence to Simon Silver or Le T. Phung.

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Silver, S., Phung, L.T. A bacterial view of the periodic table: genes and proteins for toxic inorganic ions. J IND MICROBIOL BIOTECHNOL 32, 587–605 (2005). https://doi.org/10.1007/s10295-005-0019-6

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  • DOI: https://doi.org/10.1007/s10295-005-0019-6

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