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

Environmental Biotechnology

Abstract

Essentially all bacteria have genes for toxic metal ion resistances and these include those for Ag+, AsO2, AsO43−, Cd2+, Co2+, CrO42−, Cu2+, Hg2+, Ni2+, Pb2+, TeO32−, 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.

Keywords

Toxic metal resistances Arsenic Mercury Cadmium Bacterial plasmids 

References

  1. 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 232:107–112CrossRefPubMedGoogle Scholar
  2. 2.
    Ahmann D, Roberts AL, Krumholz LR, Morel FMM (1994) Microbe grows by reducing arsenic. Nature 371:750CrossRefPubMedGoogle Scholar
  3. 3.
    Alkorta I, Hernandez-Allica J, Garbisu C (2004) Plants against the global epidemic of arsenic poisoning. Environ Int 30:949–951Google Scholar
  4. 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 343–361Google Scholar
  5. 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 267:23674–23682PubMedGoogle Scholar
  6. 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 186:7499–7507CrossRefPubMedGoogle Scholar
  7. 7.
    Arguello JM (2003) Identification of ion-selectivity determinants in heavy-metal transport P1B-type ATPases. J Membr Biol 195:93–108CrossRefPubMedGoogle Scholar
  8. 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 66:3939–3944Google Scholar
  9. 9.
    Barkay T, Miller SM, Summers AO (2003) Bacterial mercury resistance from atoms to ecosystems. FEMS Microbiol Rev 27:355–384CrossRefPubMedGoogle Scholar
  10. 10.
    Begley TP, Ealick SE (2004) Enzymatic reactions involving novel mechanisms of carbanion stabilization. Curr Opin Chem Biol 8:508–515CrossRefPubMedGoogle Scholar
  11. 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 43:8333–8345CrossRefPubMedGoogle Scholar
  12. 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 131:463–471CrossRefPubMedGoogle Scholar
  13. 13.
    Blencowe DK, Morby AP (2003) Zn(II) metabolism in prokaryotes. FEMS Microbiol Rev 27:291–311CrossRefPubMedGoogle Scholar
  14. 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 45:1421–1432CrossRefPubMedGoogle Scholar
  15. 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 183:5651–5658CrossRefPubMedGoogle Scholar
  16. 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 17:1153–1166CrossRefPubMedGoogle Scholar
  17. 17.
    Brown NL, Morby AP, Robinson NJ (2003) Thematic issue. Interactions of bacteria with metals. FEMS Microbiol Rev 27:129–447CrossRefGoogle Scholar
  18. 17a.
    Brown NL, Stoyanov JV, Kidd SP, Hobman JL (2003) The MerR family of transcriptional regulators. FEMS Microbiol Rev 27:145–163CrossRefPubMedGoogle Scholar
  19. 18.
    Busenlehner LS, Pennella MA, Giedroc DP (2003) The SmtB/ArsR family of metalloregulatory transcriptional repressors: Structural insights into prokaryotic metal resistance. FEMS Microbiol Rev 27:131–143CrossRefPubMedGoogle Scholar
  20. 19.
    Carlin A, Shi W, Dey S, Rosen BP (1995) The ars operon of Escherichia coli confers arsenical and antimonial resistance. J Bacteriol 177:981–986PubMedGoogle Scholar
  21. 20.
    Cavet JS, Borrelly GP, Robinson NJ (2003) Zn, Cu and Co in cyanobacteria: selective control of metal availability. FEMS Microbiol Rev 27:165–181CrossRefPubMedGoogle Scholar
  22. 21.
    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 25:335–347CrossRefPubMedGoogle Scholar
  23. 22.
    Chao Y, Fu D (2004a) Kinetic study of the antiport mechanism of an Escherichia coli zinc transporter, ZitB. J Biol Chem 279:12043–12050CrossRefGoogle Scholar
  24. 23.
    Chao Y, Fu D (2004b) Thermodynamic studies of the mechanism of metal binding to the Escherichia coli zinc transporter YiiP. J Biol Chem 279:17173–17180CrossRefGoogle Scholar
  25. 24.
    Chau YK, Zhang S, Maguire RJ (1992) Occurrence of butyltin species in sewage and sludge in Canada. Sci Total Environ 121:271–281CrossRefPubMedGoogle Scholar
  26. 25.
    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 44:2715–2719CrossRefPubMedGoogle Scholar
  27. 26.
    Cooksey DA (1994) Molecular mechanisms of copper resistance and accumulation in bacteria. FEMS Microbiol Rev 14:381–386CrossRefPubMedGoogle Scholar
  28. 27.
    Cooney JJ, Wuertz S (1989) Toxic effects of tin compounds on microorganisms. J Ind Microbiol 4:375–402CrossRefGoogle Scholar
  29. 28.
    Degen O, Eitinger T (2002) Substrate specificity of nickel/cobalt permeases: insights from mutants altered in transmembrane domains I and II. J Bacteriol 184:3569–3577CrossRefPubMedGoogle Scholar
  30. 29.
    DeSilva TM, Veglia G, Porcelli F, Prantner AM, Opella SJ (2002) Selectivity in heavy metal-binding to peptides and proteins. Biopolymers 64:189–197CrossRefPubMedGoogle Scholar
  31. 30.
    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 29:457–458CrossRefGoogle Scholar
  32. 31.
    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 43:8322–8332CrossRefGoogle Scholar
  33. 32.
    Diels L, De Smet M, Hooyberghs L, Corbisier P (1999) Heavy metals bioremediation of soil. Mol Biotechnol 12:149–158. Erratum in Mol Biotechnol 113:171Google Scholar
  34. 33.
    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 333:683–695CrossRefPubMedGoogle Scholar
  35. 34.
    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) 9:125–132CrossRefGoogle Scholar
  36. 35.
    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 37:11496–11507Google Scholar
  37. 36.
    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 38:3519–3529CrossRefPubMedGoogle Scholar
  38. 37.
    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 14:741–747CrossRefPubMedGoogle Scholar
  39. 38.
    Franke S, Grass G, Rensing C, Nies DH (2003) Molecular analysis of the copper-transporting efflux system CusCFBA of Escherichia coli. J Bacteriol 185:3804–3812CrossRefPubMedGoogle Scholar
  40. 39.
    Frankenberger WT Jr (ed) (2001) Environmental chemistry of arsenic. Marcel Dekker, New YorkGoogle Scholar
  41. 40.
    Frausto Da Silva JJR, Williams RJP (2001) The biological chemistry of the elements: the inorganic chemistry of life. Oxford University Press, OxfordGoogle Scholar
  42. 41.
    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 274:26065–26070CrossRefPubMedGoogle Scholar
  43. 42.
    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 187:1604–1611CrossRefGoogle Scholar
  44. 43.
    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 183:9–18CrossRefGoogle Scholar
  45. 44.
    Gupta A, Matsui K, Lo JF, Silver S (1999) Molecular basis for resistance to silver cations in Salmonella. Nat Med 5:183–188CrossRefPubMedGoogle Scholar
  46. 45.
    Gupta A, Phung LT, Taylor DE, Silver S (2001) Diversity of silver resistance genes in IncH incompatibility group plasmids. Microbiology 147:3393–3402PubMedGoogle Scholar
  47. 46.
    Haney CJ, Grass G, Franke S, Rensing C (2005) New developments in the understanding of the cation diffusion facilitator family. J Ind Microbiol Biotechnol 32:215–226CrossRefPubMedGoogle Scholar
  48. 47.
    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 238:417–425CrossRefPubMedGoogle Scholar
  49. 48.
    Hebbeln P, Eitinger T (2004) Heterologous production and characterization of bacterial nickel/cobalt permeases. FEMS Microbiol Lett 230:129–135CrossRefPubMedGoogle Scholar
  50. 49.
    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 101:9994–9999CrossRefPubMedGoogle Scholar
  51. 50.
    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 43:1667–1674CrossRefPubMedGoogle Scholar
  52. 51.
    Husain F, Humbard M, Misra R (2004) Interaction between the TolC and AcrA proteins of a multidrug efflux system of Escherichia coli. J Bacteriol 186:8533–8536CrossRefPubMedGoogle Scholar
  53. 52.
    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 232:7–14CrossRefPubMedGoogle Scholar
  54. 53.
    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 107:225–231Google Scholar
  55. 54.
    Koch AL, Silver S (2005) The first cell. Adv Microb Physiol 50 (in press)Google Scholar
  56. 55.
    Lancaster CRD (2004) Structural biology: ion pump in the movies. Nature 432:286–287CrossRefPubMedGoogle Scholar
  57. 56.
    Lebrun E, Brugna M, Baymann F, Muller D, Lievremont D, Lett MC, Nitschke W (2003) Arsenite oxidase, an ancient bioenergetic enzyme. Mol Biol Evol 20:686–693CrossRefPubMedGoogle Scholar
  58. 57.
    LeDuc DL, Terry N (2005) Phytoremediation of toxic trace elements in soil and water. J Ind Microbiol Biotechnol 32 (in press)Google Scholar
  59. 58.
    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 185:4354–4361CrossRefPubMedGoogle Scholar
  60. 59.
    Levi P (1984) Sistema periodico. English title: the periodic table, translated by Raymond Rosenthal. Schocken, New YorkGoogle Scholar
  61. 60.
    Levinson HS, Mahler I, Blackwelder P, Hood T (1996) Lead resistance and sensitivity in Staphylococcus aureus. FEMS Microbiol Lett 145:421–425CrossRefPubMedGoogle Scholar
  62. 61.
    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 277:25992–26002CrossRefPubMedGoogle Scholar
  63. 62.
    Li XZ, Nikaido H (2004) Efflux-mediated drug resistance in bacteria. Drugs 64:159–204CrossRefPubMedGoogle Scholar
  64. 63.
    Lippard SJ, Berg JM (1994) Principles of bioinorganic chemistry. University Science Books, Mill ValleyGoogle Scholar
  65. 64.
    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 3:173–187Google Scholar
  66. 65.
    Makkar NS, Cooney JJ (1990) Methylation of monomethyltin by a bacterial coculture. Geomicrobiol J 8:101–107CrossRefGoogle Scholar
  67. 66.
    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 279:54802–54807CrossRefPubMedGoogle Scholar
  68. 67.
    Meagher RB (2005) Strategies for the engineered phytoremediation of toxic element pollution: mercury and arsenic. J Ind Microbiol Bioechnol 32 (in press)Google Scholar
  69. 68.
    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 27:385–410CrossRefPubMedGoogle Scholar
  70. 69.
    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 60:1180–1184CrossRefPubMedGoogle Scholar
  71. 70.
    Miller CE, Wuertz S, Cooney JJ, Pfister RM (1995) Plasmids in tributyltin-resistant bacteria from fresh and estuarine waters. J Ind Microbiol 14:337–342CrossRefGoogle Scholar
  72. 71.
    Miller SM (1999) Bacterial detoxification of Hg(II) and organomercurials. Essays Biochem 34:17–30PubMedGoogle Scholar
  73. 72.
    Mukhopadhyay R, Rosen BP, Phung LT, Silver S (2002) Microbial arsenic: from geocycles to genes and enzymes. FEMS Microbiol Rev 26:311–325CrossRefPubMedGoogle Scholar
  74. 73.
    Muller D, Lievremont D, Simeonova DD, Hubert JC, Lett MC (2003) Arsenite oxidase aox genes from a metal-resistant beta-proteobacterium. J Bacteriol 185:135–141CrossRefPubMedGoogle Scholar
  75. 74.
    Mulrooney SB, Hausinger RP (2003) Nickel uptake and utilization by microorganisms. FEMS Microbiol Rev 27:239–261CrossRefPubMedGoogle Scholar
  76. 75.
    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 186:8036–8043CrossRefPubMedGoogle Scholar
  77. 76.
    Murakami S, Nakashima R, Yamashita E, Yamaguchi A (2002) Crystal structure of bacterial multidrug efflux transporter AcrB. Nature 419:587–593CrossRefPubMedGoogle Scholar
  78. 77.
    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 279:3743–3748CrossRefPubMedGoogle Scholar
  79. 78.
    Murakami S, Yamaguchi A (2003) Multidrug-exporting secondary transporters. Curr Opin Struct Biol 13:443–452CrossRefPubMedGoogle Scholar
  80. 79.
    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 226:415Google Scholar
  81. 80.
    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 177:2707–2712PubMedGoogle Scholar
  82. 81.
    Nies DH (2003) Efflux-mediated heavy metal resistance in prokaryotes. FEMS Microbiol Rev 27:313–339CrossRefPubMedGoogle Scholar
  83. 82.
    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 403–415Google Scholar
  84. 83.
    Opella SJ, DeSilva TM, Veglia G (2002) Structural biology of metal-binding sequences. Curr Opin Chem Biol 6:217–223CrossRefPubMedGoogle Scholar
  85. 84.
    Oremland RS, Stolz JF (2005) Arsenic, microbes and contaminated aquifers. Trends Microbiol 13:45–49CrossRefPubMedGoogle Scholar
  86. 85.
    Pilon-Smits E (2005) Phytoremediation. Annu Rev Plant Biol 56:15–39CrossRefPubMedGoogle Scholar
  87. 86.
    Pitts KE, Summers AO (2002) The roles of thiols in the bacterial organomercurial lyase (MerB). Biochemistry 41:10287–10296CrossRefPubMedGoogle Scholar
  88. 87.
    Rensing C, Grass G (2003) Escherichia coli mechanisms of copper homeostasis in a changing environment. FEMS Microbiol Rev 27:197–213CrossRefPubMedGoogle Scholar
  89. 88.
    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 278:31958–31963CrossRefPubMedGoogle Scholar
  90. 89.
    Rodrigue A, Effantin G, Mandrand-Berthelot MA (2005) Identification of rcnA (yohM), a nickel and cobalt resistance gene in Escherichia coli. J Bacteriol 187:2912–2916CrossRefPubMedGoogle Scholar
  91. 90.
    Rossbach S, Kukuk ML, Wilson TL, Feng SF, Pearson MM, Fisher MA (2000) Cadmium-regulated gene fusions in Pseudomonas fluorescens. Environ Microbiol 2:373–382Google Scholar
  92. 91.
    Rugh CL, Senecoff JF, Meagher RB, Merkle SA (1998) Development of transgenic yellow poplar for mercury phytoremediation. Nat Biotechnol 16:925–928CrossRefPubMedGoogle Scholar
  93. 92.
    Ruiz ON, Hussein HS, Terry N, Daniell H (2003) Phytoremediation of organomercurial compounds via chloroplast genetic engineering. Plant Physiol 132:1344–1352CrossRefPubMedGoogle Scholar
  94. 93.
    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 252:255Google Scholar
  95. 94.
    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 352:168–172CrossRefPubMedGoogle Scholar
  96. 95.
    Sigel A, Sigel H, Sigel RKO (eds) (2005) Biogeochemical cycles of elements, vol 43. Taylor & Francis Group, Boca RatonGoogle Scholar
  97. 96.
    Silver S (1996) Bacterial resistances to toxic metal ions—a review. Gene 179:9–19CrossRefPubMedGoogle Scholar
  98. 97.
    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 1091–1102Google Scholar
  99. 98.
    Silver S (1998) Genes for all metals–a bacterial view of the periodic table. The 1996 Thom Award Lecture. J Ind Microbiol Biotechnol 20:1–12CrossRefPubMedGoogle Scholar
  100. 99.
    Silver S (2003) Bacterial silver resistance: molecular biology and uses and misuses of silver compounds. FEMS Microbiol Rev 27:341–353CrossRefPubMedGoogle Scholar
  101. 100.
    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 10:7–12PubMedGoogle Scholar
  102. 101.
    Silver S, Phung LT (1996) Bacterial heavy metal resistance: new surprises. Annu Rev Microbiol 50:753–789CrossRefPubMedGoogle Scholar
  103. 102.
    Silver S, Phung LT (2005) Genes and enzymes involved in bacterial oxidation and reduction of inorganic arsenic. Appl Environ Microbiol 71:599–608Google Scholar
  104. 103.
    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 247–272Google Scholar
  105. 104.
    Singh SK, Grass G, Rensing C, Montfort WR (2004) Cuprous oxidase activity of CueO from Escherichia coli. J Bacteriol 186:7815–7817CrossRefPubMedGoogle Scholar
  106. 105.
    Solioz M, Odermatt A (1995) Copper and silver transport by CopB-ATPase in membrane vesicles of Enterococcus hirae. J Biol Chem 270:9217–9221CrossRefPubMedGoogle Scholar
  107. 106.
    Solioz M, Stoyanov J (2003) Copper homeostasis in Enterococcus hirae. FEMS Microbiol Rev 27:183–195CrossRefPubMedGoogle Scholar
  108. 107.
    Solioz M, Vulpe C (1996) CPX-type ATPases: a class of P-type ATPases that pump heavy metals. Trends Biochem Sci 21:237–241CrossRefPubMedGoogle Scholar
  109. 108.
    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 36:6885–6895CrossRefPubMedGoogle Scholar
  110. 109.
    Thomas DJ, Waters SB, Styblo M (2004) Elucidating the pathway for arsenic methylation. Toxicol Appl Pharmacol 198:319–326CrossRefPubMedGoogle Scholar
  111. 110.
    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 265:190–194PubMedGoogle Scholar
  112. 111.
    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 53:697–706CrossRefPubMedGoogle Scholar
  113. 112.
    Toyoshima C, Inesi G (2004) Structural basis of ion pumping by Ca2+ -ATPase of the sarcoplasmic reticulum. Annu Rev Biochem 73:269–292CrossRefPubMedGoogle Scholar
  114. 113.
    Toyoshima C, Mizutani T (2004) Crystal structure of the calcium pump with a bound ATP analogue. Nature 430:529–535CrossRefPubMedGoogle Scholar
  115. 114.
    Toyoshima C, Nomura H, Tsuda T (2004) Lumenal gating mechanism revealed in calcium pump crystal structures with phosphate analogues. Nature 432:361–368CrossRefPubMedGoogle Scholar
  116. 115.
    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 1:107–125PubMedGoogle Scholar
  117. 116.
    Wang CL, Clark DS, Keasling JD (2001) Analysis of an engineered sulfate reduction pathway and cadmium precipitation on the cell surface. Biotechnol Bioeng 75:285–291CrossRefPubMedGoogle Scholar
  118. 117.
    Wei Y, Li H, Fu D (2004) Oligomeric state of the Escherichia coli metal transporter YiiP. J Biol Chem 279:39251–39259CrossRefPubMedGoogle Scholar
  119. 118.
    White JS, Tobin JM, Cooney JJ (1999) Organotin compounds and their interactions with microorganisms. Can J Microbiol 45:541–554CrossRefPubMedGoogle Scholar
  120. 119.
    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 472:78–82CrossRefPubMedGoogle Scholar
  121. 120.
    Wuertz S, Miller CE, Pfister RM, Cooney JJ (1991) Tributyltin-resistant bacteria from estuarine and freshwater sediments. Appl Environ Microbiol 57:2783–2789Google Scholar
  122. 121.
    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 185:5657–5664CrossRefGoogle Scholar
  123. 122.
    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 300:976–980CrossRefGoogle Scholar

Copyright information

© Society for Industrial Microbiology 2005

Authors and Affiliations

  1. 1.Department of Microbiology and ImmunologyUniversity of IllinoisChicagoUSA

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