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Molecular Microbiology of Heavy Metals pp 371–406Cite as

Arsenic Metabolism in Prokaryotic and Eukaryotic Microbes

Part of the Microbiology Monographs book series (MICROMONO,volume 6)

Abstract

This chapter will focus on recent progress on the mechanisms of metalloid uptake, metabolism, and detoxification in bacteria, archaea, and eukaryotic microbes. One of the initial challenges of the earliest cells would have been the ability to detoxify heavy metal ions, transition metal ions, and metalloids, including arsenic and antimony. The presence of arsenic resistance (ars) genes in the genome of by far most living organisms sequenced to date illustrates firstly that ars genes must be ancient and secondly that arsenic is still ubiquitous in the environment, providing the selective pressure that maintains these genes in present-day organisms. Some early cells also probably could use arsenite as an electron acceptor, giving selective pressure for the evolution of respiratory arsenate reductase. As atmospheric O2 levels increased, arsenite was oxidized to arsenate abiotically. This provided an advantage for the evolution of arsenate reductases, some for arsenate respiration and energy production, and others for arsenate detoxification. Present-day selective pressure for metalloid resistance also comes from sources such as natural release of arsenic from volcanic activities, mining activities, the burning of coal, and other human activities. In addition is the use of arsenicals and antimonials as chemotherapeutic drugs for the treatment of parasitic diseases and cancer. Resistance to these drugs is becoming a major dilemma. Thus, an understanding of the molecular details of metalloid transport systems and detoxification enzymes is essential for the rational design of new drugs, and for treating drug-resistant microorganisms and tumor cells. Finally, this chapter will summarize recent identification of novel enzymes for arsenic reduction, oxidation, and methylation that expand the possibilities for metalloid metabolism and transformations.

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References

  1. Acharyya SK, Chakraborty P, Lahiri S, Raymahashay BC, Guha S, Bhowmik A (1999) Arsenic poisoning in the Ganges delta. Nature 401:545; discussion 546–547

    CrossRef  PubMed  CAS  Google Scholar 

  2. Afkar E, Lisak J, Saltikov C, Basu P, Oremland RS, Stolz JF (2003) The respiratory arsenate reductase from Bacillus selenitireducens strain MLS10. FEMS Microbiol Lett 226:107–112

    CrossRef  PubMed  CAS  Google Scholar 

  3. Agre P, King LS, Yasui M, Guggino WB, Ottersen OP, Fujiyoshi Y, Engel A, Nielsen S (2002) Aquaporin water channels—from atomic structure to clinical medicine. J Physiol 542:3–16

    CrossRef  PubMed  CAS  Google Scholar 

  4. Akter KF, Owens G, Davey DE, Naidu R (2005) Arsenic speciation and toxicity in biological systems. Rev Environ Contam Toxicol 184:97–149

    CrossRef  PubMed  CAS  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. Aslund F, Ehn B, Miranda-Vizuete A, Pueyo C, Holmgren A (1994) Two additional glutaredoxins exist in Escherichia coli: glutaredoxin 3 is a hydrogen donor for ribonucleotide reductase in a thioredoxin/glutaredoxin 1 double mutant. Proc Natl Acad Sci USA 91:9813–9817

    CrossRef  PubMed  CAS  Google Scholar 

  7. Bennett MS, Guan Z, Laurberg M, Su XD (2001) Bacillus subtilis arsenate reductase is structurally and functionally similar to low molecular weight protein tyrosine phosphatases. Proc Natl Acad Sci USA 98:13577–13582

    CrossRef  PubMed  CAS  Google Scholar 

  8. Bentley R, Chasteen TG (2002) Microbial methylation of metalloids: arsenic, antimony, and bismuth. Microbiol Mol Biol Rev 66:250–271

    CrossRef  PubMed  CAS  Google Scholar 

  9. Bhattacharjee H, Rosen BP (2000) Role of conserved histidine residues in metalloactivation of the ArsA ATPase. Biometals 13:281–288

    CrossRef  PubMed  CAS  Google Scholar 

  10. Bhattacharjee H, Li J, Ksenzenko MY, Rosen BP (1995) Role of cysteinyl residues in metalloactivation of the oxyanion-translocating ArsA ATPase. J Biol Chem 270:11245–11250

    CrossRef  PubMed  CAS  Google Scholar 

  11. Bhattacharjee H, Zhou T, Li J, Gatti DL, Walmsley AR, Rosen BP (2000) Structure–function relationships in an anion-translocating ATPase. Biochem Soc Trans 28:520–526

    CrossRef  PubMed  CAS  Google Scholar 

  12. Bhattacharjee H, Ho YS, Rosen BP (2001) Genomic organization and chromosomal localization of the Asna1 gene, a mouse homologue of a bacterial arsenic-translocating ATPase gene. Gene 272:291–299

    CrossRef  PubMed  CAS  Google Scholar 

  13. Bhattacharjee H, Carbrey J, Rosen BP, Mukhopadhyay R (2004) Drug uptake and pharmacological modulation of drug sensitivity in leukemia by AQP9. Biochem Biophys Res Commun 322:836–841

    CrossRef  PubMed  CAS  Google Scholar 

  14. Bobrowicz P, Wysocki R, Owsianik G, Goffeau A, Ulaszewski S (1997) Isolation of three contiguous genes, ACR1, ACR2, and ACR3, involved in resistance to arsenic compounds in the yeast Saccharomyces cerevisiae. Yeast 13:819–828

    CrossRef  PubMed  CAS  Google Scholar 

  15. Boles E, Hollenberg CP (1997) The molecular genetics of hexose transport in yeasts. FEMS Microbiol Rev 21:85–111

    CrossRef  PubMed  CAS  Google Scholar 

  16. Borgnia M, Nielsen S, Engel A, Agre P (1999) Cellular and molecular biology of the aquaporin water channels. Annu Rev Biochem 68:425–458

    CrossRef  PubMed  CAS  Google Scholar 

  17. Bun-ya M, Shikata K, Nakade S, Yompakdee C, Harashima S, Oshima Y (1996) Two new genes, PHO86 and PHO87, involved in inorganic phosphate uptake in Saccharomyces cerevisiae. Curr Genet 29:344–351

    PubMed  CAS  Google Scholar 

  18. Busenlehner LS, Cosper NJ, Scott RA, Rosen BP, Wong MD, Giedroc DP (2001) Spectroscopic properties of the metalloregulatory Cd(II) and Pb(II) sites of Staphylococcus aureus pI258 CadC. Biochemistry 40:4426–4436

    CrossRef  PubMed  CAS  Google Scholar 

  19. Busenlehner LS, Apuy JL, Giedroc DP (2002) Characterization of a metalloregulatory bismuth(III) site in Staphylococcus aureus pI258 CadC repressor. J Biol Inorg Chem 7:551–559

    CrossRef  PubMed  CAS  Google Scholar 

  20. Butcher BG, Rawlings DE (2002) The divergent chromosomal ars operon of Acidithiobacillus ferrooxidans is regulated by an atypical ArsR protein. Microbiology 148:3983–3992

    PubMed  CAS  Google Scholar 

  21. Butcher BG, Deane SM, Rawlings DE (2000) The chromosomal arsenic resistance genes of Thiobacillus ferrooxidans have an unusual arrangement and confer increased arsenic and antimony resistance to Escherichia coli. Appl Environ Microbiol 66:1826–1833

    CrossRef  PubMed  CAS  Google Scholar 

  22. Carbrey JM, Gorelick-Feldman DA, Kozono D, Praetorius J, Nielsen S, Agre P (2003) Aquaglyceroporin AQP9: solute permeation and metabolic control of expression in liver. Proc Natl Acad Sci USA 100:2945–2950

    CrossRef  PubMed  CAS  Google Scholar 

  23. Cavet JS, Meng W, Pennella MA, Appelhoff RJ, Giedroc DP, Robinson NJ (2002) A nickel–cobalt sensing ArsR–SmtB family repressor: contributions of cytosol and effector binding sites to metal selectivity. J Biol Chem 277:38441–38448

    CrossRef  PubMed  CAS  Google Scholar 

  24. Cavet JS, Graham AI, Meng W, Robinson NJ (2003) A cadmium–lead sensing ArsR–SmtB repressor with novel sensory sites: complementary metal-discrimination by NMTR and CMTR in a common cytosol. J Biol Chem 278:44560–44566

    CrossRef  PubMed  CAS  Google Scholar 

  25. Chen CM, Misra TK, Silver S, Rosen BP (1986) Nucleotide sequence of the structural genes for an anion pump. The plasmid-encoded arsenical resistance operon. J Biol Chem 261:15030–15038

    PubMed  CAS  Google Scholar 

  26. Chen Y, Rosen BP (1997) Metalloregulatory properties of the ArsD repressor. J Biol Chem 272:14257–14262

    CrossRef  PubMed  CAS  Google Scholar 

  27. Cole SP, Sparks KE, Fraser K, Loe DW, Grant CE, Wilson GM, Deeley RG (1994) Pharmacological characterization of multidrug-resistant MRP-transfected human tumor cells. Cancer Res 54:5902–5910

    PubMed  CAS  Google Scholar 

  28. 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

    CrossRef  PubMed  CAS  Google Scholar 

  29. Dembitsky VM, Levitsky DO (2004) Arsenolipids. Prog Lipid Res 43:403–448

    CrossRef  PubMed  CAS  Google Scholar 

  30. DeMel S, Shi J, Martin P, Rosen BP, Edwards BF (2004) Arginine 60 in the ArsC arsenate reductase of E. coli plasmid R773 determines the chemical nature of the bound As(III) product. Protein Sci 13:2330–2340

    CrossRef  PubMed  CAS  Google Scholar 

  31. Denu JM, Dixon JE (1995) A catalytic mechanism for the dual-specific phosphatases. Proc Natl Acad Sci USA 92:5910–5914

    CrossRef  PubMed  CAS  Google Scholar 

  32. Dey S, Rosen BP (1995) Dual mode of energy coupling by the oxyanion-translocating ArsB protein. J Bacteriol 177:385–389

    CrossRef  PubMed  CAS  Google Scholar 

  33. Dey S, Dou D, Rosen BP (1994) ATP-dependent arsenite transport in everted membrane vesicles of Escherichia coli. J Biol Chem 269:25442–25446

    PubMed  CAS  Google Scholar 

  34. Drobna Z, Waters SB, Devesa V, Harmon AW, Thomas DJ, Styblo M (2005) Metabolism and toxicity of arsenic in human urothelial cells expressing rat arsenic (+3 oxidation state)-methyltransferase. Toxicol Appl Pharmacol 207:147–159

    CrossRef  PubMed  CAS  Google Scholar 

  35. Duan G, Zhou Y, Tong YP, Mukhopadhyay R, Rosen BP, Zhu YG (2007) Two A CDC25 homologue from rice functions as an arsenate reductase. New Phytologist, in press

    Google Scholar 

  36. Ellis DR, Gumaelius L, Indriolo E, Pickering IJ, Banks JA, Salt DE (2006) A novel arsenate reductase from the arsenic hyperaccumulating fern Pteris vittata. Plant Physiol 141:1544–1554

    CrossRef  PubMed  CAS  Google Scholar 

  37. Ellis PJ, Conrads T, Hille R, Kuhn P (2001) Crystal structure of the - 100kDa arsenite oxidase from Alcaligenes faecalis in two crystal forms at 1.64 Åand 2.03 Å. Structure 9:125–132

    CrossRef  PubMed  CAS  Google Scholar 

  38. Endo G, Silver S (1995) CadC, the transcriptional regulatory protein of the cadmium resistance system of Staphylococcus aureus plasmid pI258. J Bacteriol 177:4437–4441

    PubMed  CAS  Google Scholar 

  39. Fauman EB, Cogswell JP, Lovejoy B, Rocque WJ, Holmes W, Montana VG, Piwnica-Worms H, Rink MJ, Saper MA (1998) Crystal structure of the catalytic domain of the human cell cycle control phosphatase, Cdc25A. Cell 93:617–625

    CrossRef  PubMed  CAS  Google Scholar 

  40. Ghosh M, Shen J, Rosen BP (1999) Pathways of As(III) detoxification in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 96:5001–5006

    CrossRef  PubMed  CAS  Google Scholar 

  41. Gihring TM, Bond PL, Peters SC, Banfield JF (2003) Arsenic resistance in the archaeon “Ferroplasma acidarmanus”: new insights into the structure and evolution of the ars genes. Extremophiles 7:123–130

    PubMed  CAS  Google Scholar 

  42. Gladysheva TB, Oden KL, Rosen BP (1994) Properties of the arsenate reductase of plasmid R773. Biochemistry 33:7288–7293

    CrossRef  PubMed  CAS  Google Scholar 

  43. Gourbal B, Sonuc N, Bhattacharjee H, Legare D, Sundar S, Ouellette M, Rosen BP, Mukhopadhyay R (2004) Drug uptake and modulation of drug resistance in Leishmania by an aquaglyceroporin. J Biol Chem 279:31010–31017

    CrossRef  PubMed  CAS  Google Scholar 

  44. Guo X, Li Y, Peng K, Hu Y, Li C, Xia B, Jin C (2005) Solution structures and backbone dynamics of arsenate reductase from Bacillus subtilis: reversible conformational switch associated with arsenate reduction. J Biol Chem 280:39601–39608

    CrossRef  PubMed  CAS  Google Scholar 

  45. Hamson GC, Stosick AJ (1938) The molecular structure of arsenious oxide, As4O6, phosphorus trioxide, P4O6, phosphorus pentoxide, P4010, and hexamethylenetetramine, (CH6)N4, by electron diffraction. J Am Chem Soc 60:1814–1822

    CrossRef  Google Scholar 

  46. Harvey CF, Swartz CH, Badruzzaman AB, Keon-Blute N, Yu W, Ali MA, Jay J, Beckie R, Niedan V, Brabander D, Oates PM, Ashfaque KN, Islam S, Hemond HF, Ahmed MF (2002) Arsenic mobility and groundwater extraction in Bangladesh. Science 298:1602–1606

    CrossRef  PubMed  CAS  Google Scholar 

  47. Heller KB, Lin EC, Wilson TH (1980) Substrate specificity and transport properties of the glycerol facilitator of Escherichia coli. J Bacteriol 144:274–278

    PubMed  CAS  Google Scholar 

  48. Hirano S, Kobayashi Y, Cui X, Kanno S, Hayakawa T, Shraim A (2004) The accumulation and toxicity of methylated arsenicals in endothelial cells: important roles of thiol compounds. Toxicol Appl Pharmacol 198:458–467

    CrossRef  PubMed  CAS  Google Scholar 

  49. Huckle JW, Morby AP, Turner JS, Robinson NJ (1993) Isolation of a prokaryotic metallothionein locus and analysis of transcriptional control by trace metal ions. Mol Microbiol 7:177–187

    CrossRef  PubMed  CAS  Google Scholar 

  50. Islam FS, Gault AG, Boothman C, Polya DA, Charnock JM, Chatterjee D, Lloyd JR (2004) Role of metal-reducing bacteria in arsenic release from Bengal delta sediments. Nature 430:68–71

    CrossRef  PubMed  CAS  Google Scholar 

  51. Ji G, Silver S (1992) Reduction of arsenate to arsenite by the ArsC protein of the arsenic resistance operon of Staphylococcus aureus plasmid pI258. Proc Natl Acad Sci USA 89:9474–9478

    CrossRef  PubMed  CAS  Google Scholar 

  52. Ji G, Garber EAE, Armes LG, Chen CM, Fuchs JA, Silver S (1994) Arsenate reductase of Staphylococcus aureus plasmid pI258. Biochemistry 33:7294–7299

    CrossRef  PubMed  CAS  Google Scholar 

  53. Karkaria CE, Chen CM, Rosen BP (1990) Mutagenesis of a nucleotide-binding site of an anion-translocating ATPase. J Biol Chem 265:7832–7836

    PubMed  CAS  Google Scholar 

  54. Kaur P, Rosen BP (1992) Mutagenesis of the C-terminal nucleotide-binding site of an anion-translocating ATPase. J Biol Chem 267:19272–19277

    PubMed  CAS  Google Scholar 

  55. King LS, Kozono D, Agre P (2004) From structure to disease: the evolving tale of aquaporin biology. Nat Rev Mol Cell Biol 5:687–698

    CrossRef  PubMed  CAS  Google Scholar 

  56. Krafft T, Macy JM (1998) Purification and characterization of the respiratory arsenate reductase of Chrysiogenes arsenatis. Eur J Biochem 255:647–653

    CrossRef  PubMed  CAS  Google Scholar 

  57. Kuroda M, Dey S, Sanders OI, Rosen BP (1997) Alternate energy coupling of ArsB, the membrane subunit of the Ars anion-translocating ATPase. J Biol Chem 272:326–331

    CrossRef  PubMed  CAS  Google Scholar 

  58. 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

    CrossRef  PubMed  CAS  Google Scholar 

  59. Leipe DD, Wolf YI, Koonin EV, Aravind L (2002) Classification and evolution of P-loop GTPases and related ATPases. J Mol Biol 317:41–72

    CrossRef  PubMed  CAS  Google Scholar 

  60. Leslie EM, Haimeur A, Waalkes MP (2004) Arsenic transport by the human multidrug resistance protein 1 (MRP1/ABCC1). Evidence that a tri-glutathione conjugate is required. J Biol Chem 279:32700–32708

    CrossRef  PubMed  CAS  Google Scholar 

  61. Li R, Haile JD, Kennelly PJ (2003) An arsenate reductase from Synechocystis sp. strain PCC 6803 exhibits a novel combination of catalytic characteristics. J Bacteriol 185:6780–6789

    CrossRef  PubMed  CAS  Google Scholar 

  62. Lin S, Shi Q, Nix FB, Styblo M, Beck MA, Herbin-Davis KM, Hall LL, Simeonsson JB, Thomas DJ (2002) A novel S-adenosyl-l-methionine:arsenic(III) methyltransferase from rat liver cytosol. J Biol Chem 277:10795–10803

    CrossRef  PubMed  CAS  Google Scholar 

  63. Lin SJ, Pufahl RA, Dancis A, O'Halloran TV, Culotta VC (1997) A role for the Saccharomyces cerevisiae ATX1 gene in copper trafficking and iron transport. J Biol Chem 272:9215–9220

    CrossRef  PubMed  CAS  Google Scholar 

  64. Lin YF, Walmsley AR, Rosen BP (2006) An arsenic metallochaperone for an arsenic detoxification pump. Proc Natl Acad Sci USA 103:15617–15622

    CrossRef  PubMed  CAS  Google Scholar 

  65. Liu Z, Sanchez M, Jiang X, Boles E, Landerfear S, Rosen BP (2006) Mammalian glucose transporter GLUT1 facilitates transport of arsenic trioxide and methylarsonous acid. Biochem Biophys Res Commun 351:424–430

    CrossRef  PubMed  CAS  Google Scholar 

  66. Liu J, Rosen BP (1997) Ligand interactions of the ArsC arsenate reductase. J Biol Chem 272:21084–21089

    CrossRef  PubMed  CAS  Google Scholar 

  67. Liu J, Gladysheva TB, Lee L, Rosen BP (1995) Identification of an essential cysteinyl residue in the ArsC arsenate reductase of plasmid R773. Biochemistry 34:13472–13476

    CrossRef  PubMed  CAS  Google Scholar 

  68. Liu Z, Shen J, Carbrey JM, Mukhopadhyay R, Agre P, Rosen BP (2002) Arsenite transport by mammalian aquaglyceroporins AQP7 and AQP9. Proc Natl Acad Sci USA 99:6053–6058

    CrossRef  PubMed  CAS  Google Scholar 

  69. Liu Z, Boles E, Rosen BP (2004a) Arsenic trioxide uptake by hexose permeases in Saccharomyces cerevisiae. J Biol Chem 279:17312–17318

    CrossRef  PubMed  CAS  Google Scholar 

  70. Liu Z, Carbrey JM, Agre P, Rosen BP (2004b) Arsenic trioxide uptake by human and rat aquaglyceroporins. Biochem Biophys Res Commun 316:1178–1185

    CrossRef  PubMed  CAS  Google Scholar 

  71. Lopez-Maury L, Florencio FJ, Reyes JC (2003) Arsenic sensing and resistance system in the cyanobacterium Synechocystis sp. strain PCC 6803. J Bacteriol 185:5363–5371

    CrossRef  PubMed  CAS  Google Scholar 

  72. Maciaszczyk E, Wysocki R, Golik P, Lazowska J, Ulaszewski S (2004) Arsenical resistance genes in Saccharomyces douglasii and other yeast species undergo rapid evolution involving genomic rearrangements and duplications. FEMS Yeast Res 4:821–832

    CrossRef  PubMed  CAS  Google Scholar 

  73. Marger MD, Saier MH Jr (1993) A major superfamily of transmembrane facilitators that catalyse uniport, symport and antiport. Trends Biochem Sci 18:13–20

    CrossRef  PubMed  CAS  Google Scholar 

  74. Martin P, DeMel S, Shi J, Gladysheva T, Gatti DL, Rosen BP, Edwards BF (2001) Insights into the structure, solvation, and mechanism of ArsC arsenate reductase, a novel arsenic detoxification enzyme. Structure 9:1071–1081

    CrossRef  PubMed  CAS  Google Scholar 

  75. Meng YL, Liu Z, Rosen BP (2004) As(III) and Sb(III) uptake by GlpF and efflux by ArsB in Escherichia coli. J Biol Chem 279:18334–18341

    CrossRef  PubMed  CAS  Google Scholar 

  76. Messens J, Hayburn G, Desmyter A, Laus G, Wyns L (1999) The essential catalytic redox couple in arsenate reductase from Staphylococcus aureus. Biochemistry 38:16857–16865

    CrossRef  PubMed  CAS  Google Scholar 

  77. Messens J, Martins JC, Van Belle K, Brosens E, Desmyter A, De Gieter M, Wieruszeski JM, Willem R, Wyns L, Zegers I (2002) All intermediates of the arsenate reductase mechanism, including an intramolecular dynamic disulfide cascade. Proc Natl Acad Sci USA 99:8506–8511

    CrossRef  PubMed  CAS  Google Scholar 

  78. Metz J, Wachter A, Schmidt B, Bujnicki JM, Schwappach B (2006) The yeast Arr4p ATPase binds the chloride transporter Gef1p when copper is available in the cytosol. J Biol Chem 281:410–417

    CrossRef  PubMed  CAS  Google Scholar 

  79. Morby AP, Turner JS, Huckle JW, Robinson NJ (1993) SmtB is a metal-dependent repressor of the cyanobacterial metallothionein gene smtA: identification of a Zn inhibited DNA–protein complex. Nucleic Acids Res 21:921–925

    CrossRef  PubMed  CAS  Google Scholar 

  80. Mukhopadhyay R, Rosen BP (1998) Saccharomyces cerevisiae ACR2 gene encodes an arsenate reductase. FEMS Microbiol Lett 168:127–136

    CrossRef  PubMed  CAS  Google Scholar 

  81. Mukhopadhyay R, Rosen BP (2001) The phosphatase C(X)5R motif is required for catalytic activity of the Saccharomyces cerevisiae Acr2p arsenate reductase. J Biol Chem 276:34738–34742

    CrossRef  PubMed  CAS  Google Scholar 

  82. Mukhopadhyay R, Rosen BP (2002) Arsenate reductases in prokaryotes and eukaryotes. Environ Health Perspect 110(Suppl 5):745–748

    PubMed  CAS  Google Scholar 

  83. Mukhopadhyay R, Shi J, Rosen BP (2000) Purification and characterization of Acr2p, the Saccharomyces cerevisiae arsenate reductase. J Biol Chem 275:21149–21157

    CrossRef  PubMed  CAS  Google Scholar 

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

    CrossRef  PubMed  CAS  Google Scholar 

  85. Mukhopadhyay R, Zhou Y, Rosen BP (2003) Directed evolution of a yeast arsenate reductase into a protein–tyrosine phosphatase. J Biol Chem 278:24476–24480

    CrossRef  PubMed  CAS  Google Scholar 

  86. Mukhopadhyay R, Ho YS, Swiatek PJ, Rosen BP, Bhattacharjee H (2006) Targeted disruption of the mouse Asna1 gene results in embryonic lethality. FEBS Lett 580:3889–3894

    CrossRef  PubMed  CAS  Google Scholar 

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

    CrossRef  PubMed  CAS  Google Scholar 

  88. Neyt C, Iriarte M, Thi VH, Cornelis GR (1997) Virulence and arsenic resistance in Yersiniae. J Bacteriol 179:612–619

    PubMed  CAS  Google Scholar 

  89. Ordonez E, Letek M, Valbuena N, Gil JA, Mateos LM (2005) Analysis of genes involved in arsenic resistance in Corynebacterium glutamicum ATCC 13032. Appl Environ Microbiol 71:6206–6215

    CrossRef  PubMed  CAS  Google Scholar 

  90. Oremland RS, Stolz JF (2003) The ecology of arsenic. Science 300:939–944

    CrossRef  PubMed  CAS  Google Scholar 

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

    CrossRef  PubMed  CAS  Google Scholar 

  92. Petrick JS, Ayala-Fierro F, Cullen WR, Carter DE, Vasken Aposhian H (2000) Monomethylarsonous acid (MMA(III)) is more toxic than arsenite in Chang human hepatocytes. Toxicol Appl Pharmacol 163:203–207

    CrossRef  PubMed  CAS  Google Scholar 

  93. Qin J, Rosen BP, Zhang Y, Wang G, Franke S, Rensing C (2006) Arsenic detoxification and evolution of trimethylarsine gas by a microbial arsenite S-adenosylmethionine methyltransferase. Proc Natl Acad Sci USA 103:2075–2080

    CrossRef  PubMed  CAS  Google Scholar 

  94. Ramirez-Solis A, Mukopadhyay R, Rosen BP, Stemmler TL (2004) Experimental and theoretical characterization of arsenite in water: insights into the coordination environment of As–O. Inorg Chem 43:2954–2959

    CrossRef  PubMed  CAS  Google Scholar 

  95. Roos G, Loverix S, Brosens E, Van Belle K, Wyns L, Geerlings P, Messens J (2006) The activation of electrophile, nucleophile and leaving group during the reaction catalysed by pI258 arsenate reductase. Chembiochem 7:981–989

    CrossRef  PubMed  CAS  Google Scholar 

  96. Rosen BP (2002) Biochemistry of arsenic detoxification. FEBS Lett 529:86–92

    CrossRef  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  98. Rosenberg H, Gerdes RG, Chegwidden K (1977) Two systems for the uptake of phosphate in Escherichia coli. J Bacteriol 131:505–511

    PubMed  CAS  Google Scholar 

  99. Rosenzweig AC (2002) Metallochaperones: bind and deliver. Chem Biol 9:673–677

    CrossRef  PubMed  CAS  Google Scholar 

  100. Ruan X, Bhattacharjee H, Rosen BP (2006) Cys-113 and Cys-422 form a high-affinity metalloid binding site in the ArsA ATPase. J Biol Chem 281:9925–9934

    CrossRef  PubMed  CAS  Google Scholar 

  101. Ryan D, Colleran E (2002) Arsenical resistance in the IncHI2 plasmids. Plasmid 47:234–240

    CrossRef  PubMed  CAS  Google Scholar 

  102. Saltikov CW, Newman DK (2003) Genetic identification of a respiratory arsenate reductase. Proc Natl Acad Sci USA 100:10983–10988

    CrossRef  PubMed  CAS  Google Scholar 

  103. Saltikov CW, Cifuentes A, Venkateswaran K, Newman DK (2003) The ars detoxification system is advantageous but not required for As(V) respiration by the genetically tractable Shewanella species strain ANA-3. Appl Environ Microbiol 69:2800–2809

    CrossRef  PubMed  CAS  Google Scholar 

  104. Sanders OI, Rensing C, Kuroda M, Mitra B, Rosen BP (1997) Antimonite is accumulated by the glycerol facilitator GlpF in Escherichia coli. J Bacteriol 179:3365–3367

    PubMed  CAS  Google Scholar 

  105. Santini JM, van den Hoven RN (2004) Molybdenum-containing arsenite oxidase of the chemolithoautotrophic arsenite oxidizer NT-26. J Bacteriol 186:1614–1619

    CrossRef  PubMed  CAS  Google Scholar 

  106. Santini JM, Sly LI, Schnagl RD, Macy JM (2000) A new chemolithoautotrophic arsenite-oxidizing bacterium isolated from a gold mine: phylogenetic, physiological, and preliminary biochemical studies. Appl Environ Microbiol 66:92–97

    CrossRef  PubMed  CAS  Google Scholar 

  107. Sato T, Kobayashi Y (1998) The ars operon in the skin element of Bacillus subtilis confers resistance to arsenate and arsenite. J Bacteriol 180:1655–1661

    PubMed  CAS  Google Scholar 

  108. Schuldiner M, Collins SR, Thompson NJ, Denic V, Bhamidipati A, Punna T, Ihmels J, Andrews B, Boone C, Greenblatt JF, Weissman JS, Krogan NJ (2005) Exploration of the function and organization of the yeast early secretory pathway through an epistatic miniarray profile. Cell 123:507–519

    CrossRef  PubMed  CAS  Google Scholar 

  109. Shen J, Hsu CM, Kang BK, Rosen BP, Bhattacharjee H (2003) The Saccharomyces cerevisiae Arr4p is involved in metal and heat tolerance. Biometals 16:369–378

    CrossRef  PubMed  CAS  Google Scholar 

  110. Shi J, Vlamis-Gardikas A, Aslund F, Holmgren A, Rosen BP (1999) Reactivity of glutaredoxins 1, 2, and 3 from Escherichia coli shows that glutaredoxin 2 is the primary hydrogen donor to ArsC-catalyzed arsenate reduction. J Biol Chem 274:36039–36042

    CrossRef  PubMed  CAS  Google Scholar 

  111. Shi J, Mukhopadhyay R, Rosen BP (2003) Identification of a triad of arginine residues in the active site of the ArsC arsenate reductase of plasmid R773. FEMS Microbiol Lett 227:295–301

    CrossRef  PubMed  CAS  Google Scholar 

  112. 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

    PubMed  CAS  Google Scholar 

  113. Shi W, Dong J, Scott RA, Ksenzenko MY, Rosen BP (1996) The role of arsenic–thiol interactions in metalloregulation of the ars operon. J Biol Chem 271:9291–9297

    CrossRef  PubMed  CAS  Google Scholar 

  114. Soignet SL (2001) Clinical experience of arsenic trioxide in relapsed acute promyelocytic leukemia. Oncologist 6 Suppl 2:11–16

    Google Scholar 

  115. Soignet SL, Maslak P, Wang ZG, Jhanwar S, Calleja E, Dardashti LJ, Corso D, DeBlasio A, Gabrilove J, Scheinberg DA, Pandolfi PP, Warrell RPJ Jr (1998) Complete remission after treatment of acute promyelocytic leukemia with arsenic trioxide. N Engl J Med 339:1341–1348

    CrossRef  PubMed  CAS  Google Scholar 

  116. Stolz JF, Basu P, Santini JM, Oremland RS (2006) Arsenic and selenium in microbial metabolism. Annu Rev Microbiol 60:107–130

    CrossRef  PubMed  CAS  Google Scholar 

  117. Sun Y, Wong MD, Rosen BP (2001) Role of cysteinyl residues in sensing Pb(II), Cd(II), and Zn(II) by the plasmid pI258 CadC repressor. J Biol Chem 276:14955–14960

    CrossRef  PubMed  CAS  Google Scholar 

  118. Tauriainen S, Karp M, Chang W, Virta M (1998) Luminescent bacterial sensor for cadmium and lead. Biosens Bioelectron 13:931–938

    CrossRef  PubMed  CAS  Google Scholar 

  119. 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 

  120. van den Hoven RN, Santini JM (2004) Arsenite oxidation by the heterotroph Hydrogenophaga sp. str. NT-14: the arsenite oxidase and its physiological electron acceptor. Biochim Biophys Acta 1656:148–155

    CrossRef  CAS  Google Scholar 

  121. VanZile ML, Cosper NJ, Scott RA, Giedroc DP (2000) The zinc metalloregulatory protein Synechococcus PCC7942 SmtB binds a single zinc ion per monomer with high affinity in a tetrahedral coordination geometry. Biochemistry 39:11818–11829

    CrossRef  PubMed  CAS  Google Scholar 

  122. VanZile ML, Chen X, Giedroc DP (2002a) Allosteric negative regulation of smt O/P binding of the zinc sensor, SmtB, by metal ions: a coupled equilibrium analysis. Biochemistry 41:9776–9786

    CrossRef  PubMed  CAS  Google Scholar 

  123. VanZile ML, Chen X, Giedroc DP (2002b) Structural characterization of distinct α3N and α5 metal sites in the cyanobacterial zinc sensor SmtB. Biochemistry 41:9765–9775

    CrossRef  PubMed  CAS  Google Scholar 

  124. Walmsley AR, Zhou T, Borges-Walmsley MI, Rosen BP (1999) The ATPase mechanism of ArsA, the catalytic subunit of the arsenite pump. J Biol Chem 274:16153–16161

    CrossRef  PubMed  CAS  Google Scholar 

  125. Walmsley AR, Zhou T, Borges-Walmsley MI, Rosen BP (2001a) Antimonite regulation of the ATPase activity of ArsA, the catalytic subunit of the arsenical pump. Biochem J 360:589–597

    CrossRef  PubMed  CAS  Google Scholar 

  126. Walmsley AR, Zhou T, Borges-Walmsley MI, Rosen BP (2001b) A kinetic model for the action of a resistance efflux pump. J Biol Chem 276:6378–6391

    CrossRef  PubMed  CAS  Google Scholar 

  127. Willsky GR, Malamy MH (1980a) Characterization of two genetically separable inorganic phosphate transport systems in Escherichia coli. J Bacteriol 144:356–365

    PubMed  CAS  Google Scholar 

  128. Willsky GR, Malamy MH (1980b) Effect of arsenate on inorganic phosphate transport in Escherichia coli. J Bacteriol 144:366–374

    PubMed  CAS  Google Scholar 

  129. Wong MD, Lin YF, Rosen BP (2002) The soft metal ion binding sites in the Staphylococcus aureus pI258 CadC Cd(II)/Pb(II)/Zn(II)-responsive repressor are formed between subunits of the homodimer. J Biol Chem 277:40930–40936

    CrossRef  PubMed  CAS  Google Scholar 

  130. Wu J, Rosen BP (1991) The ArsR protein is a trans-acting regulatory protein. Mol Microbiol 5:1331–1336

    CrossRef  PubMed  CAS  Google Scholar 

  131. Wu J, Rosen BP (1993) Metalloregulated expression of the ars operon. J Biol Chem 268:52–58

    PubMed  CAS  Google Scholar 

  132. Wu J, Tisa LS, Rosen BP (1992) Membrane topology of the ArsB protein, the membrane subunit of an anion-translocating ATPase. J Biol Chem 267:12570–12576

    PubMed  CAS  Google Scholar 

  133. Wysocki R, Chery CC, Wawrzycka D, Van Hulle M, Cornelis R, Thevelein JM, Tamás MJ (2001) The glycerol channel Fps1p mediates the uptake of arsenite and antimonite in Saccharomyces cerevisiae. Mol Microbiol 40:1391–1401

    CrossRef  PubMed  CAS  Google Scholar 

  134. Xu C, Rosen BP (1999) Metalloregulation of soft metal resistance pumps. In: Sarkar B (ed) Metals and genetics. Plenum, New York, pp 5–19

    Google Scholar 

  135. Xu C, Shi W, Rosen BP (1996) The chromosomal arsR gene of Escherichia coli encodes a trans-acting metalloregulatory protein. J Biol Chem 271:2427–2432

    CrossRef  PubMed  CAS  Google Scholar 

  136. Yang HC, Cheng J, Finan TM, Rosen BP, Bhattacharjee H (2005) Novel pathway for arsenic detoxification in the legume symbiont Sinorhizobium meliloti. J Bacteriol 187:6991–6997

    CrossRef  PubMed  CAS  Google Scholar 

  137. Ye J, Kandegedara A, Martin P, Rosen BP (2005) Crystal structure of the Staphylococcus aureus pI258 CadC Cd(II)/Pb(II)/Zn(II)-responsive repressor. J Bacteriol 187:4214–4221

    CrossRef  PubMed  CAS  Google Scholar 

  138. Zegers I, Martins JC, Willem R, Wyns L, Messens J (2001) Arsenate reductase from S. aureus plasmid pI258 is a phosphatase drafted for redox duty. Nat Struct Biol 8:843–847

    CrossRef  PubMed  CAS  Google Scholar 

  139. Zhou T, Rosen BP (1997) Tryptophan fluorescence reports nucleotide-induced conformational changes in a domain of the ArsA ATPase. J Biol Chem 272:19731–19737

    CrossRef  PubMed  CAS  Google Scholar 

  140. Zhou T, Liu S, Rosen BP (1995) Interaction of substrate and effector binding sites in the ArsA ATPase. Biochemistry 34:13622–13626

    CrossRef  PubMed  CAS  Google Scholar 

  141. Zhou T, Radaev S, Rosen BP, Gatti DL (2000) Structure of the ArsA ATPase: the catalytic subunit of a heavy metal resistance pump. Embo J 19:4838–4845

    CrossRef  PubMed  CAS  Google Scholar 

  142. Zhou T, Radaev S, Rosen BP, Gatti DL (2001) Conformational changes in four regions of the Escherichia coli ArsA ATPase link ATP hydrolysis to ion translocation. J Biol Chem 276:30414–30422

    CrossRef  PubMed  CAS  Google Scholar 

  143. Zhou T, Shen J, Liu Y, Rosen BP (2002) Unisite and multisite catalysis in the ArsA ATPase. J Biol Chem 277:23815–23820

    CrossRef  PubMed  CAS  Google Scholar 

  144. Zhou Y, Messier N, Ouellette M, Rosen BP, Mukhopadhyay R (2004) Leishmania major LmACR2 is a pentavalent antimony reductase that confers sensitivity to the drug pentostam. J Biol Chem 279:37445–37451

    CrossRef  PubMed  CAS  Google Scholar 

  145. Zhou Y, Bhattacharjee H, Mukhopadhyay R (2006) Bifunctional role of the leishmanial antimonate reductase LmACR2 as a protein tyrosine phosphatase. Mol Biochem Parasitol 148:161–168

    CrossRef  PubMed  CAS  Google Scholar 

  146. Zuniga S, Boskovic J, Jimenez A, Ballesta JP, Remacha M (1999) Disruption of six Saccharomyces cerevisiae novel genes and phenotypic analysis of the deletants. Yeast 15:945–953

    CrossRef  PubMed  CAS  Google Scholar 

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  1. Department of Biochemistry and Molecular Biology, Wayne State University School of Medicine, 540 E. Canfield Avenue, 48201, Detroit, MI, USA

    Hiranmoy Bhattacharjee & Barry P. Rosen

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  1. Hiranmoy Bhattacharjee
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Dietrich H. Nies Simon Silver

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Bhattacharjee, H., Rosen, B.P. (2007). Arsenic Metabolism in Prokaryotic and Eukaryotic Microbes. In: Nies, D.H., Silver, S. (eds) Molecular Microbiology of Heavy Metals. Microbiology Monographs, vol 6. Springer, Berlin, Heidelberg. https://doi.org/10.1007/7171_2006_086

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