Linking selenium biogeochemistry to the sulfur-dependent biological detoxification of arsenic

Environmental Microbiology

Volumn 14, Issue 7, 2012, Pages 1612-1623

  Couture, Raoul Marie ^a   Sekowska, Agnieszka ^b   Fang, Gang ^c   Danchin, Antoine ^b,d  

^a UNIVERSITY OF WATERLOO   (Canada)

^b AMAbiotics SAS   (France)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

[No Author keywords available]

Indexed keywords

ARSENIC; BACTERIAL PROTEIN; SELENIUM; SULFUR;

BACTERIUM; CHEMISTRY; DRUG DETOXIFICATION; GENETICS; METABOLISM; METHYLATION; OXIDATION REDUCTION REACTION; SHORT SURVEY;

ARSENIC; BACTERIA; BACTERIAL PROTEINS; METABOLIC DETOXICATION, DRUG; METHYLATION; OXIDATION-REDUCTION; SELENIUM; SULFUR;

BACTERIA (MICROORGANISMS);

EID: 84863191969     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2012.02758.x     Document Type: Short Survey

References (105)

1. Akter, K.F., Owens, G., Davey, D.E., and Naidu, R. (2005) Arsenic speciation and toxicity in biological systems. Rev Environ Contam Toxicol 184: 97-149.
2. Arsene-Ploetze, F., Koechler, S., Marchal, M., Coppee, J.Y., Chandler, M., Bonnefoy, V., etal. (2010) Structure, function, and evolution of the Thiomonas spp. genome. PLoS Genet 6: e1000859.
3. Barbe, V., Cruveiller, S., Kunst, F., Lenoble, P., Meurice, G., Sekowska, A., etal. (2009) From a consortium sequence to a unified sequence: the Bacillus subtilis 168 reference genome a decade later. Microbiology 155: 1758-1775.
4. Bayard, R., Chatain, V., Gachet, C., Troadec, A., and Gourdon, R. (2006) Mobilisation of arsenic from a mining soil in batch slurry experiments under bio-oxidative conditions. Water Res 40: 1240-1248.
5. Benson, A.A., and Summons, R.E. (1981) Arsenic accumulation in Great Barrier Reef invertebrates. Science 211: 482-483.
6. Bentley, R., and Chasteen, T.G. (2002) Microbial methylation of metalloids: arsenic, antimony, and bismuth. Microbiol Mol Biol Rev 66: 250-271.
7. Cai, L., Rensing, C., Li, X., and Wang, G. (2009) Novel gene clusters involved in arsenite oxidation and resistance in two arsenite oxidizers: Achromobacter sp. SY8 and Pseudomonas sp. TS44. Appl Microbiol Biotechnol 83: 715-725.
8. Challenger, F. (1951) Biological methylation. Adv Enzymol Relat Subj Biochem 12: 429-491.
9. Chen, P., Yan, L., Leng, F., Nan, W., Yue, X., Zheng, Y., etal. (2011) Bioleaching of realgar by Acidithiobacillus ferrooxidans using ferrous iron and elemental sulfur as thesole and mixed energy sources. Bioresour Technol 102: 3260-3267.
10. Couture, R.-M., and Van Cappellen, P. (2011) Reassessing the role of sulfur geochemistry on arsenic speciation in reducing environments. J Hazard Mater 189: 647-652.
11. Cutter, G.A. (1982) Selenium in reducing waters. Science 217: 829-831.
12. Danchin, A. (2010) Science and arsenic fool's gold: a toxic broth. J Cosmol 13: 3617-3620.
13. Dani, S.U. (2011) The arsenic for phosphorus swap is accidental, rather than a facultative one, and the question whether arsenic is nonessential or toxic is quantitative, not a qualitative one. Sci Total Environ 409: 4889-4890.
14. Dembitsky, V.M., and Levitsky, D.O. (2004) Arsenolipids. Prog Lipid Res 43: 403-448.
15. Doblin, M.A., Baines, S.B., Cutter, L.S., and Cutter, G.A. (2006) Sources and biogeochemical cycling of particulate selenium in the San Francisco Bay estuary. Est Coast Shelf Sci 67: 681-694.
16. Dopson, M., Lindstrom, E.B., and Hallberg, K.B. (2001) Chromosomally encoded arsenical resistance of the moderately thermophilic acidophile Acidithiobacillus caldus. Extremophiles 5: 247-255.
17. Drobna, Z., Naranmandura, H., Kubachka, K.M., Edwards, B.C., Herbin-Davis, K., Styblo, M., etal. (2009) Disruption of the arsenic (+3 oxidation state) methyltransferase gene in the mouse alters the phenotype for methylation of arsenic and affects distribution and retention of orally administered arsenate. Chem Res Toxicol 22: 1713-1720.
18. Edmonds, J.S., and Francesconi, K.A. (1987) Transformations of arsenic in the marine environment. Experientia 43: 553-557.
19. Fekry, M.I., Tipton, P.A., and Gates, K.S. (2011) Kinetic consequences of replacing the internucleotide phosphorus atoms in DNA with arsenic. ACS Chem Biol 6: 127-130.
20. Franz, A.K. (2007) The synthesis of biologically active organosilicon small molecules. Curr Opin Drug Discov Devel 10: 654-671.
21. Garelick, H., Jones, H., Dybowska, A., and Valsami-Jones, E. (2008) Arsenic pollution sources. Rev Environ Contam Toxicol 197: 17-60.
22. Glass, R.S., Singh, W.P., Jung, W., Veres, Z., Scholz, T.D., and Stadtman, T.C. (1993) Monoselenophosphate: synthesis, characterization, and identity with the prokaryotic biological selenium donor, compound SePX. Biochemistry 32: 12555-12559.
23. Haft, D.H., and Self, W.T. (2008) Orphan SelD proteins and selenium-dependent molybdenum hydroxylases. Biol Direct 3: 4.
24. Hansen, H.R., Jaspars, M., and Feldmann, J. (2004) Arsinothioyl-sugars produced by in vitro incubation of seaweed extract with liver cytosol analysed by HPLC coupled simultaneously to ES-MS and ICP-MS. Analyst 129: 1058-1064.
25. Härtig, C., and Planer-Friedrich, B. (2012) Thioarsenate transformation by filamentous microbial mats thriving in an alkaline, sulfidic hot spring. Environ Sci Technol. DOI: 10.1021/es204277j.
26. Helz, G.R., and Tossell, J.A. (2008) Thermodynamic model for arsenic speciation in sulfidic waters: a novel use of ab initio computations. Geochim Cosmochim Acta 72: 4457-4468.
27. Hoeft, S.E., Kulp, T.R., Han, S., Lanoil, B., and Oremland, R.S. (2010) Coupled arsenotrophy in a hot spring photosynthetic biofilm at Mono Lake, California. Appl Environ Microbiol 76: 4633-4639.
28. Iciek, M., and Wlodek, L. (2001) Biosynthesis and biological properties of compounds containing highly reactive, reduced sulfane sulfur. Pol J Pharmacol 53: 215-225.
29. Izquierdo, A., Casas, C., and Herrero, E. (2010) Selenite-induced cell death in Saccharomyces cerevisiae: protective role of glutaredoxins. Microbiology 156: 2608-2620.
30. Johnston, D.T., Farquhar, J., Habicht, K.S., and Canfield, D.E. (2008) Sulphur isotopes and the search for life: strategies for identifying sulphur metabolisms in the rock record and beyond. Geobiology 6: 425-435.
31. Khersonsky, O., and Tawfik, D.S. (2010) Enzyme promiscuity: a mechanistic and evolutionary perspective. Annu Rev Biochem 79: 471-505.
32. Kulp, T.R., Hoeft, S.E., Miller, L.G., Saltikov, C., Murphy, J.N., Han, S., etal. (2006) Dissimilatory arsenate and sulfate reduction in sediments of two hypersaline, arsenic-rich soda lakes: Mono and Searles Lakes, California. Appl Environ Microbiol 72: 6514-6526.
33. Langner, P., Mikutta, C., and Kretzschmar, R. (2012) Arsenic sequestration by organic sulphur in peat. Nature Geosci 5: 66-73.
34. Lattanzi, P., Da Pelo, S., Musu, E., Atzei, D., Elsener, B., Fantauzzi, M., and Rossi, A. (2008) Enargite oxidation: a review. Earth Sci Rev 86: 62-88.
35. Leisser, H. (2007) Column experiments simulating various scenarios for arsenic mobilisation in Bangladesh. Diploma Thesis. Bayreuth, Germany: Universität Bayreuth.
36. Leonard, A., and Lauwerys, R.R. (1980) Carcinogenicity, teratogenicity and mutagenicity of arsenic. Mutat Res 75: 49-62.
37. Leufroy, A., Noel, L., Dufailly, V., Beauchemin, D., and Guerin, T. (2011) Determination of seven arsenic species in seafood by ion exchange chromatography coupled to inductively coupled plasma-mass spectrometry following microwave assisted extraction: method validation and occurrence data. Talanta 83: 770-779.
38. Lin, S., Shi, Q., Nix, F.B., Styblo, M., Beck, M.A., Herbin-Davis, K.M., etal. (2002) A novel S-adenosyl-L-methionine:arsenic(III) methyltransferase from rat liver cytosol. J Biol Chem 277: 10795-10803.
39. Lin, Y.F., Walmsley, A.R., and Rosen, B.P. (2006) An arsenic metallochaperone for an arsenic detoxification pump. Proc Natl Acad Sci USA 103: 15617-15622.
40. Llorente-Mirandes, T., Ruiz-Chancho, M.J., Barbero, M., Rubio, R., and Lopez-Sanchez, J.F. (2010) Measurement of arsenic compounds in littoral zone algae from the Western Mediterranean Sea. Occurrence of arsenobetaine. Chemosphere 81: 867-875.
41. Lopez, P.J., Descles, J., Allen, A.E., and Bowler, C. (2005) Prospects in diatom research. Curr Opin Biotechnol 16: 180-186.
42. Macy, J.M., Nunan, K., Hagen, K.D., Dixon, D.R., Harbour, P.J., Cahill, M., and Sly, L.I. (1996) Chrysiogenes arsenatis gen. nov., sp. nov., a new arsenate-respiring bacterium isolated from gold mine wastewater. Int J Syst Bacteriol 46: 1153-1157.
43. Martin, A.J., Simpson, S., Fawcett, S., Wiramanaden, C.I.E., Pickering, I.J., Belzile, N., etal. (2011) Biogeochemical mechanisms of selenium exchange between water andsediments in two contrasting lentic environments. Environ Sci Technol 45: 2605-2612.
44. de Melo Pereira, G.V., Magalhaes, K.T., Lorenzetii, E.R., Souza, T.P., and Schwan, R.F. (2012) A multiphasic approach for the identification of endophytic bacterial in strawberry fruit and their potential for plant growth promotion. Microb Ecol 63: 405-417.
45. Mestrot, A., Merle, J.K., Broglia, A., Feldmann, J., and Krupp, E.M. (2011) Atmospheric stability of arsine and methylarsines. Environ Sci Technol 45: 4010-4015.
46. Molin, M., Ulven, S.M., Dahl, L., Telle-Hansen, V.H., Holck, M., Skjegstad, G., etal. (2012) Humans seem to produce arsenobetaine and dimethylarsinate after a bolus dose of seafood. Environ Res 112: 28-39.
47. Motchnik, P.A., and Tappel, A.L. (1990) Multiple selenocysteine content of selenoprotein P in rats. J Inorg Biochem 40: 265-269.
48. Muller, D., Medigue, C., Koechler, S., Barbe, V., Barakat, M., Talla, E., etal. (2007) A tale of two oxidation states: bacterial colonization of arsenic-rich environments. PLoS Genet 3: e53.
49. Navas-Acien, A., Francesconi, K.A., Silbergeld, E.K., and Guallar, E. (2010) Seafood intake and urine concentrations of total arsenic, dimethylarsinate and arsenobetaine in the US population. Environ Res 111: 110-118.
50. Newman, W.R. (1991) The Summa Perfectionis and Late Medieval Alchemy: A Critical Edition, Translation and Study. Leiden, The Netherlands: EJ Brill Academic Publishers.
51. Nielsen, F.H. (1991) Nutritional requirements for boron, silicon, vanadium, nickel, and arsenic: current knowledge and speculation. FASEB J 5: 2661-2667.
52. Ninh, T.D., Nagashima, Y., and Shiomi, K. (2007) Water-soluble and lipid-soluble arsenic compounds in japanese flying squid Todarodes pacificus. J Agric Food Chem 55: 3196-3202.
53. Nriagu, J.O., and Pacyna, J.M. (1988) Quantitative assessment of worldwide contamination of air, water and soils by trace metals. Nature 333: 134-139.
54. O'Day, P.A., Vlassopoulos, D., Root, R., and Rivera, N. (2004) The influence of sulfur and iron on dissolved arsenic concentrations in the shallow subsurface under changing redox conditions. Proc Natl Acad Sci USA 101: 13703-13708.
55. Orthaber, A., Sax, A.F., and Francesconi, K.A. (2012) Oxygen versus sulfur: structure and reactivity of substituted arsine oxides and arsine sulfides. J Comput Chem 33: 112-117.
56. Paez-Espino, D., Tamames, J., de Lorenzo, V., and Canovas, D. (2009) Microbial responses to environmental arsenic. Biometals 22: 117-130.
57. Pedersen, K., Ekendahl, S., Tullborg, E.L., Furnes, H., Thorseth, I., and Tumyr, O. (1997) Evidence of ancient life at 207 m depth in a granitic aquifer. Geology 25: 827-830.
58. Perry, C.C., and Keeling-Tucker, T. (2000) Biosilicification: the role of the organic matrix in structure control. J Biol Inorg Chem 5: 537-550.
59. Pettine, M., Gennari, F., Campanella, L., Casentini, B., and Marani, D. (2012) Environmental selenium research: from microscopic processes to global understanding. Geochim Cosmochim Acta 83: 37-47.
60. Phung, L.T., Silver, S., Trimble, W.L., and Gilbert, J. (2011) The Halomonas Sp. GFAJ-1 Whole Genome Shotgun (WGS) Project In GenBank. Bethesda, USA: NCBI.
61. Pierce, B.L., Kibriya, M.G., Tong, L., Jasmine, F., Argos, M., Roy, S., etal. (2012) Genome-wide association study identifies chromosome 10q24.32 variants associated with arsenic metabolism and toxicity phenotypes in bangladesh. PLoS Genet 8: e1002522.
62. Planer-Friedrich, B., and Wallschläger, D. (2009) A critical investigation of hydride generation-based arsenic speciation in sulfidic waters. Environ Sci Technol 43: 5007-5013.
63. Planer-Friedrich, B., London, J., McCleskey, R.B., Nordstrom, D.K., and Wallschläger, D. (2007) Thioarsenates in geothermal waters of Yellowstone National Park:? Determination, preservation, and geochemical importance. Environ Sci Technol 41: 5245-5251.
64. Planer-Friedrich, B., Franke, D., Merkel, B., and Wallschlager, D. (2008) Acute toxicity of thioarsenates to Vibrio fischeri. Environ Toxicol Chem 27: 2027-2035.
65. Planer-Friedrich, B., Fisher, J.C., Hollibaugh, J.T., Sab, E., and Wallschläger, D. (2009) Oxidative transformation of trithioarsenate along alkaline geothermal drainages-abiotic versus microbially mediated processes. Geomicrobiol J 26: 339-350.
66. Planer-Friedrich, B., Suess, E., Scheinost, A.C., and Wallschläger, D. (2010) Arsenic speciation in sulfidic waters: reconciling contradictory spectroscopic and chromatographic evidence. Anal Chem 82: 10228-10235.
67. Plant, J.A., Kinniburgh, D.G., Smedley, P.L., Fordyce, F.M., Klinck, B.A., Heinrich, D.H., and Karl, K.T. (2003) Arsenic and selenium. In Treatise on Geochemistry. Holland, H.D., and Turekian, K.K. (eds). Oxford, UK: Elsevier-Pergamon, pp. 17-66.
68. Qin, J., Rosen, B.P., Zhang, Y., Wang, G., Franke, S., and 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.
69. Raber, G., Khoomrung, S., Taleshi, M.S., Edmonds, J.S., and Francesconi, K.A. (2009) Identification of arsenolipids with GC/MS. Talanta 78: 1215-1218.
70. Rosen, B.P., and Tamas, M.J. (2010) Arsenic transport in prokaryotes and eukaryotic microbes. Adv Exp Med Biol 679: 47-55.
71. Ruangwises, S., and Ruangwises, N. (2011) Concentrations of total and inorganic arsenic in fresh fish, mollusks, and crustaceans from the Gulf of Thailand. J Food Prot 74: 450-455.
72. Sato, T., and Kobayashi, Y. (1998) The ars operon in the skin element of Bacillus subtilis confers resistance to arsenate and arsenite. J Bacteriol 180: 1655-1661.
73. Schmeisser, E., Goessler, W., and Francesconi, K.A. (2006) Human metabolism of arsenolipids present in cod liver. Anal Bioanal Chem 385: 367-376.
74. Schwedt, G., and Rieckhoff, M. (1996) Separation of thio- and oxothioarsenates by capillary zone electrophoresis and ion chromatography. J Chromatogr A 736: 341-350.
75. Seby, F., Potin-Gautier, M., Giffaut, E., Borge, G., and Donard, O.F.X. (2001) A critical review of thermodynamic data for selenium species at 25 degrees C. Chem Geol 171: 173-194.
76. Sekowska, A., Kung, H.F., and Danchin, A. (2000) Sulfur metabolism in Escherichia coli and related bacteria: facts and fiction. J Mol Microbiol Biotechnol 2: 145-177.
77. Sekowska, A., Denervaud, V., Ashida, H., Michoud, K., Haas, D., Yokota, A., and Danchin, A. (2004) Bacterial variations on the methionine salvage pathway. BMC Microbiol 4: 9.
78. Shi, R., Proteau, A., Villarroya, M., Moukadiri, I., Zhang, L., Trempe, J.F., etal. (2010) Structural basis for Fe-S cluster assembly and tRNA thiolation mediated by IscS protein-protein interactions. PLoS Biol 8: e1000354.
79. Slaughter, D.C., Macur, R.E., and Inskeep, W.P. (2011) Inhibition of microbial arsenate reduction by phosphate. Microbiol Res 167: 151-156.
80. Smedley, P.L., and Kinniburgh, D.G. (2002) A review of the source, behaviour and distribution of arsenic in natural waters. Appl Geochem 17: 517-568.
81. Stolz, J.F., Basu, P., Santini, J.M., and Oremland, R.S. (2006) Arsenic and selenium in microbial metabolism. Annu Rev Microbiol 60: 107-130.
82. Su, D., Ojo, T.T., Soll, D., and Hohn, M.J. (2012) Selenomodification of tRNA in archaea requires a bipartite rhodanese enzyme. FEBS Lett 586: 717-721.
83. Suess, E. (2011) Investigations towards a better understanding of arsenic-sulfur speciation in aquatic environments: formation, stability, structural characterization, and conflicting analyses. PhD Thesis. Bayreuth, Germany: Universität Bayreuth, p. 98.
84. Suess, E., Scheinost, A.C., Bostick, B.C., Merkel, B.J., Wallschläger, D., and Planer-Friedrich, B. (2009) Discrimination of thioarsenites and thioarsenates by X-ray absorption spectroscopy. Anal Chem 81: 8318-8326.
85. Suess, E., Wallschläger, D., and Planer-Friedrich, B. (2011) Stabilization of thioarsenates in iron-rich waters. Chemosphere 83: 1524-1531.
86. Switzer Blum, J., Burns Bindi, A., Buzzelli, J., Stolz, J.F., and Oremland, R.S. (1998) Bacillus arsenicoselenatis, sp. nov., and Bacillus selenitireducens, sp. nov.: two haloalkaliphiles from Mono Lake, California that respire oxyanions of selenium and arsenic. Arch Microbiol 171: 19-30.
87. Taleshi, M.S., Edmonds, J.S., Goessler, W., Ruiz-Chancho, M.J., Raber, G., Jensen, K.B., and Francesconi, K.A. (2010) Arsenic-containing lipids are natural constituents of sashimi tuna. Environ Sci Technol 44: 1478-1483.
88. Tamaki, S., and Frankenberger, W.T., Jr (1992) Environmental biochemistry of arsenic. Rev Environ Contam Toxicol 124: 79-110.
89. Veres, Z., Tsai, L., Scholz, T.D., Politino, M., Balaban, R.S., and Stadtman, T.C. (1992) Synthesis of 5-methylaminomethyl-2-selenouridine in tRNAs: 31P NMR studies show the labile selenium donor synthesized by the selD gene product contains selenium bonded to phosphorus. Proc Natl Acad Sci USA 89: 2975-2979.
90. Vlassopoulos, D., Bessinger, B., and O'Day, P. (2010) Aqueous solubility of As2S3 and thermodynamic stability of thioarsenites. In 13th International Symposium on Water-Rock Interaction, WRI-13. Birlke, P., and Torress-Alvarado, I.S. (eds). Guanajuato, Mexico: Mexico Taylor & Francis Group, pp. 323-327.
91. Waxman, S., and Anderson, K.C. (2001) History of the development of arsenic derivatives in cancer therapy. Oncologist 6 (Suppl. 2): 3-10.
92. 3 and speciation of As in dilute and sulfide-bearing fluids at 25 and 90°C. Geochim Cosmochim Acta 54: 1009-1017.
93. Wen, H., and Carignan, J. (2011) Selenium isotopes trace the source and redox processes in the black shale-hosted Se-rich deposits in China. Geochim Cosmochim Acta 75: 1411-1427.
94. Wilkin, R.T., Wallschläger, D., and Ford, R.G. (2003) Speciation of arsenic in sulfidic waters. Geochem Trans 4: 1-7.
95. Winkel, L., Johnson, C., Lenz, M., Grundl, T., Leupin, O., Amini, M., and Charlet, L. (2011) Environmental selenium research: from microscopic processes to global understanding. Environ Sci Technol 46: 571-579.
96. Wolfe-Simon, F., Switzer Blum, J., Kulp, T.R., Gordon, G.W., Hoeft, S.E., Pett-Ridge, J., etal. (2010) A bacterium that can grow by using arsenic instead of phosphorus. Science 332: 1163-1166.
97. Wu, B., Song, J., and Beitz, E. (2010) Novel channel enzyme fusion proteins confer arsenate resistance. J Biol Chem 285: 40081-40087.
98. Yang, H.C., Cheng, J., Finan, T.M., Rosen, B.P., and Bhattacharjee, H. (2005) Novel pathway for arsenic detoxification in the legume symbiont Sinorhizobium meliloti. J Bacteriol 187: 6991-6997.
99. Yin, X.X., Chen, J., Qin, J., Sun, G.X., Rosen, B.P., and Zhu, Y.G. (2011) Biotransformation and volatilization of arsenic by three photosynthetic cyanobacteria. Plant Physiol 156: 1631-1638.
100. Yoshinaga, M., Cai, Y., and Rosen, B.P. (2011) Demethylation of methylarsonic acid by a microbial community. Environ Microbiol 13: 1205-1215.
101. Zakharyan, R., Wu, Y., Bogdan, G.M., and Aposhian, H.V. (1995) Enzymatic methylation of arsenic compounds: assay, partial purification, and properties of arsenite methyltransferase and monomethylarsonic acid methyltransferase of rabbit liver. Chem Res Toxicol 8: 1029-1038.
102. Zargar, K., Hoeft, S., Oremland, R., and Saltikov, C.W. (2010) Identification of a novel arsenite oxidase gene, arxA, in the haloalkaliphilic, arsenite-oxidizing bacterium Alkalilimnicola ehrlichii strain MLHE-1. J Bacteriol 192: 3755-3762.
103. Zerkle, A., House, C., and Brantley, S. (2005) Biogeochemical signatures through time as inferred from whole microbial genomes. Am J Sci 305: 467-502.
104. Zhang, S. (2004) Oxidation of Refractory Gold Concentrates and Simultaneous Dissolution of Fold in Aerated Alkaline Solutions. Bayreuth, Germany: Murdoch University, p. 358.
105. Zhang, Y., Turanov, A.A., Hatfield, D.L., and Gladyshev, V.N. (2008) In silico identification of genes involved in selenium metabolism: evidence for a third selenium utilization trait. BMC Genomics 9: 251.