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Bacterial Metabolism of Selenium—For Survival or Profit

  • Lucian C. StaicuEmail author
  • Larry L. Barton
Chapter

Abstract

Selenium (Se) is transformed by phylogenetically diverse bacteria following several basic strategies which include: (1) satisfying a trace element requirement for bacterial synthetic machinery (assimilatory metabolism), (2) cellular energy production coupled to oxidation/reduction reactions (dissimilatory metabolism), and (3) detoxification processes. Some bacteria can use Se for respiration under limiting anaerobic conditions, generating energy to sustain growth. Under aerobic conditions, Se behaves as a toxicant and bacteria have evolved different strategies to counteract it. An important detoxification mechanism involves the formation of Se nanoparticles with a diminished toxic potential, but the cells have to properly manage these products in order to maintain their integrity. The bacterial metabolism of Se can be regarded as a survival mechanism when Se compounds prove to be highly toxic. Secondly, selenium is used to obtain energy in a nutrient-depleted environment, therefore allowing to specialized bacterial species to prevail over competitors that cannot exploit this resource. To achieve the Se metabolic activities, numerous unique enzymes are employed. While some enzymes have been isolated and are markedly specific for Se, many of the Se enzymes remain to be isolated. The formation of Se nanoparticles inside bacteria and the transportation mechanisms to the extracellular environment are still under debate. Se nanoparticles do not appear to play a nutritional (energy storage) or ecological function for bacteria, being by-products of bacterial metabolism. However, from a biotechnological standpoint, these conversions could be used to (1) clean up industrial effluents rich in Se and (2) to produce biomaterials with industrial applications (biofactory).

Keywords

Selenium Bacterial metabolism Dissimilatory selenate reduction Selenium toxicity Selenium nanoparticles Biotechnology 

Abbreviations

DSeR

Dissimilatory selenate reduction

GSH

Glutathione

M

Molar

NAD+

Nicotinamide adenine dinucleotide

NP

Nanoparticle

QD

Quantum dots

ROS

Reactive oxygen species

Se

Selenium

Se0

Elemental selenium (zero valence state)

Se(IV)

Selenite, SeO3 2−

Se(VI)

Selenate, SeO4 2−

Sec

Selenocysteine

SefA

Selenium factor A

SeMet

Selenomethionine

SeOx

Selenium oxyanions (selenite and selenate)

SerABC

Selenate reductase isolated from Thauera selenatis

SOD

Superoxide dismutase

SRB

Sulfate-reducing bacteria

References

  1. Afkar E, Lasak J, Saltikov C, Basu P, Oremland RS, Stolz JF (2003) The respiratory arsenate reductase from Bacillus selenitireducens strain MLS10. FEMS Microbiol Lett 226:107–112CrossRefGoogle Scholar
  2. Barton LL, Nuttall HE Jr, Blake RC II (1994) Biocolloid formation: an approach to bioremediation of toxic metal wastes. In: Wise DL, Trantolo DJ (eds) Remediation of hazardous waste contaminated soils. Marcel Dekker, New York, USAGoogle Scholar
  3. Barton LL, Fauque GD (2009) Biochemistry, physiology and biotechnology of sulfate-reducing bacteria. Adv Appl Microbiol 68:41–98CrossRefGoogle Scholar
  4. Barton LL, Tomei-Torres FA, Xu H, Zocco T (2014) Nanoparticles formed by microbial metabolism of metals and minerals. In: Barton LL, Bazylinski DA, Hufang Xu (eds) Nanomicrobiology—physiological and environmental characteristics. Springer, New York, USAGoogle Scholar
  5. Bebien M, Chauvin J-P, Adriano J-M, Grosse S, Vermeglio A (2001) Effect of selenite on growth and protein synthesis in the phototrophic bacterium Rhodobacter sphaeroides. Appl Environ Microbiol 6:4440–4447CrossRefGoogle Scholar
  6. Bebien M, Kirsch J, Mejean V, Vermeglio A (2002a) Involvement of a putative molybdenum enzyme in the rediction of selenate by Escherichia coli. Microbiol 148:3865–3872CrossRefGoogle Scholar
  7. Bebien M, Lagniel G, Garin J, Touati D, Vermeglio A, Labarre J (2002b) Involvement of superoxide dismutases in the response of Escherichia coli to selenium oxides. J Bacteriol 184:1556–1564CrossRefGoogle Scholar
  8. Blake RC II, Choate DM, Bardhan S, Revis N, Barton LL, Zocco TG (1993) Chemical transformation of toxic metals by a Pseudomonas strain from a toxic waste site. Environ Toxicol Chem 1:1365–1376CrossRefGoogle Scholar
  9. Brown TA, Shrift A (1980) Assimilation of selenate and selenite by Salmonella typhimurium. Can J Microbiol 26:671–675CrossRefGoogle Scholar
  10. Bryant RD, Laishley EJ (1988) Evidence for two transporters of sulfur and selenium oxyanions in Clostridium pasteurianum. Can J Microbiol 34:700–703CrossRefGoogle Scholar
  11. Buchs B, Evangelou MWH, Winkel LHE, Lenz M (2013) Colloidal properties of nanoparticular biogenic selenium govern environmental fate and bioremediation effectiveness. Environ Sci Technol 47:2401–2407CrossRefGoogle Scholar
  12. Butler CS, Debieux CM, Dridge EJ, Splatt P, Wright M (2012) Biomineralization of selenium by the selenate-respiring bacterium Thauera selenatis. Biochem Soc Trans 40:1239–1243CrossRefGoogle Scholar
  13. Canstein Hv, Ogawa J, Shimizu S, Lloyd JR (2008) Secretion of flavins by Shewanella species and their role in extracellular electron transfer. Appl Environ Microbiol 74:615–623CrossRefGoogle Scholar
  14. Chapman PM, Adams WJ, Brooks M, Delos CG, Luoma SN, Maher WA, Ohlendorf HM, Presser TS, Shaw P (2010) Ecological assessment of selenium in the aquatic environments. SETAC Press, PensacolaCrossRefGoogle Scholar
  15. Debieux CM, Dridge EJ, Mueller CM, Splatt P, Paszkiewicz K, Knight I, Florance H, Love J, Titball RW, Lewis RJ, Richardson DJ, Butler CS (2011) A bacterial process for selenium nanospehere assembly. Proc Natl Acad Sci USA 108:13480–13485CrossRefGoogle Scholar
  16. Dobias J, Suvorova EI, Bernier-Latmani R (2011) Role of proteins in controlling selenium nanoparticle size. Nanotechnology 22:196505CrossRefGoogle Scholar
  17. DeMoll-Decker H, Macy JM (1993) The periplasmic nitrite reductase of Thauera selenatis may catalyze the reduction of selenite to elemental reduction. Arc Microbiol 160:241–247Google Scholar
  18. Doran JW (1982) Microorganisms and the biological cycling of selenium. Adv Microbiol Ecol 6:1–32CrossRefGoogle Scholar
  19. Doran JW, Alexander M (1977) Microbial transformations of selenium. Appl Environ Microbiol 33:31–37Google Scholar
  20. Dowdle PR, Oremland RS (1998) Microbial oxidation of elemental selenium in soil slurries and bacterial cultures. Environ Sci Technol 32:3749–3755CrossRefGoogle Scholar
  21. Dridge EJ, Watts CA, Jepson BJ, Line K, Santini JM, Richardson DJ, Butler CS (2007) Investigation of the redox centres of periplasmic selenate reductase from Thauera selenatis by EPR spectroscopy. Biochem J 408:19–28CrossRefGoogle Scholar
  22. Dridge EJ, Butler CS (2010) Thermostable properties of the periplasmic selenate reductase from Thauera selenatis. Biochimie 92:1268–1273CrossRefGoogle Scholar
  23. Dugan SR, Frankenberger WT Jr (2001) Factors affecting the volatilization of dimethylselenide by Enterobacter cloacae SLD1a-1. Soil Biol Biochem 32:1353–1358CrossRefGoogle Scholar
  24. Duran RS, Yates SR, Frankenberger WT Jr (2003) Transformations of selenate and selenite by Stenotrophomonas maltophilia isolated from a seleniferous agricultural drainage pond sediment. Environ Microbiol 5:287–295CrossRefGoogle Scholar
  25. Fernandez-Martinez A, Charlet L (2009) Selenium environmental cycling and bioavailability: a structural chemist point of view. Rev Environ Sci Biotechnol 8:81–110CrossRefGoogle Scholar
  26. Ganther HE (1968) Selenotrisulfides. Formation by reaction of thiols with selenious acid. Biochem 7:2898–2905CrossRefGoogle Scholar
  27. Garbisu C, Ishii T, Leighton T, Buchanan BB (1996) Bacterial reduction of selenite to elemental selenium. Chem Geol 132:199–204CrossRefGoogle Scholar
  28. Garbisu C, Carlson D, Adamkiewicz M, Yee BC, Wong JH, Resto E, Leighton T, Buchanan BB (1999) Morphological and biochemical responses of Bacillus subtilis to selenite stress. BioFactors 10:311–319CrossRefGoogle Scholar
  29. Guzzo J, Dubow MS (2000) A novel selenite- and tellurite-inducible gene in Escherichia coli. Appl Environ Microbiol 66:4972–4978CrossRefGoogle Scholar
  30. Hamilton SJ (2004) Review of selenium toxicity in the aquatic food chain. Sci Total Environ 326:1–31CrossRefGoogle Scholar
  31. Herbel MJ, Blum JS, Borglin SE, Oremland RS (2003) Reduction of elemental selenium to selenide: experiments with anoxic sediments and bacteria that respire Se-oxyanions. Geomicrobiol J 20:587–602Google Scholar
  32. Hoffman DJ (2002) Role of selenium toxicity and oxidative stress in aquatic birds. Aquat Toxicol 57:11–26CrossRefGoogle Scholar
  33. Huber R, Sacher M, Vollmann A, Huber H, Rose D (2000) Respiration of arsenate and selenite by hyperthermophilic archaea. Syst Appl Microbiol 23:305–314CrossRefGoogle Scholar
  34. Hunter WJ (2007) An Azospira oryzae (syn Dechlorosoma suillum) strain that reduces selenate and selenite to elemental red selenium. Curr Microbiol 54:376–381CrossRefGoogle Scholar
  35. Hunter WJ, Kuyendall LD (2007) Reduction of selenite to elemental red selenium by Rhizobium sp. Strain B1. Curr Microbiol 55:344–349CrossRefGoogle Scholar
  36. Hunter WJ, Manter DK (2008) Bio-reduction of selenite to elemental red selenium by Tetrathiobacter kashmirensis. Curr Microbiol 57:83–88CrossRefGoogle Scholar
  37. Hunter WJ, Manter (2009) Reduction of selenite to elemental red selenium by Pseudomonas sp. Strain CA5. Curr Microbiol 58:493–498CrossRefGoogle Scholar
  38. Hunter WJ (2014) Pseudomonas seleniipraecipitans proteins potentially involved in selenite reduction. Curr Microbiol 69:69–74CrossRefGoogle Scholar
  39. Kabata-Pendias A (2000) Trace elements in soil and plants, 3rd edn. CRC Press, Boca RatonGoogle Scholar
  40. Kessi J, Ramuz M, Wehrli E, Spycher M, Bachofen R (1999) Reduction of selenite and detoxification of elemental selenium by the phototrophic bacterium Rhodospirillum rubrum. Appl Environ Microbiol 65:4734–4740 Google Scholar
  41. Kessi J, Hanselmann KW (2004) Similarities between the abiotic reduction of selenite with glutathione and the dissimiltory reaction mediated by Rhodospirillum rubrum and Escherichia coli. J Biol Chem 279:50662–50669CrossRefGoogle Scholar
  42. Kessi J (2006) Enzymic systems proposed to be involved in the dissimilatory reduction of selenite in the purple non-sulfur bacteria Rhodospirillum rubrum and Rhodobacter capsulatus. Microbiology 15:731–743CrossRefGoogle Scholar
  43. Knight VV, Blakemore R (1998) Reduction of diverse electron acceptors by Aeromonas hydrophila. Arch Microbiol 169:239–248CrossRefGoogle Scholar
  44. Krafft T, Bowen A, Theis F, Macy JM (2000) Cloning and sequencing of the genes encoding the periplasmic-cytochrome b-containing selenate reductase of Thauera selenatis. DNA Sequation 10:365–377CrossRefGoogle Scholar
  45. Kramer GF, Ames BN (1988) Mechanisms of mutagenicity of sodium selenite (Na2SeO3) in Salmonella typhimurium. Mutat Res 201:169–180CrossRefGoogle Scholar
  46. Kuroda M, Yamashita M, Miwa E, Imao K, Fujimoto N, Ono H, Nagano K, Sei K, Ike M (2011) Molecular cloning and characterization of the srdBCA operon, encoding the respiratory selenate reductase complex, form the selenate-reducing bacterium Bacillus selenatarsenatis SF-1. J Bacteriol 193:2141–2148CrossRefGoogle Scholar
  47. Labunskyy VM, Hatfield DL, Gladyshev VN (2014) Selenoproteins: molecular pathways and physiological roles. Physiol Rev 94:739–777CrossRefGoogle Scholar
  48. Lai CY, Wen LL, Shi LD, Zhao KK, Wang YQ, Yang X, Rittmann BE, Zhou C, Tang Y, Zheng P, Zhao HP (2016) Selenate and nitrate bioreductions using methane as the electron donor in a membrane biofilm reactor. Environ Sci Technol 50:10179–10186CrossRefGoogle Scholar
  49. Laishley EJ, Harrison GI, Bryant RD, Krouse HR (1980) Influence of selenium compounds on reduction of sulphur compounds and associated sulphur isotope fractions in Clostridium pasteurianum. In: Trudinger PA, Walter MR, Ralph BJ (eds) Biogeochemistry of ancient and modern environments. Australian Academy of Sciences, Canberra, AustraliaGoogle Scholar
  50. Leifson E (1939) New selenite selective enrichment medium for the isolation of typhoid and paratyphoid bacilli. Am J Hyg 24:423–432Google Scholar
  51. Lemly AD (2002) Symptoms and implications of selenium toxicity in fish: the Belews Lake case example. Aquat Toxicol 57:39–49CrossRefGoogle Scholar
  52. Lenz M, Kolvenbach B, Gygax B, Moes S, Corvinni PFX (2011) Shedding light on selenium biomineralization: proteins associated with bionanominerals. Appl Environ Microb 77:4676–4680CrossRefGoogle Scholar
  53. Li D-B, Cheng Y-Y, Wu C, Li W-W, Li N, Yang Z-C, Tong Z-H, Yu H-Q (2014) Selenite reduction by Shewanella oneidensis MR-1 is mediated by fumarate reductase in periplasm. Sci Rep 4:3735CrossRefGoogle Scholar
  54. Losi ME, Frankenberger WT (1997) Reduction of selenium oxyanions by Enterobacter cloacae SLD1a-1: isolation and growth of the bacterium and its expulsion of selenium particles. Appl Environ Microbiol 63:3079–3084Google Scholar
  55. Lovley DR (1993) Dissimilatory metal reduction. Ann Rev Microbiol 47:263–290CrossRefGoogle Scholar
  56. Lowe EC, Bydder S, Hartshorne RS, Tape HL, Dridge EJ, Debieux CM, Paszkiewicz K, Singleton I, Lewis RJ, Santini JM, Richardson DJ, Butler CS (2010) Quinol-cytochrome c oxidoreductase and cytochrome c4 mediate electron transfer during selenate respiration in Thauera selenatis. J Biol Chem 285:18433–18442CrossRefGoogle Scholar
  57. Luoma SN, Johns C, Fisher NS, Steinberg NA, Oremland RS, Reinfelder JR (1992) Determination of selenium bioavailability to a bivalve from particulate and solute pathways. Environ Sci Technol 26:485–491CrossRefGoogle Scholar
  58. Macy JM, Michel TA, Kirsch DG (1989) Selenate reduction by Pseudomonas species: a new mode of anaerobic respiration. FEMS Microbiol Lett 61:195–198CrossRefGoogle Scholar
  59. Macy JM, Rech S, Auling G, Dorsch M, Stackebrandt E, Sly LI (1993) Thauera selenatis gen. nov., sp. nov., a member of the beta subclass of Proteobacteria with a novel type of anaerobic respiration. Int J Syst Bacteriol 43:135–142CrossRefGoogle Scholar
  60. Marsili E, Baron DB, Shikhare ID, Coursoulle D, Gralnick JA, Bond DR (2008) Shewanella secretes flavins that mediate extracellular electron transfer. Proc Natl Acad Sci USA 10:3968–3973CrossRefGoogle Scholar
  61. Mezes M, Balogh K (2009) Prooxidant mechanisms of selenium toxicity—a review. Acta Biologica Szegediensis 53, Suppl.1. http://www.sci.u-szeged.hu/ABS
  62. Muyzer G, Stams AJ (2008) The ecology and biotechnology of sulphate-reducing bacteria. Nat Rev Microbiol 6:441–454Google Scholar
  63. Nakagawa T, Lino T, Suzuki K-I, Harayama S (2006) Ferrimonas futtsuensis sp. nov. and Ferrimonas kyonanensis sp. nov. selenate-reducing bacteria belonging to the Gammaproteobacteria isolated from Tokyo Bay. Internat J Systematic Evol Microbiol 56:2639–2645CrossRefGoogle Scholar
  64. Nancharaiah YV, Lens PNL (2015a) Ecology and biotechnology of selenium-respiring bacteria. Microbiol Mol Biol Rev 79:61–80CrossRefGoogle Scholar
  65. Nancharaiah YV, Lens PNL (2015b) Selenium biomineralization for biotechnological applications. Trends Biotechnol 6:323–330CrossRefGoogle Scholar
  66. Narasingarao P, Haggblom MM (2007) Pelobacter seleniigenes sp. nov. a selenate-respiring bacterium. Int J Syst Evol Microbiol 57:1937–1942CrossRefGoogle Scholar
  67. Ni TW, Staicu LC, Nemeth R, Schwartz C, Crawford D, Seligman J, Hunter WJ, Pilon-Smits EAH, Ackerson CJ (2015) Progress toward clonable inorganic nanoparticles. Nanoscale 7:17320–17327Google Scholar
  68. Noblitt SD, Staicu LC, Ackerson CJ, Henry CS (2014) Sensitive, selective analysis of selenium oxoanions using microchip electrophoresis with contact conductivity detection. Anal Chem 86:8425–8432CrossRefGoogle Scholar
  69. Ohlendorf HM (1989) Bioaccumulation and effects of selenium in wildlife. In: Jacobs LW (ed) Selenium in agriculture and the environment. American Society of Agronomy, Inc. Soil Science Society of America, Inc. 5585, Madison, USAGoogle Scholar
  70. Oremland RS, Hollibaugh JT, Maest AS, Presser TS, Miller LG, Culberston CW (1989) Selenate reduction to elemental selenium by anaerobic bacteria in sediments and culture: biogeochemical significance of a novel, sulfate-independent respiration. Appl Environ Microbiol 55:2333–2343Google Scholar
  71. Oremland RS, Switzer Blum J, Culberston CW, Visscher PT, Miller LG, Dowdle P, Strohmaier FE (1994) Isolation, growth and metabolism of an obligately anaerobic, selenate-respiring bacterium, strain SES-3. Appl Environ Microbiol 60:3011–3019Google Scholar
  72. Oremland RS, Blum JS, Bindi AB, Dowdle PR, Herbel M, Stolz JF (1999) Simultaneous reduction of nitrate and selenate by cell suspensions of selenium-respiring bacteria. Appl Environ Microbiol 65:4385–4392Google Scholar
  73. Oremland RS, Herbel MJ, Blum JS, Langley S, Beveridge TJ, Ajayan PM, Sutto T, Ellis AV, Curran S (2004) Structural and spectral features of selenium nanospheres produced by se-respiring bacteria. Appl Environ Microbiol 70:52–60CrossRefGoogle Scholar
  74. Pearce CI, Coker VS, Charnock JM, Pattrick RAD, Mosselmans JFW, Law N, Beveridge TJ, Lloyd JR (2008) Microbial manufacture of chalcogenide-based nanoparticles via the reduction of selenite using Veillonella atypica: an in situ EXAFS study. Nanotechnology 19:155603CrossRefGoogle Scholar
  75. Pittman MS, Robinson HC, Poole RK (2005) A bacterial glutathione transporter (Escherichia coli CydDC) exports reductant to the periplasm. J Biol Chem 280:32254–32261CrossRefGoogle Scholar
  76. Presser TS, Ohlendorf HM (1987) Biogeochemical cycling of selenium in the San Joaquin Valley, California. Environ Manag 11:805–821CrossRefGoogle Scholar
  77. Rathgeber C, Yurkova N, Stackebrandt E, Beatty JT, Yurkov V (2002) Isolation of tellurite- and selenite-resistant bacteria from hydrothermal vents of the Juan de Fuca Ridge in the Pacific Ocean. Appl Environ Microbiol 68:4613–4622CrossRefGoogle Scholar
  78. Rauschenbach I, Narasingarao P, Haggblom MM (2011) Desulfurispirillum indicum sp. nov. a selenate- and selenite-respiring bacterium isolated from an estuarine canal. Int J Syst Evol Microbiol 61:654–658CrossRefGoogle Scholar
  79. Rayman MP (2000) The importance of selenium to human health. Lancet 356:233–241CrossRefGoogle Scholar
  80. Rech SA, Macy JM (1992) The terminal reductases for selenate and nitrate respiration in Thauera selenatis are two distinct enzymes. J Bacteriol 174:7316–7320CrossRefGoogle Scholar
  81. Ridley H, Watts CA, Richardson DJ, Butler CS (2006) Resolution of distinct membrane-bound enzymes from Enterobacter cloacae SLD1a-1 that are responsible for selective reduction of nitrate and selenate oxyanions. Appl Environ Microbiol 72:5173–5180CrossRefGoogle Scholar
  82. Rosen BP, Liu Z (2009) Transport pathways for arsenic and selenium: a minireview. Environ Int 35:512–515CrossRefGoogle Scholar
  83. Sabaty M, Avazeri C, Pignol D, Vermeglio A (2001) Characterization of the reduction of selenate and tellurite by nitrate reductases. Appl Environ Microbiol 67:5122–5126CrossRefGoogle Scholar
  84. Sarathchandra SU, Watkinson JH (1981) Oxidation of elemental selenium to selenite by Bacillus megaterium. Science 211:600–601CrossRefGoogle Scholar
  85. Sarret G, Avoscan L, Carriere M, Collins R, Geoffroy N, Carrot F, Coves J, Gouget B (2005) Chemical forms of selenium in the metal-resistant bacterium Ralstonia metallidurans CH34 exposed to selenite and selenate. Appl Environ Microbiol 71:2331–2337CrossRefGoogle Scholar
  86. Schlekat CE, Dowdle PR, Lee BG, Luoma SN, Oremland RS (2000) Bioavailability of particle-associated selenium on the bivalve Potamocorbila amuresis. Environ Sci Technol 34:4504–4510CrossRefGoogle Scholar
  87. Schrauzer GN (2000) Selenomethionine: a review of its nutritional significance, metabolism and toxicity. J Nutr 130:1653–1656Google Scholar
  88. Schroder I, Rech S, Krafft T, Macy JM (1997) Purification and characterization of the selenate reductase from Thauera selenatis. J Biol Chem 272:23765–23768CrossRefGoogle Scholar
  89. Shi L, Richardson DJ, Wang Z, Kerisit SN, Rosso KM, Zachare JM, Fredrickson JK (2009) The roles of outer membrane cytochromes of Shewanella and Geobacter in extracellular electron transfer. Environ Microbiol Rep 1:220–227CrossRefGoogle Scholar
  90. Shrift A (1964) A selenium cycle in nature? Nature 201:1304–1305CrossRefGoogle Scholar
  91. Stadtman TC (1974) Selenium biochemistry. Science 183:915–922CrossRefGoogle Scholar
  92. Staicu LC, van Hullebusch ED, Oturan MA, Ackerson CJ, Lens PNL (2015a) Removal of colloidal biogenic selenium from wastewater. Chemosphere 125:130–138CrossRefGoogle Scholar
  93. Staicu LC, Ackerson CJ, Cornelis P et al (2015b) Pseudomonas moraviensis subsp. stanleyae: a bacterial endophyte capable of efficient selenite reduction to elemental selenium under aerobic conditions. J Appl Microb 119:400–410CrossRefGoogle Scholar
  94. Staicu LC, van Hullebusch ED, Lens PNL, Pilon-Smits EAH, Oturan MA (2015c) Electrocoagulation of colloidal biogenic selenium. Environ Sci Pollut Res Int 22:3127–3137CrossRefGoogle Scholar
  95. Staicu LC, Morin-Crini N, Crini G (2017) Desulfurization: Critical step towards enhanced selenium removal from industrial effluents. Chemosphere 117:111–119CrossRefGoogle Scholar
  96. Stolz JF, Ellis DJ, Blum JS, Ahmann D, Lovley DR, Oremland RS (1999) Sulfurospirillum barnesii sp. nov. and Sulfurospirillum arsenophilum sp. nov., new members of the Sulfurospirillum clade of the epsilon Proteobacteria. Int J Syst Bacteriol 49:1177–1180CrossRefGoogle Scholar
  97. Stolz JF, Oremland RS (1999) Bacterial respiration of arsenic and selenium. FEMS Microbiol Rev 23:615–627CrossRefGoogle Scholar
  98. Sura-de Jong M, Reynolds J, Richterova M et al (2015) Selenium hyperaccumulators harbor a diverse endophytic bacterial community characterized by high selenium tolerance and growth promoting properties. Front Plant Sci 6:113CrossRefGoogle Scholar
  99. Switzer Blum J, Burns Bindi A, Buzzelli J, Stolz JF, Oremland RS (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 171:19–30CrossRefGoogle Scholar
  100. Switzer Blum J, Stolz JF, Oren A, Oremland RS (2001) Selenihalanaerobacter shriftii gen. nov. sp. nov., a halophilic anaerobe from Dead Sea sediments that respires selenate. Arch Microbiol 75:208–219CrossRefGoogle Scholar
  101. Tan LC, Nancharaiah YV, van Hullebusch ED, Lens PNL (2016) Selenium: environmental significance, pollution, and biological treatment technologies. Biotechnol Adv 34:886–907CrossRefGoogle Scholar
  102. Taratus EM, Eubanks SG, DiChristina TJ (2000) Design and application of a rapid screening technique for isolation of selenite reduction-deficient mutants of Shewanella putrefaciens. Microbiol Res 155:79–85CrossRefGoogle Scholar
  103. Thorsen M, Jacobson T, Vooijs R, Navarrete C, Bliek T, Schat H, Tamas MJ (2012) Glutathione serves an extracellular defence function to decrease arsenite accumulation and toxicity in yeast. Mol Microbiol 84:1177–1188CrossRefGoogle Scholar
  104. Tomei FA, Barton LL, Lemanski CL, Zocco TG (1992) Reduction of selenate and selenite to elemental selenium by Wolinella succinogenes. Can J Microbiol 38:1328–1333CrossRefGoogle Scholar
  105. Tomei FA, Barton LL, Lemanski CL, Zocco TG, Fink NH, Sillerud LO (1995) Transformation of selenate and selenite to elemental selenium by Desulfovibrio desulfuricans. J Ind Microbiol 14:329–336CrossRefGoogle Scholar
  106. Turner RJ, Weiner JH, Taylor DE (1998) Selenium metabolism in Escherichia coli. Biometals 11:223–227CrossRefGoogle Scholar
  107. von Wintzingerode F, Gobel UB, Siddiqui RA, Rosick U, Schumann P, Fruhling A, Rohde M, Pukall R, Stackebrandt E (2001) Salana multivorans gen. nov. sp. nov., a novel actinobacterium isolated from an anaerobic bioreactor and capable of selenate reduction. Int J Syst Evol Microbiol 51:1653–1661CrossRefGoogle Scholar
  108. Watts CA, Ridley H, Condie KL, Leaver JT, Richardson DJ, Butler CS (2003) Selenate reduction by Enterobacter cloacae SLD1a-1 is catalysed by a molybdenum-dependent membrane-bound enzyme that is distinct from the membrane-bound nitrate reductase. FEMS Microbiol Lett 228:273–279CrossRefGoogle Scholar
  109. Wilson LG, Bandurski R (1958) Enzymatic reactions involving sulfate, sulfite, selenate and molybdate. J Biol Chem 233:975–981Google Scholar
  110. Winkel LHE, Johnson CA, Lenz M, Grundl T, Leupin OX, Amini M, Charlet L (2011) Environmental selenium research: from microscopic processes to global understanding. Environ Sci Technol 46:571–579CrossRefGoogle Scholar
  111. Yee N, Ma J, Dalia A, Boonfueng T, Kobayashi DY (2007) Se(VI) reduction and the precipitation of Se(0) by the facultative bacterium Enterobacter cloacae SLD1a-1 are regulated by FNR. Appl Environ Microbiol 73:1914–1920CrossRefGoogle Scholar
  112. Youssef GA, El-Aassar SA, Berekaa M, El-Shaer M, Stolz J (2009) Arsenate and selenite reduction by some facultative bacteria in the Nile Delta. Am Eurasian J Agric Environ Sci 5:847–855Google Scholar
  113. Zahir ZA, Zhang Y, Frankenberger WT Jr (2003) Fate of selenate metabolized by Enterobacter taylorae isolated from rice straw. J Agric Food Chem 51:3609–3613CrossRefGoogle Scholar
  114. Zannoni D, Borsetti F, Harrison JJ, Turner RJ (2008) The bacterial response to the chalcogen metalloids Se and Te. Adv Microb Physiol 53:1–72Google Scholar
  115. Zehr JP, Oremland RS (1987) Reduction of selenate to selenide by sulfate-respiring bacteria: experiments with cell suspensions and estuarine sediments. Appl Environ Chem 53:1365–1369Google Scholar
  116. Zhao R, Xiang N, Domann FE, Zhong W (2006) Expression of p53 enhances selenite-induced superoxide production and apoptosis in human prostate cancer cells. Cancer Res 66:2296–2304CrossRefGoogle Scholar
  117. Zhang Y, Siddique T, Wang J, Frankenberger WT Jr (2004) Selenate reduction in river water by Citrobacter freundii isolated from a selenium-contaminated sediment. J Agric Food Chem 52:1594–1600CrossRefGoogle Scholar
  118. Zhang Y, Okeke BC, Frankenberger WT (2008) Bacterial reduction of selenite to elemental selenium utilizing molasses as a carbon source. Bioresour Technol 99:1267–1273CrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Faculty of Applied Chemistry and Materials ScienceUniversity Politehnica of BucharestBucharestRomania
  2. 2.Department of BiologyUniversity of New MexicoAlbuquerqueUSA

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