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Bacteria Versus Selenium: A View from the Inside Out

  • Lucian C. Staicu
  • Ronald S. Oremland
  • Ryuta Tobe
  • Hisaaki MiharaEmail author
Chapter
Part of the Plant Ecophysiology book series (KLEC, volume 11)

Abstract

Bacteria and selenium (Se) are closely interlinked as the element serves both essential nutrient requirements and energy generation functions. However, Se can also behave as a powerful toxicant for bacterial homeostasis. Conversely, bacteria play a tremendous role in the cycling of Se between different environmental compartments, and bacterial metabolism has been shown to participate to all valence state transformations undergone by Se in nature. Bacteria possess an extensive molecular repertoire for Se metabolism. At the end of the 1980s, a novel mode of anaerobic respiration based on Se oxyanions was experimentally documented for the first time. Following this discovery, specific enzymes capable of reducing Se oxyanions and harvesting energy were found in a number of anaerobic bacteria. The genes involved in the expression of these enzymes have later been identified and cloned. This iterative approach undertaken outside-in led to the understanding of the molecular mechanisms of Se transformations in bacteria. Based on the extensive knowledge accumulated over the years, we now have a full(er) view from the inside out, from DNA-encoding genes to enzymes and thermodynamics. Bacterial transformations of Se for assimilatory purposes have been the object of numerous studies predating the investigation of Se respiration. Remarkable contributions related to the understating of the molecular picture underlying seleno-amino acid biosynthesis are reviewed herein. Under certain circumstances, Se is a toxicant for bacterial metabolism and bacteria have evolved strategies to counteract this toxicity, most notably by the formation of elemental Se (nano)particles. Several biotechnological applications, such as the production of functional materials and the biofortification of crop species using Se-utilizing bacteria, are presented in this chapter.

Keywords

Selenium Bacteria Anaerobic respiration Selenium detoxification Selenoenzymes 

Notes

Acknowledgments

R.S.O. is supported by the U.S. Geological Survey National Research Program. Mention of any brand name products does not constitute an endorsement by the USGS. The authors would like to acknowledge Elizabeth Pilon-Smits (Colorado State University) for helpful comments.

References

  1. Andreesen JR, Makdessi K (2008) Tungsten, the surprisingly positively acting heavy metal element for prokaryotes. Ann N Y Acad Sci 1125:215–229PubMedCrossRefGoogle Scholar
  2. Avazeri C, Turner RJ, Pommier J, Weiner JH, Giordano G, Vermeglio A (1997) Tellurite reductase activity of nitrate reductase is responsible for the basal resistance of Escherichia coli to tellurite. Microbiology 143:1181–1189PubMedCrossRefGoogle Scholar
  3. Avoscan L, Carriere M, Proux O, Sarret G, Degrouard J, Coves J, Gouget B (2009) Enhanced selenate accumulation in Cupriavidus metallidurans CH34 does not trigger a detoxification pathway. Appl Environ Microbiol 75:2250–2252PubMedPubMedCentralCrossRefGoogle Scholar
  4. Axley MJ, Böck A, Stadtman TC (1991) Catalytic properties of an Escherichia coli formate dehydrogenase mutant in which sulfur replaces selenium. Proc Natl Acad Sci U S A 88:8450–8454PubMedPubMedCentralCrossRefGoogle Scholar
  5. Ayano H, Miyake M, Terasawa K, Kuroda M, Soda S, Sakaguchi T, Ike M (2014) Isolation of a selenite-reducing and cadmium-resistant bacterium Pseudomonas sp. strain RB for microbial synthesis of CdSe nanoparticles. J Biosci Bioeng 117:576–581PubMedCrossRefGoogle Scholar
  6. Baesman SM, Bullen TD, Dewald J, Zhang DH, Curran S, Islam FS, Beveridge TJ, Oremland RS (2007) Formation of tellurium nanocrystals during anaerobic growth of bacteria that use Te oxyanions as respiratory electron acceptors. Appl Environ Microbiol 73:2135–2143PubMedPubMedCentralCrossRefGoogle Scholar
  7. Baesman SM, Stolz JF, Kulp TR, Oremland RS (2009) Enrichment and isolation of Bacillus beveridgei sp. nov., a facultative anaerobic haloalkaliphile from Mono Lake, California that respires oxyanions of tellurium, selenium, and arsenic. Extremophiles 13:695–705PubMedCrossRefGoogle Scholar
  8. Baron C, Böck A (1991) The length of the aminoacyl-acceptor stem of the selenocysteine-specific tRNA(Sec) of Escherichia coli is the determinant for binding to elongation factors SELB or Tu. J Biol Chem 266:20375–20379PubMedGoogle Scholar
  9. Bebien M, Kirsch J, Mejean V, Vermeglio A (2002) Involvement of a putative molybdenum enzyme in the reduction of selenate by Escherichia coli. Microbiology 148:3865–3872PubMedCrossRefGoogle Scholar
  10. Berntsson RP, Alia Oktaviani N, Fusetti F, Thunnissen AM, Poolman B, Slotboom DJ (2009) Selenomethionine incorporation in proteins expressed in Lactococcus lactis. Protein Sci 18:1121–1127PubMedPubMedCentralCrossRefGoogle Scholar
  11. Björnstedt M, Kumar S, Holmgren A (1992) Selenodiglutathione is a highly efficient oxidant of reduced thioredoxin and a substrate for mammalian thioredoxin reductase. J Biol Chem 267:8030–8034PubMedGoogle Scholar
  12. Bult CJ, White O, Olsen GJ, Zhou L, Fleischmann RD, Sutton GG, Blake JA, FitzGerald LM, Clayton RA, Gocayne JD, Kerlavage AR, Dougherty BA, Tomb JF, Adams MD, Reich CI, Overbeek R, Kirkness EF, Weinstock KG, Merrick JM, Glodek A, Scott JL, Geoghagen NS, Venter JC et al (1996) Complete genome sequence of the methanogenic archaeon, Methanococcus jannaschii. Science 273:1058–1073Google Scholar
  13. Butler CS, Debieux CM, Dridge EJ, Splatt P, Wright M (2012) Biomineralization of selenium by the selenate-respiring bacterium Thauera selenatis. Biochem Soc Trans 40:1239–1243PubMedCrossRefGoogle 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. CRC Press, Boca RatonCrossRefGoogle Scholar
  15. Chau YK, Wong PT, Silverberg BA, Luxon PL, Bengert GA (1976) Methylation of selenium in the aquatic environment. Science 192:1130–1131PubMedCrossRefGoogle Scholar
  16. Chen CS, Stadtman TC (1980) Selenium-containing tRNAs from Clostridium sticklandii: cochromatography of one species with l-prolyl-tRNA. Proc Natl Acad Sci U S A 77:1403–1407PubMedPubMedCentralCrossRefGoogle Scholar
  17. Chen T, Wong YS (2008) In vitro antioxidant and antiproliferative activities of selenium-containing phycocyanin from selenium-enriched Spirulina platensis. J Agric Food Chem 56:4352–4358PubMedCrossRefGoogle Scholar
  18. Ching WM, Alzner-DeWeerd B, Stadtman TC (1985a) A selenium-containing nucleoside at the first position of the anticodon in seleno-tRNAGlu from Clostridium sticklandii. Proc Natl Acad Sci U S A 82:347–350PubMedPubMedCentralCrossRefGoogle Scholar
  19. Ching WM, Tsai L, Wittwer AJ (1985b) Selenium-containing transfer RNAs. Curr Top Cell Regul 27:497–507PubMedCrossRefGoogle Scholar
  20. Chocat P, Esaki N, Nakamura T, Tanaka H, Soda K (1983) Microbial distribution of selenocysteine lyase. J Bacteriol 156:455–457PubMedPubMedCentralGoogle Scholar
  21. Chocat P, Esaki N, Tanizawa K, Nakamura K, Tanaka H, Soda K (1985) Purification and characterization of selenocysteine β-lyase from Citrobacter freundii. J Bacteriol 163:669–676PubMedPubMedCentralGoogle Scholar
  22. Commans S, Böck A (1999) Selenocysteine inserting tRNAs: an overview. FEMS Microbiol Rev 23:335–351PubMedCrossRefGoogle Scholar
  23. Cone JE, Del Rio RM, Davis JN, Stadtman TC (1976) Chemical characterization of the selenoprotein component of clostridial glycine reductase: identification of selenocysteine as the organoselenium moiety. Proc Natl Acad Sci U S A 73:2659–2663PubMedPubMedCentralCrossRefGoogle Scholar
  24. Cox JC, Edwards ES, DeMoss JA (1981) Resolution of distinct selenium-containing formate dehydrogenases from Escherichia coli. J Bacteriol 145:1317–1324PubMedPubMedCentralGoogle Scholar
  25. 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 nanosphere assembly. Proc Natl Acad Sci U S A 108:13480–13485PubMedPubMedCentralCrossRefGoogle Scholar
  26. Dietrichs D, Meyer M, Rieth M, Andreesen JR (1991) Interaction of selenoprotein PA and the thioredoxin system, components of the NADPH-dependent reduction of glycine in Eubacterium acidaminophilum and Clostridium litorale. J Bacteriol 173:5983–5991PubMedPubMedCentralCrossRefGoogle Scholar
  27. Ding GB, Nie RH, Lv LH, Wei GQ, Zhao LQ (2014) Preparation and biological evaluation of a novel selenium-containing exopolysaccharide from Rhizobium sp. N613. Carbohydr Polym 109:28–34PubMedCrossRefGoogle Scholar
  28. Dowdle PR, Oremland RS (1998) Microbial oxidation of elemental selenium in soils and bacterial cultures. Environ Sci Technol 32:3749–3755CrossRefGoogle Scholar
  29. Durán P, Acuña J, Jorquera M, Azcón R, Paredes C, Rengel Z, de la Luz Mora M (2014) Endophytic bacteria from selenium-supplemented wheat plants could be useful for plant-growth promotion, biofortification and Gaeumannomyces graminis biocontrol in wheat production. Biol Fertil Soils 50:983–990Google Scholar
  30. El Mehdawi AF, Pilon-Smits EAH (2012) Ecological aspects of plant selenium hyperaccumulation. Plant Biol 14:1–10PubMedCrossRefGoogle Scholar
  31. Ellis AS, Johnson TM, Herbel MJ, Bullen TD (2003) Stable isotope fractionation by natural microbial consortia. Chem Geol 195:119–129CrossRefGoogle Scholar
  32. Esaki N, Tanaka H, Uemura S, Suzuki T, Soda K (1979) Catalytic action of l-methionine γ-lyase on selenomethionine and selenols. Biochemistry 18:407–410PubMedCrossRefGoogle Scholar
  33. Esaki N, Seraneeprakarn V, Tanaka H, Soda K (1988) Purification and characterization of Clostridium sticklandii d-selenocystine α, β-lyase. J Bacteriol 170:751–756PubMedPubMedCentralCrossRefGoogle Scholar
  34. Fellowes JW, Pattrick RAD, Lloyd JR, Charnock JM, Mosselmans JFW, Weng T-C, Pearce CI (2013) Ex situ formation of metal selenide quantum dots using bacterially derived selenide precursors. Nanotech 24:145603CrossRefGoogle Scholar
  35. 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
  36. Ferry JG (1990) Formate dehydrogenase. FEMS Microbiol Rev 7:377–382PubMedCrossRefGoogle Scholar
  37. Fonknechten N, Chaussonnerie S, Tricot S, Lajus A, Andreesen JR, Perchat N, Pelletier E, Gouyvenoux M, Barbe V, Salanoubat M, Le Paslier D, Weissenbach J, Cohen GN, Kreimeyer A (2010) Clostridium sticklandii, a specialist in amino acid degradation: revisiting its metabolism through its genome sequence. BMC Genomics 11:555Google Scholar
  38. Forchhammer K, Böck A (1991) Selenocysteine synthase from Escherichia coli. Analysis of the reaction sequence. J Biol Chem 266:6324–6328PubMedGoogle Scholar
  39. Forchhammer K, Leinfelder W, Böck A (1989) Identification of a novel translation factor necessary for the incorporation of selenocysteine into protein. Nature 342:453–456PubMedCrossRefGoogle Scholar
  40. Forchhammer K, Rucknagel KP, Böck A (1990) Purification and biochemical characterization of SELB, a translation factor involved in selenoprotein synthesis. J Biol Chem 265:9346–9350PubMedGoogle Scholar
  41. Forchhammer K, Leinfelder W, Boesmiller K, Veprek B, Böck A (1991) Selenocysteine synthase from Escherichia coli. Nucleotide sequence of the gene (selA) and purification of the protein. J Biol Chem 266:6318–6323PubMedGoogle Scholar
  42. Forster C, Ott G, Forchhammer K, Sprinzl M (1990) Interaction of a selenocysteine-incorporating tRNA with elongation factor Tu from E.coli. Nucleic Acids Res 18:487–491PubMedPubMedCentralCrossRefGoogle Scholar
  43. Fujita M, Ike M, Nisbimoto S, Takahasbi K, Kasbiwa M (1997) Isolation and characterization of a novel selenate-reducing bacterium, Bacillus sp. SF-1. J Ferment Bioeng 83:517–522CrossRefGoogle Scholar
  44. Ganther HE (1968) Selenotrisulfides. Formation by reaction of thiols with selenious acid. Biochem 7:2898–2905CrossRefGoogle Scholar
  45. Ganther HE (1971) Reduction of the selenotrisulfide derivative of glutathione to a persulfide analog by glutathione reductase. Biochemistry 10:4089–4098PubMedCrossRefGoogle Scholar
  46. Ganther HE, Levander OA, Baumann CA (1966) Dietary control of selenium volatilization in the rat. J Nutr 88:55–60PubMedGoogle Scholar
  47. Garcia GE, Stadtman TC (1992) Clostridium sticklandii glycine reductase selenoprotein A gene: cloning, sequencing, and expression in Escherichia coli. J Bacteriol 174:7080–7089PubMedPubMedCentralCrossRefGoogle Scholar
  48. Gerrard TL, Telford JN, Williams HH (1974) Detection of selenium deposits in Escherichia coli by electron microscopy. J Bacteriol 119:1057–1060PubMedPubMedCentralGoogle Scholar
  49. Gladyshev VN, Khangulov SV, Stadtman TC (1994) Nicotinic acid hydroxylase from Clostridium barkeri: electron paramagnetic resonance studies show that selenium is coordinated with molybdenum in the catalytically active selenium-dependent enzyme. Proc Natl Acad Sci U S A 91:232–236PubMedPubMedCentralCrossRefGoogle Scholar
  50. Glass RS, Singh WP, Jung W, Veres Z, Scholz TD, Stadtman TC (1993) Monoselenophosphate: synthesis, characterization, and identity with the prokaryotic biological selenium donor, compound SePX. Biochemistry 32:12555–12559PubMedCrossRefGoogle Scholar
  51. Gojkovic Z, Vilchez C, Torronteras R, Vigara J, Gomez-Jacinto V, Janzer N, Gomez-Ariza JL, Marova I, Garbayo I (2014) Effect of selenate on viability and selenomethionine accumulation of Chlorella sorokiniana grown in batch culture. Sci World J 2014:401265CrossRefGoogle Scholar
  52. Gonzalez-Gil G, Lens PNL, Saikaly PE (2016) Selenite reduction by anaerobic microbial aggregates: microbial community structure, and proteins associated to the produced selenium spheres. Front Microbiol 7:571PubMedPubMedCentralCrossRefGoogle Scholar
  53. Gristwood T, McNeil MB, Clulow JS, Salmond GP, Fineran PC (2011) PigS and PigP regulate prodigiosin biosynthesis in Serratia via differential control of divergent operons, which include predicted transporters of sulfur-containing molecules. J Bacteriol 193:1076–1085PubMedCrossRefGoogle Scholar
  54. Gursinsky T, Gröbe D, Schierhorn A, Jäger J, Andreesen JR, Söhling B (2008) Factors and selenocysteine insertion sequence requirements for the synthesis of selenoproteins from a gram-positive anaerobe in Escherichia coli. Appl Environ Microbiol 74:1385–1393Google Scholar
  55. Guymer D, Maillard J, Sargent F (2009) A genetic analysis of in vivo selenate reduction by Salmonella enterica serovar Typhimurium LT2 and Escherichia coli K12. Arch Microbiol 191:519–528PubMedCrossRefGoogle Scholar
  56. Haft DH, Self WT (2008) Orphan SelD proteins and selenium-dependent molybdenum hydroxylases. Biol Direct 3:4PubMedPubMedCentralCrossRefGoogle Scholar
  57. Halboth S, Klein A (1992) Methanococcus voltae harbors four gene clusters potentially encoding two [NiFe] and two [NiFeSe] hydrogenases, each of the cofactor F420-reducing or F420-non-reducing types. Mol Gen Genet 233:217–224PubMedCrossRefGoogle Scholar
  58. Herbel MJ, Johnson TM, Oremland RS, Bullen TD (2000) Fractionation of selenium isotopes during bacterial respiratory reduction of selenium oxyanions. Geochim Cosmochim Acta 64:3701–3709CrossRefGoogle Scholar
  59. Herbel MJ, Johnson TM, Tanji KK, Gao S, Bullen TD (2002) Selenium stable isotope ratios in California agricultural drainage water. J Environ Qual 31:1146–1156PubMedCrossRefGoogle Scholar
  60. Herbel MJ, Blum JS, Oremland RS, Borglin SE (2003) Reduction of elemental selenium to selenide: experiments with anoxic sediments and bacteria that respire Se-oxyanions. Geomicrobiol J 20:587–602CrossRefGoogle Scholar
  61. Hockin SL, Gadd GM (2003) Linked redox precipitation of sulfur and selenium under anaerobic conditions by sulfate-reducing bacterial biofilms. Appl Environ Microbiol 69:7063–7072PubMedPubMedCentralCrossRefGoogle Scholar
  62. Hoffman DJ (2002) Role of selenium toxicity and oxidative stress in aquatic birds. Aquat Toxicol 57:11–26PubMedCrossRefGoogle Scholar
  63. Hormann K, Andreesen JR (1989) Reductive cleavage of sarcosine and betaine by Eubacterium acidaminophilum via enzyme systems different from glycine reductase. Arch Microbiol 153:50–59CrossRefGoogle Scholar
  64. Hryniewicz M, Sirko A, Pałucha A, Böck A, Hulanicka D (1990) Sulfate and thiosulfate transport in Escherichia coli K-12: identification of a gene encoding a novel protein involved in thiosulfate binding. J Bacteriol 172:3358–3366PubMedPubMedCentralCrossRefGoogle Scholar
  65. Huber R, Sacher M, Vollmann A, Huber H, Rose D (2000) Respiration of arsenate and selenate by hyperthermophilic archaea. Syst Appl Microbiol 23:305–314PubMedCrossRefGoogle Scholar
  66. Jain R, Jordan N, Weiss S, Foerstendorf H, Heim K, Kacker R, Hübner R, Kramer H, van Hullebusch ED, Farges F, Lens PNL (2015) Extracellular polymeric substances (EPS) govern the surface charge of biogenic elemental selenium nanoparticles. Environ Sci Technol 49:1713–1720PubMedCrossRefGoogle Scholar
  67. Johnson TM, Herbel MJ, Bullen TD, Zawislanski PT (1999) Selenium isotope ratios as indicators of selenium sources and oxyanion reduction. Geochim Cosmochim Acta 63:2775–2783CrossRefGoogle Scholar
  68. Jones JB, Dilworth GL, Stadtman TC (1979) Occurrence of selenocysteine in the selenium-dependent formate dehydrogenase of Methanococcus vannielii. Arch Biochem Biophys 195:255–260PubMedCrossRefGoogle Scholar
  69. Kabisch UC, Grantzdorffer A, Schierhorn A, Rucknagel KP, Andreesen JR, Pich A (1999) Identification of d-proline reductase from Clostridium sticklandii as a selenoenzyme and indications for a catalytically active pyruvoyl group derived from a cysteine residue by cleavage of a proprotein. J Biol Chem 274:8445–8454PubMedCrossRefGoogle Scholar
  70. Kagami T, Narita T, Kuroda M, Notaguchi E, Yamashita M, Sei K, Soda S, Ike M (2013) Effective selenium volatilization under aerobic conditions and recovery from the aqueous phase by Pseudomonas stutzeri NT-I. Water Res 47:1361–1368PubMedCrossRefGoogle Scholar
  71. Kertesz MA (2001) Bacterial transporters for sulfate and organosulfur compounds. Res Microbiol 152:279–290PubMedCrossRefGoogle Scholar
  72. 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 65:4734–4740PubMedPubMedCentralGoogle Scholar
  73. Kim HY, Zhang Y, Lee BC, Kim JR, Gladyshev VN (2009) The selenoproteome of Clostridium sp. OhILAs: characterization of anaerobic bacterial selenoprotein methionine sulfoxide reductase A. Proteins 74:1008–1017PubMedPubMedCentralCrossRefGoogle Scholar
  74. Kim MJ, Lee BC, Jeong J, Lee KJ, Hwang KY, Gladyshev VN, Kim HY (2011) Tandem use of selenocysteine: adaptation of a selenoprotein glutaredoxin for reduction of selenoprotein methionine sulfoxide reductase. Mol Microbiol 79:1194–1203PubMedPubMedCentralCrossRefGoogle Scholar
  75. Kim MJ, Lee BC, Hwang KY, Gladyshev VN, Kim HY (2015) Selenium utilization in thioredoxin and catalytic advantage provided by selenocysteine. Biochem Biophys Res Commun 461:648–652PubMedPubMedCentralCrossRefGoogle Scholar
  76. Kramer GF, Ames BN (1988) Isolation and characterization of a selenium metabolism mutant of Salmonella typhimurium. J Bacteriol 170:736–743PubMedPubMedCentralCrossRefGoogle Scholar
  77. Krittaphol W, Wescombe PA, Thomson CD, McDowell A, Tagg JR, Fawcett JP (2011) Metabolism of L-selenomethionine and selenite by probiotic bacteria: in vitro and in vivo studies. Biol Trace Elem Res 144:1358–1369PubMedCrossRefGoogle Scholar
  78. Kromayer M, Wilting R, Tormay P, Böck A (1996) Domain structure of the prokaryotic selenocysteine-specific elongation factor SelB. J Mol Biol 262:413–420PubMedCrossRefGoogle Scholar
  79. Kryukov GV, Gladyshev VN (2004) The prokaryotic selenoproteome. EMBO Rep 5:538–543PubMedPubMedCentralCrossRefGoogle Scholar
  80. 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, from the selenate-reducing bacterium Bacillus selenatarsenatis SF-1. J Bacteriol 193:2141–2148PubMedPubMedCentralCrossRefGoogle Scholar
  81. Labunskyy VM, Hatfield DL, Gladyshev VN (2014) Selenoproteins: molecular pathways and physiological roles. Physiol Rev 94:739–777PubMedPubMedCentralCrossRefGoogle Scholar
  82. Lacourciere GM, Mihara H, Kurihara T, Esaki N, Stadtman TC (2000) Escherichia coli NifS-like proteins provide selenium in the pathway for the biosynthesis of selenophosphate. J Biol Chem 275:23769–23773PubMedCrossRefGoogle Scholar
  83. Laverman AM, Switzer Blum J, Schaefer JK, Phillips EJP, Lovley DR, Oremland RS (1995) Growth of strain SES-3 with arsenate and other diverse electron acceptors. Appl Environ Microbiol 61:3556–3561PubMedPubMedCentralGoogle Scholar
  84. Leinfelder W, Stadtman TC, Böck A (1989) Occurrence in vivo of selenocysteyl-tRNA(SERUCA) in Escherichia coli. Effect of sel mutations. J Biol Chem 264:9720–9723PubMedGoogle Scholar
  85. Leinfelder W, Forchhammer K, Veprek B, Zehelein E, Böck A (1990) In vitro synthesis of selenocysteinyl-tRNAUCA from seryl-tRNAUCA: involvement and characterization of the selD gene product. Proc Natl Acad Sci U S A 87:543–547PubMedPubMedCentralCrossRefGoogle Scholar
  86. Lenz M, Kolvenbach B, Gygax B, Moes S, Corvini FX (2011) Shedding light on selenium biomineralization: proteins associated with bionanominerals. Appl Environ Microbiol 77:4676–4680PubMedPubMedCentralCrossRefGoogle Scholar
  87. Li DB, Cheng YY, Wu C, Li WW, Li N, Yang ZC, Tong ZH, Yu HQ (2014) Selenite reduction by Shewanella oneidensis MR-1 is mediated by fumarate reductase in periplasm. Sci Rep 4:3735PubMedPubMedCentralCrossRefGoogle Scholar
  88. Lin J, Peng T, Jiang L, Ni JZ, Liu Q, Chen L, Zhang Y (2015) Comparative genomics reveals new candidate genes involved in selenium metabolism in prokaryotes. Genome Biol Evol 7:664–676PubMedPubMedCentralCrossRefGoogle Scholar
  89. 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 63:3079–3084PubMedPubMedCentralGoogle Scholar
  90. 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 c 4 mediate electron transfer during selenate respiration in Thauera selenatis. J Biol Chem 285:18433–18442Google Scholar
  91. 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
  92. Macy JM, Rech S, Auling G, Dorsch M, Stackebrandt E, Sly LI (1993) Thauera selenatis gen. nov. a member of the beta subclass of Proteobacteria with a novel type of anaerobic respiration. Int J Syst Bacteriol 43:135–142PubMedCrossRefGoogle Scholar
  93. Mal J, Yarlagadda VN, Hullebusch EDV, Lens PNL (2016) Metal chalcogenide quantum dots: biotechnological synthesis and applications. RSC Adv 6:41477–41495CrossRefGoogle Scholar
  94. McCarty S, Chasteen T, Marshall M, Fall R, Bachofen R (1993) Phototrophic bacteria produce volatile, methylated sulfur and selenium compounds. FEMS Microbiol Lett 112:93–98CrossRefGoogle Scholar
  95. Meyer M, Granderath K, Andreesen JR (1995) Purification and characterization of protein PB of betaine reductase and its relationship to the corresponding proteins glycine reductase and sarcosine reductase from Eubacterium acidaminophilum. Eur J Biochem 234:184–191PubMedCrossRefGoogle Scholar
  96. Mihara H, Kurihara T, Yoshimura T, Esaki N (2000) Kinetic and mutational studies of three NifS homologs from Escherichia coli: mechanistic difference between l-cysteine desulfurase and l-selenocysteine lyase reactions. J Biochem 127:559–567PubMedCrossRefGoogle Scholar
  97. Nancharaiah YV, Lens PN (2015) Ecology and biotechnology of selenium-respiring bacteria. Microbiol Mol Biol Rev 79:61–80PubMedPubMedCentralCrossRefGoogle Scholar
  98. 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 7:17320–17327PubMedPubMedCentralCrossRefGoogle Scholar
  99. Oremland RS, Zehr JP (1986) Formation of methane and carbon dioxide from dimethylselenide in anoxic sediments and by a methanogenic bacterium. Appl Environ Microbiol 52:1031–1036PubMedPubMedCentralGoogle Scholar
  100. 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 55:2333–2343PubMedPubMedCentralGoogle Scholar
  101. Oremland RS, Steinberg NA, Maest AS, Miller LG, Hollibaugh JT (1990) Measurement of in situ rates of selenate removal by dissimilatory bacterial reduction in sediments. Environ Sci Technol 24:1157–1164CrossRefGoogle Scholar
  102. Oremland RS, Steinberg NA, Presser TS, Miller LG (1991) In situ bacterial selenate reduction in the agricultural drainage systems of western Nevada. Appl Environ Microbiol 57:615–617PubMedPubMedCentralGoogle Scholar
  103. 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 60:3011–3019PubMedPubMedCentralGoogle Scholar
  104. Oremland RS, Herbel MJ, Switzer Blum J, Langley S, Beveridge TJ, Sutto T, Ajayan PM, Ellis A, Curran S (2004) Structural and spectral features of selenium nanospheres formed by Se-respiring bacteria. Appl Environ Microbiol 70:52–60PubMedPubMedCentralCrossRefGoogle Scholar
  105. Pearce CI, Coker VS, Charnock JM, Pattrick RA, Mosselmans JF, 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 19:155603PubMedCrossRefGoogle Scholar
  106. Pearce CI, Baesman SM, Blum JS, Fellowes JW, Oremland RS (2011) Nanoparticles formed from microbial oxyanion reduction of toxic group 15 and group 16 metalloids. In: Stolz JF, Oremland RS (eds) Microbial metal and metalloid metabolism: advances and applications. ASM Press, Washington, DCGoogle Scholar
  107. Peng T, Lin J, Xu YZ, Zhang Y (2016) Comparative genomics reveals new evolutionary and ecological patterns of selenium utilization in bacteria. ISME J 10:2048–2059PubMedPubMedCentralCrossRefGoogle Scholar
  108. Pettine M, Gennari F, Campanella L (2013) The reaction of selenium (IV) with ascorbic acid: its relevance in aqueous and soil systems. Chemosphere 90:245–250PubMedCrossRefGoogle Scholar
  109. Pflugrath JW, Quiocho FA (1985) Sulphate sequestered in the sulphate-binding protein of Salmonella typhimurium is bound solely by hydrogen bonds. Nature 314:257–260PubMedCrossRefGoogle Scholar
  110. Ranjard L, Prigent-Combaret C, Nazaret S, Cournoyer B (2002) Methylation of inorganic and organic selenium by the bacterial thiopurine methyltransferase. J Bacteriol 184:3146–3149PubMedPubMedCentralCrossRefGoogle Scholar
  111. Ranjard L, Nazaret S, Cournoyer B (2003) Freshwater bacteria can methylate selenium through the thiopurine methyltransferase pathway. Appl Environ Microbiol 69:3784–3790PubMedPubMedCentralCrossRefGoogle Scholar
  112. Ranjard L, Prigent-Combaret C, Favre-Bonté S, Monnez C, Nazaret S, Cournoyer B (2004) Characterization of a novel selenium methyltransferase from freshwater bacteria showing strong similarities with the calicheamicin methyltransferase. Biochim Biophys Acta 1679:80–85PubMedCrossRefGoogle Scholar
  113. Rech SA, Macy JM (1992) The terminal reductases for selenate and nitrate respiration in Thauera selenatis are two distinct enzymes. J Bacteriol 174:7316–7320PubMedPubMedCentralCrossRefGoogle Scholar
  114. 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 72:5173–5180PubMedPubMedCentralCrossRefGoogle Scholar
  115. Rother M, Wilting R, Commans S, Böck A (2000) Identification and characterisation of the selenocysteine-specific translation factor SelB from the archaeon Methanococcus jannaschii. J Mol Biol 299:351–358PubMedCrossRefGoogle Scholar
  116. Rother M, Resch A, Wilting R, Böck A (2001) Selenoprotein synthesis in archaea. Biofactors 14:75–83PubMedCrossRefGoogle Scholar
  117. Saier MH Jr, Tran CV, Barabote RD (2006) TCDB: the transporter classification database for membrane transport protein analyses and information. Nucleic Acids Res 34:D181–D186PubMedCrossRefGoogle Scholar
  118. Santos S, Ungureanu G, Boaventura R, Botelho C (2015) Selenium contaminated waters: an overview of analytical methods, treatment options and recent advances in sorption methods. Sci Total Environ 521-522C:246–260CrossRefGoogle Scholar
  119. Sawers RG, Blokesch M, Böck A (2004) Anaerobic formate and hydrogen metabolism. EcoSal Plus 1(1). doi: 10.1128/ecosalplus.3.5.4
  120. Schellenger AEP, Onnis-Hayden A, Jisi DP, Larese-Casanova P (2015) Oxygen kinetic isotope effects in selenate during microbial reduction. Appl Geochem 63:261–271CrossRefGoogle Scholar
  121. Schon A, Böck A, Ott G, Sprinzl M, Söll D (1989) The selenocysteine-inserting opal suppressor serine tRNA from E. coli is highly unusual in structure and modification. Nucleic Acids Res 17:7159–7165PubMedPubMedCentralCrossRefGoogle Scholar
  122. Schräder T, Rienhöfer A, Andreesen JR (1999) Selenium-containing xanthine dehydrogenase from Eubacterium barkeri. Eur J Biochem 264:862–871PubMedCrossRefGoogle Scholar
  123. Schröder I, Rech S, Krafft T, Macy JM (1997) Purification and characterization of the selenate reductase from Thauera selenatis. J Biol Chem 272:23765–23768PubMedCrossRefGoogle Scholar
  124. Self WT, Stadtman TC (2000) Selenium-dependent metabolism of purines: a selenium-dependent purine hydroxylase and xanthine dehydrogenase were purified from Clostridium purinolyticum and characterized. Proc Natl Acad Sci U S A 97:7208–7213PubMedPubMedCentralCrossRefGoogle Scholar
  125. Self WT, Wolfe MD, Stadtman TC (2003) Cofactor determination and spectroscopic characterization of the selenium-dependent purine hydroxylase from Clostridium purinolyticum. Biochemistry 42:11382–11390PubMedCrossRefGoogle Scholar
  126. Shirsat S, Kadam A, Naushad M, Mane RS (2015) Selenium nanostructures: microbial synthesis and applications. Roy Soc Chem Adv 5:92799–92811Google Scholar
  127. Shrift A (1964) A selenium cycle in nature? Nature 201:1304–1305PubMedCrossRefGoogle Scholar
  128. Simmons DB, Wallschlaeger D (2005) A critical review of the biogeochemistry and ecotoxicology of selenium in lotic and lentic environments. Environ Toxicol Chem 24:1331–1343PubMedCrossRefGoogle Scholar
  129. Sirko A, Hryniewicz M, Hulanicka D, Böck A (1990) Sulfate and thiosulfate transport in Escherichia coli K-12: nucleotide sequence and expression of the cysTWAM gene cluster. J Bacteriol 172:3351–3357PubMedPubMedCentralCrossRefGoogle Scholar
  130. Sohling B, Parther T, Rucknagel KP, Wagner MA, Andreesen JR (2001) A selenocysteine-containing peroxiredoxin from the strictly anaerobic organism Eubacterium acidaminophilum. Biol Chem 382:979–986PubMedCrossRefGoogle Scholar
  131. Sorgenfrei O, Klein A, Albracht SP (1993) Influence of illumination on the electronic interaction between 77Se and nickel in active F420-non-reducing hydrogenase from Methanococcus voltae. FEBS Lett 332:291–297PubMedCrossRefGoogle Scholar
  132. Stadtman TC (1974) Selenium biochemistry. Science 183:915–922PubMedCrossRefGoogle Scholar
  133. Stadtman TC, Davis JN, Zehelein E, Böck A (1989) Biochemical and genetic analysis of Salmonella typhimurium and Escherichia coli mutants defective in specific incorporation of selenium into formate dehydrogenase and tRNAs. Biofactors 2:35–44PubMedGoogle Scholar
  134. Staicu LC, van Hullebusch ED, Lens PNL (2015a) Production, recovery and reuse of biogenic elemental selenium. Environ Chem Lett 13:89–96CrossRefGoogle Scholar
  135. Staicu LC, Ackerson CJ, Cornelis P, Ye L, Berendsen RL, Hunter WJ, Noblitt SD, Henry CS, Cappa JJ, Montenieri RL, Wong AO, Musilova L, Sura-de Jong M, van Hullebusch ED, Lens PN, Reynolds RJ, Pilon-Smits EA et al (2015b) Pseudomonas moraviensis subsp. stanleyae: a bacterial endophyte capable of efficient selenite reduction to elemental selenium under aerobic conditions. J Appl Microbiol 119:400–410Google Scholar
  136. Staicu LC, van Hullebusch ED, Oturan MA, Ackerson CJ, Lens PNL (2015c) Removal of colloidal biogenic selenium from wastewater. Chemosphere 125:130–138PubMedCrossRefGoogle Scholar
  137. Steinberg NA, Oremland RS (1990) Dissimilatory selenate reduction potentials in a diversity of sediment types. Appl Environ Microbiol 56:3550–3557PubMedPubMedCentralGoogle Scholar
  138. Stolz JF, Oremland RS (1999) Bacterial respiration of arsenic and selenium. FEMS Microbiol Rev 23:615–627PubMedCrossRefGoogle Scholar
  139. Stolz JF, Basu P, Santini JM, Oremland RS (2006) Arsenic and selenium in microbial metabolism. Annu Rev Microbiol 60:107–130PubMedCrossRefGoogle Scholar
  140. Sura-de Jong M, Reynolds RJ, Richterova MK, Musilova L, Staicu LC, Chocholata I, Cappa JJ, Taghavi S, van der Lelie D, Frantik T, Dolinova I, Strejcek M, Cochran AT, Lovecka P, Pilon-Smits EA et al (2015) Selenium hyperaccumulators harbor a diverse endophytic bacterial community characterized by high selenium tolerance and growth promoting properties. Front Plant Sci 6:113Google Scholar
  141. 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 171:19–30PubMedCrossRefGoogle Scholar
  142. Tamura T, Yamamoto S, Takahata M, Sakaguchi H, Tanaka H, Stadtman TC, Inagaki K (2004) Selenophosphate synthetase genes from lung adenocarcinoma cells: Sps1 for recycling L-selenocysteine and Sps2 for selenite assimilation. Proc Natl Acad Sci U S A 101:16162–16167PubMedPubMedCentralCrossRefGoogle Scholar
  143. 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
  144. 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
  145. Tormay P, Wilting R, Heider J, Böck A (1994) Genes coding for the selenocysteine-inserting tRNA species from Desulfomicrobium baculatum and Clostridium thermoaceticum: structural and evolutionary implications. J Bacteriol 176:1268–1274PubMedPubMedCentralCrossRefGoogle Scholar
  146. Turner RJ, Weiner JH, Taylor DE (1998) Selenium metabolism in Escherichia coli. Biometals 11:223–227PubMedCrossRefGoogle Scholar
  147. Veres Z, Stadtman TC (1994) A purified selenophosphate-dependent enzyme from Salmonella typhimurium catalyzes the replacement of sulfur in 2-thiouridine residues in tRNAs with selenium. Proc Natl Acad Sci U S A 91:8092–8096PubMedPubMedCentralCrossRefGoogle Scholar
  148. Veres Z, Tsai L, Scholz TD, Politino M, Balaban RS, Stadtman T (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 U S A 89:2975–2979PubMedPubMedCentralCrossRefGoogle Scholar
  149. Vorholt JA, Vaupel M, Thauer RK (1997) A selenium-dependent and a selenium-independent formylmethanofuran dehydrogenase and their transcriptional regulation in the hyperthermophilic Methanopyrus kandleri. Mol Microbiol 23:1033–1042PubMedCrossRefGoogle Scholar
  150. Wadhwani SA, Shedbalkar UU, Singh R, Chopade BA (2016) Biogenic selenium nanoparticles: current status and future prospects. Appl Microbiol Biotechnol 100:2555–2566PubMedCrossRefGoogle Scholar
  151. Wagner M, Sonntag D, Grimm R, Pich A, Eckerskorn C, Sohling B, Andreesen JR (1999) Substrate-specific selenoprotein B of glycine reductase from Eubacterium acidaminophilum. Biochemical and molecular analysis. Eur J Biochem 260:38–49PubMedCrossRefGoogle Scholar
  152. Wilting R, Schorling S, Persson BC, Böck A (1997) Selenoprotein synthesis in archaea: identification of an mRNA element of Methanococcus jannaschii probably directing selenocysteine insertion. J Mol Biol 266:637–641PubMedCrossRefGoogle Scholar
  153. Winkel LHE, Vriens B, Jones GD, Schneider LS, Pilon-Smits EAH, Banuelos GS (2015) Selenium cycling across soil-plant-atmosphere interfaces: a critical review. Forum Nutr 7:4199–4239Google Scholar
  154. Wittwer AJ, Tsai L, Ching WM, Stadtman TC (1984) Identification and synthesis of a naturally occurring selenonucleoside in bacterial tRNAs: 5-[(methylamino)methyl]-2-selenouridine. Biochemistry 23:4650–4655PubMedCrossRefGoogle Scholar
  155. Wolfe MD, Ahmed F, Lacourciere GM, Lauhon CT, Stadtman TC, Larson TJ (2004) Functional diversity of the rhodanese homology domain: the Escherichia coli ybbB gene encodes a selenophosphate-dependent tRNA 2-selenouridine synthase. J Biol Chem 279:1801–1809PubMedCrossRefGoogle Scholar
  156. Wu Z, Bañuelos GS, Lin ZQ, Liu Y, Yuan L, Yin X, Li M (2015) Biofortification and phytoremediation of selenium in China. Front Plant Sci 6:136PubMedPubMedCentralGoogle Scholar
  157. Yamazaki S (1982) A selenium-containing hydrogenase from Methanococcus vannielii. Identification of the selenium moiety as a selenocysteine residue. J Biol Chem 257:7926–7929PubMedGoogle Scholar
  158. Yasin M, El Mehdawi AF, Jahn CE, Turner MFS, Faisal M, Pilon-Smits EAH (2015a) Seleniferous soils as a source for production of selenium-enriched foods and potential of bacteria to enhance plant selenium uptake. Plant Soil 386:385–394CrossRefGoogle Scholar
  159. Yasin M, El-Mehdawi AF, Anwar A, Pilon-Smits EAH, Faisal M (2015b) Microbial-enhanced selenium and iron biofortification of wheat (Triticum aestivum L.) – applications in phytoremediation and biofortification. Int J Phytoremediation 17:341–347PubMedCrossRefGoogle Scholar
  160. Yuan J, Palioura S, Salazar JC, Su D, O'Donoghue P, Hohn MJ, Cardoso AM, Whitman WB, Söll D (2006) RNA-dependent conversion of phosphoserine forms selenocysteine in eukaryotes and archaea. Proc Natl Acad Sci U S A 103:18923–18927PubMedPubMedCentralCrossRefGoogle Scholar
  161. Zannoni D, Borsetti F, Harrison JJ, Turner RJ (2008) The bacterial response to the chalcogen metalloids Se and Te. Adv Microb Physiol 53:1–72PubMedCrossRefGoogle Scholar
  162. Zawadzka AM, Crawford RL, Paszczynski AJ (2006) Pyridine-2,6-bis(thiocarboxylic acid) produced by Pseudomonas stutzeri KC reduces and precipitates selenium and tellurium oxyanions. Appl Environ Microbiol 72:3119–3129PubMedPubMedCentralCrossRefGoogle Scholar
  163. Zhang Y, Romero H, Salinas G, Gladyshev VN (2006) Dynamic evolution of selenocysteine utilization in bacteria: a balance between selenoprotein loss and evolution of selenocysteine from redox active cysteine residues. Genome Biol 7:R94PubMedPubMedCentralCrossRefGoogle Scholar
  164. Zhang Y, Turanov AA, Hatfield DL, Gladyshev VN (2008) In silico identification of genes involved in selenium metabolism: evidence for a third selenium utilization trait. BMC Genomics 9:251PubMedPubMedCentralCrossRefGoogle Scholar
  165. Zhu J-M, Johnson TM, Clark SK, Wang X (2014) Selenium redox cycling during weathering of Se-rich shales: a selenium isotope study. Geochim Cosmochim Acta 126:228–249CrossRefGoogle Scholar
  166. Zinoni F, Birkmann A, Stadtman TC, Böck A (1986) Nucleotide sequence and expression of the selenocysteine-containing polypeptide of formate dehydrogenase (formate-hydrogen-lyase-linked) from Escherichia coli. Proc Natl Acad Sci U S A 83:4650–4654PubMedPubMedCentralCrossRefGoogle Scholar
  167. Zinoni F, Birkmann A, Leinfelder W, Böck A (1987) Cotranslational insertion of selenocysteine into formate dehydrogenase from Escherichia coli directed by a UGA codon. Proc Natl Acad Sci U S A 84:3156–3160PubMedPubMedCentralCrossRefGoogle Scholar
  168. Zolotarev AS, Unnikrishnan M, Shmukler BE, Clark JS, Vandorpe DH, Grigorieff N, Rubin EJ, Alper SL (2008) Increased sulfate uptake by E. coli overexpressing the SLC26-related SulP protein Rv1739c from Mycobacterium tuberculosis. A Mol Integr Physiol 149:255–266CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  • Lucian C. Staicu
    • 1
  • Ronald S. Oremland
    • 2
  • Ryuta Tobe
    • 3
  • Hisaaki Mihara
    • 3
    Email author
  1. 1.Faculty of Applied Chemistry and Materials ScienceUniversity Politehnica of BucharestBucharestRomania
  2. 2.US Geological SurveyMenlo ParkUSA
  3. 3.Laboratory of Applied Molecular Microbiology, Department of BiotechnologyCollege of Life Sciences, Ritsumeikan UniversityKusatsuJapan

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