BACKGROUND: Selenium is a trace element performing important biological functions in many organisms including humans. It usually affects organisms in a strictly dosage-dependent manner being essential at low and toxic at higher concentrations. The impact of selenium on mammalian and land plant cells has been quite extensively studied. Information about algal cells is rare despite of the fact that they could produce selenium enriched biomass for biotechnology purposes. RESULTS: We studied the impact of selenium compounds on the green chlorococcal alga Scenedesmus quadricauda. Both the dose and chemical forms of Se were critical factors in the cellular response. Se toxicity increased in cultures grown under sulfur deficient conditions. We selected three strains of Scenedesmus quadricauda specifically resistant to high concentrations of inorganic selenium added as selenite (Na2SeO3) - strain SeIV, selenate (Na2SeO4) - strain SeVI or both - strain SeIV+VI. The total amount of Se and selenomethionine in biomass increased with increasing concentration of Se in the culturing media. The selenomethionine made up 30-40% of the total Se in biomass. In both the wild type and Se-resistant strains, the activity of thioredoxin reductase, increased rapidly in the presence of the form of selenium for which the given algal strain was not resistant. CONCLUSION: The selenium effect on the green alga Scenedesmus quadricauda was not only dose dependent, but the chemical form of the element was also crucial. With sulfur deficiency, the selenium toxicity increases, indicating interference of Se with sulfur metabolism. The amount of selenium and SeMet in algal biomass was dependent on both the type of compound and its dose. The activity of thioredoxin reductase was affected by selenium treatment in dose-dependent and toxic-dependent manner. The findings implied that the increase in TR activity in algal cells was a stress response to selenium cytotoxicity. Our study provides a new insight into the impact of selenium on green algae, especially with regard to its toxicity and bioaccumulation.

Laboratory of Cell Cycles of Algae Division of Autotrophic Microorganisms Institute of Microbiology Academy of Sciences of the Czech Republic 379 81 Trebon Czech Republic

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Ebert R, Ulmer M, Zeck S, Meissner-Weigl J, Schneider D, Stopper H, Schupp N, Kassem M, Jakob F. Selenium supplementation restores the antioxidative capacity and prevents cell damage in bone marrow stromal cells in vitro. Stem Cells. 2006;24:1226–1235. PubMed

Chang WP, Combs GFJ, Scanes CG, Marsh JA. The effects of dietary vitamin E and selenium deficiencies on plasma thyroid and thymic hormone concentrations in the chicken. Dev Comp Immunol. 2005;29:265–273. PubMed

Patrick L. Selenium biochemistry and cancer: A review of the literature. Altern Med Rev. 2004;9:239–258. PubMed

Schomburg L, Schweizer U, Kohrle J. Selenium and selenoproteins in mammals: extraordinary, essential, enigmatic. Cell Mol Life Sci. 2004;61:1988–1995. PubMed PMC

Arthur JR, McKenzie RC, Beckett GJ. Selenium in the immune system. J Nutr. 2003;133:1457–1459. PubMed

Rayman MP. The importance of selenium to human health. Lancet. 2000;356:233–241. PubMed

Letavayova L, Vlckova V, Brozmanova J. Selenium: From cancer prevention to DNA damage. Toxicology. 2006;227:1–14. PubMed

Baines SB, Fisher NS, Doblin MA, Cutter GA, Cutter LS, Cole B. Light dependence of selenium uptake by phytoplankton and implications for predicting selenium incorporation into food webs. Limnol Oceanogr. 2004;49:566–578.

Doblin MA, Blackburn SI, Hallegraeff GM. Comparative study of selenium requirements of three phytoplankton species: Gymnodinium catenatum, Alexandrium minutum (Dinophyta) and Chaetoceros cf. tenuissimus (Bacillariophyta) J Plankton Res. 1999;21:1153–1169.

Danbara A, Shiraiwa Y. The requirement of selenium for the growth of marine coccolithophorids, Emiliania huxleyi, Gephyrocapsa oceanica and Helladosphaera sp (Prymnesiophyceae) Plant Cell Physiol. 1999;40:762–766.

Harrison PJ, Yu PW, Thompson PA, Price NM, Phillips DJ. Survey of selenium requirements in marine phytoplankton. Marine Ecol-Progr Ser. 1988;47:89–96.

Fu L-H, Wang X-F, Eyal Y, She Y-M, Donald L-J, Standing KG, Ben-Hayyim G. A selenoprotein in the plant kingdom. J Biol Chem. 2002;277:25983–25991. PubMed

Merchant SS, Allen MD, Kropat J, Moseley JL, Long JC, Tottey S, Terauchi AM. Between a rock and a hard place: Trace element nutrition in Chlamydomonas. Biochim Biophys Acta. 2006;1763:578–594. PubMed

Stadtman TC. Selenocysteine. Annu Rev Biochem. 1996;65:83–100. PubMed

Kryukov GV, Castellano S, Novoselov SV, Lobanov AV, Zehtab O, Guigo R, Gladyshev VN. Characterization of mammalian selenoproteomes. Science. 2003;300:1439–1443. PubMed

Novoselov SV, Rao M, Onoshko NV, Zhi H, Kryukov GV, Xiang Y, Weeks DP, Hatfield DL, Gladyshev VN. Selenoproteins and selenocysteine insertion system in the model plant cell system Chlamydomonas reinhardtii. EMBO J. 2002;21:3681–3693. PubMed PMC

Grossman AR, Croft M, Gladyshev VN, Merchant SS, Posewitz MC, Prochnik S, Spalding MH. Novel metabolism in Chlamydomonas through the lens of genomics. Curr Opin Plant Biol. 2007;10:190–198. PubMed

Lobanov AV, Fomenko DE, Zhang Y, Sengupta A, Hatfield DL, Gladyshev VN. Evolutionary dynamics of eukaryotic selenoproteomes: large selenoproteomes may associate with aquatic life and small with terrestrial life. Genome Biol. 2007;8:R198. PubMed PMC

Maruyama S, Misumi O, Ishii Y, Asakawa S, Shimizu A, Sasaki T, Matsuzaki M, Shin-i T, Nozaki H, Kohara Y, et al. The minimal eukaryotic ribosomal DNA units in the primitive red alga Cyanidioschyzon merolae. DNA Res. 2004;11:83–91. PubMed

Derelle E, Ferraz C, Rombauts S, Rouze P, Worden AZ, Robbens S, Partensky F, Degroeve S, Echeynie S, Cooke R, et al. Genome analysis of the smallest free-living eukaryote Ostreococcus tauri unveils many unique features. Proc Natl Acad Sci USA. 2006;103:11647–11652. PubMed PMC

Palenik B, Grimwood J, Aerts A, Rouze P, Salamov A, Putnam N, Dupont C, Jorgensen R, Derelle E, Rombauts S, et al. The tiny eukaryote Ostreococcus provides genomic insights into the paradox of plankton speciation. Proc Natl Acad Sci U S A. 2007;104:7705–7710. PubMed PMC

Araie H, Suzuki I, Shiraiwa Y. Identification and characterization of a selenoprotein, thioredoxin reductase, in a unicellular marine haptophyte lga, Emiliania huxleyi. J Biol Chem. 2008;283:35329–35336. PubMed

Gromer S, Urig S, Becker K. The thioredoxin system – from science to clinic. Med Res Rev. 2004;24:40–89. PubMed

Hanikenne M, Merchant SS, Hamel P. Transition metal nutrition: A balance between deficiency and toxicity. In: Stern D, editor. The Chlamydomonas sourcebook, organellar and metabolic processes. Vol. 2. Amsterdam, Boston, Heidelberg, London, New York, Oxford, Paris, San Diego, San Francisco, Sydney, Tokyo: Academic Press Elsevier; 2009. pp. 333–379.

Meyers J, Craig J, Odde DJ. Potential for control of signaling pathways via cell size and shape. Curr Biol. 2006;16:1685–1693. PubMed

Crosley LK, Méplan C, Nicol F, Rundlőf AK, Arnér ESJ, Hesketh JE, Arthur JR. Differential regulation of expression of cytosolic and mitochondrial thioredoxin reductase in rat liver and kidney. Arch Biochem Biophys. 2007;459:178–188. PubMed

Madeja Z, Sroka J, Nystrőm C, Bjőrkhem-Bergman L, Nordman T, Damdimopoulos A, Nalvarte I, Eriksson LC, Spyrou G, Olsson JM, et al. The role of thioredoxin reductase activity in selenium-induced cytotoxicity. Biochem Pharmacol. 2005;69:1765–1772. PubMed

Zhang JZ, Peng DG, Lu HJ, Liu QL. Attenuating the toxicity of cisplatin by using selenosulfate with reduced risk of selenium toxicity as compared with selenite. Toxicol Appl Pharmacol. 2008;226:251–259. PubMed

Brown TA, Shrift A. Selenium – toxicity and tolerance in higher plants. Biol Rev Cambridge Philosoph Soc. 1982;57:59–84.

Geoffroy L, Gilbin R, Simon O, Floriani M, Adam C, Pradines C, Cournac L, Garnier-Laplace J. Effect of selenate on growth and photosynthesis of Chlamydomonas reinhardtii. Aquat Toxicol. 2007;83:149–158. PubMed

Morlon H, Fortin C, Floriani M, Adam C, Garnier-Laplace J, Boudou AB. Toxicity of selenite in the unicellular green alga Chlamydomonas reinhardtii : Comparison between effects at the population and sub-cellular level. Aquat Toxicol. 2005;73:65–78. PubMed

Morlon H, Fortin C, Adam C, Garnier-Laplace J. Selenite transport and its inhibition in the unicellular green alga Chlamydomonas reinhardtii. Environ Toxicol Chem. 2006;25:1408–1417. PubMed

Yu MK, Moos PJ, Cassidy P, Wade M, Fitzpatrick FA. Conditional expression of 15-lipoxygenase-1 inhibits the selenoenzyme thioredoxin reductase: modulation of selenoproteins by lipoxygenase enzymes. J Biol Chem. 2004;279:28028–28035. PubMed

Pelah D, Cohen E. Cellular response of Chlorella zofingiensis to exogenous selenium. Plant Growth Reg. 2005;45:225–232.

Doušková I, Hlavová M, Umysová D, Vítová M, Zachleder V. Industrial strain Scenedesmus quadricauda SeIV of the green chlorococcal alga Scenedesmus quadricauda (Turp.) Bréb. PV 2007-765 (Z7560) in Czech. 2007.

Doušková I, Hlavová M, Umysová D, Vítová M, Zachleder V. Industrial strain Scenedesmus quadricauda SeVI of the green chlorococcal alga Scenedesmus quadricauda (Turp.) Bréb. PV 2007-766 (Z7561) in Czech. 2007.

Doušková I, Hlavová M, Umysová D, Vítová M, Zachleder V. Industrial strain Scenedesmus quadricauda SeIV+VI of the green chlorococcal alga Scenedesmus quadricauda (Turp.) Bréb. PV 2007-764 (Z7559) in Czech. 2007.

Gouget B, Avoscan L, Sarret G, Collins R, Carriere M. Resistance, accumulation and transformation of selenium in the cyanobacterium Synechocystis sp. PCC 6803 after exposure to inorganic Se-VI or Se-IV. Radiochim Acta. 2005;93:683–689.

Terry N, Zayed AM, de Souza MP, Tarun AS. Selenium in higher plants. Annu Rev Plant Physiol Plant Mol Biol. 2000;51:401–432. PubMed

Lindblow-Kull C, Kull FJ, Shrift A. Single transporter for sulfate, selenate, and selenite in Escherichia coli K-12. J Bacteriol. 1985;163:1267–1269. PubMed PMC

Cherest H, Davidian JC, Thomas D, Benes V, Ansorge W, Surdin-Kerjan Y. Molecular characterization of two high affinity sulfate transporters in Saccharomyces cerevisiae. Genetics. 1997;145:627–635. PubMed PMC

Yu XZ, Gu JD. Differences in uptake and translocation of selenate and selenite by the weeping willow and hybrid willow. Environ Sci Pollut Res Int. 2008;15:499–508. PubMed

Wheeler AE, Zingaro RA, Irgolic K, Bottino NR. The effect of selenate, selenite, and sulfate on the growth of 6 unicellular marine-species. J Exp Mar Biol Ecol. 1982;57:181–194.

Riedel GF, Sanders JG, Gilmour CC. Uptake, transformation, and impact of selenium in freshwater phytoplankton and bacterioplankton communities. Aquatic Microbial Ecol. 1996;11:43–51.

Li HF, McGrath SP, Zhao FJ. Selenium uptake, translocation and speciation in wheat supplied with selenate or selenite. New Phytologist. 2008;178:92–102. PubMed

Anderson JW, Scarf AR. Selenium and plant metabolism. In: Robb DA, editor. Metals and micronutrients: uptake and utilization by plants. Piermont WS: Academic Press; 1983. pp. 241–275.

Zayed A, Lytle CM, Terry N. Accumulation and volatilization of different chemical species of selenium by plants. Planta. 1998;206:284–292.

Wu L, Huang ZZ, Burau RG. Selenium accumulation and selenium-salt cotolerance in 5 grass species. Crop Sci. 1988;28:517–522.

Larsen EH, Hansen M, Fan T, Vahl M. Speciation of selenoamino acids, selenonium ions and inorganic selenium by ion exchange HPLC with mass spectrometric detection and its application to yeast and algae. J Analyt Atom Spectrom. 2001;16:1403–1408.

Neumann PM, De Souza MP, Pickering IJ, Terry N. Rapid microalgal metabolism of selenate to volatile dimethylselenide. Plant Cell Environ. 2003;26:897–905. PubMed

Bjőrnstedt M, Kumar S, Holmgren A. Methods in Enzymology. Vol. 252. Academic Press; 1995. Selenite and selenogluttathione – Reactions with thioredoxin systems; pp. 209–219. PubMed

Xiao L. Lipid Hydroperoxide (LOOH) Free Radical Rad Biol Prog. 2003. pp. 1–12.

Bjőrnstedt M, Kumar S, Holmgren A. Selenodiglutathione is a higly efficiant oxidant of reduced thioredoxin and a substrate for mammalian thiredoxin reductase. J Biol Chem. 1992;267:8030–8034. PubMed

Zachleder V, Setlik I. Effect of irradiance on the course of RNA synthesis in the cell-cycle of Scenedesmus quadricauda. Biol Plant. 1982;24:341–353.

Wrobel K, Kannamkumarath SS, Wrobel K, Caruso JA. Hydrolysis of proteins with methanesulfonic acid for improved HPLC-ICP-MS determination of seleno-methionine in yeast and nuts. Anal Bioanal Chem. 2003;375:133–138. PubMed

Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle protein-dye binding. Analyt Biochem. 1976;72:248–254. PubMed

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