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Sulfur Metabolism in Phototrophic Organisms pp 231–267Cite as

The State of Sulfur Metabolism in Algae: From Ecology to Genomics

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Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 27))

Sulfur, primarily in the form of sulfate, is transported into algal and plant cells and reduced to sulfide in the chloroplast. Both sulfate and sulfide can be incorporated into a variety of sulfur-containing compounds critical for protein, lipid and polysaccharide synthesis, as well as signaling molecules. Most of our current knowledge about sulfur metabolism and the acclimation of photosynthetic organisms to conditions of sulfur deprivation, especially at the molecular level, are from studies that have exploited the model plant Arabidopsis thaliana, or the freshwater alga Chlamydomonas reinhardtii. However, there are also novel aspects of the biosynthesis and function of sulfur metabolites, especially volatile metabolites synthesized by marine algae that might have antifreeze and antioxidant functions and also influence global features of climate. This chapter describes sulfate assimilation in algae and the adaptation and acclimation of algae to changing sulfur environments.

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References

  • Aguilera, A. and Amils, R. (2005) Tolerance to cadmium in Chlamydomonas sp. (Chlorophyta) strains isolated from an extreme acidic environment, the Tinto River (SW, Spain). Aquat Toxicol, 75, 316–329.

    Article  PubMed  CAS  Google Scholar 

  • Anantharaman, V., Koonin, E.V. and Aravind, L. (2001) Regulatory potential, phyletic distribution and evolution of ancient, intracellular small-molecule-binding domains. J Mol Biol, 307, 1271–1292.

    Article  PubMed  CAS  Google Scholar 

  • Andreae, M.O. and Crutzen, P.J. (1997) Atmospheric aerosols: biogeochemical sources and role in atmospheric chemistry. Science, 276, 1052–1058.

    Article  CAS  Google Scholar 

  • Andreae, M.O. and Raemdonch, H., 1983. (1983) Dimethyl sulfide in the surface ocean and the marine atmosphere – A global view. Science, 221, 744.

    Article  PubMed  CAS  Google Scholar 

  • Antal, T.K. and Lindblad, P. (2005) Production of H2 by sulphur-deprived cells of the unicellular cyanobacteria Gloeocapsa alpicola and Synechocystis sp. PCC 6803 during dark incubation with methane or at various extracellular pH. J Appl Microbiol, 98, 114–120.

    Article  CAS  Google Scholar 

  • Arz, H.E., Gisselmann, G., Schiffmann, S. and Schwenn, J.D. (1994) A cDNA for adenylyl sulphate (APS)-kinase from Arabidopsis thaliana. Biochim Biophys Acta, 1218, 447–452.

    PubMed  CAS  Google Scholar 

  • Ashida, H., Sawa, Y. and Shibata, H. (2005) Cloning, biochemical and phylogenetic characterizations of gamma-glutamylcysteine synthetase from Anabaena sp. PCC 7120. Plant Cell Physiol, 46, 557–562.

    Article  PubMed  CAS  Google Scholar 

  • Aviles, C., Torres-Marquez, M.E., Mendoza-Cozatl, D. and Moreno-Sanchez, R. (2005) Time-course development of Cd2+ hyper-accumulating phenotype in Euglena gracilis. Arch Microbiol, 184, 83–92.

    Article  PubMed  CAS  Google Scholar 

  • Bacic, M.K. and Yoch, D.C. (1998) In vivo characterization of dimethylsulfoniopropionate lyase in the fungus Fusarium lateritium. Appl Environ Microbiol, 64, 106–111.

    PubMed  CAS  Google Scholar 

  • Ball, S.G., Dirick, L., Decq, A., Martiat, J.C. and Matagne, R.F. (1990) Physiology of starch storage in the monocellular alga Chlamydomonas reinhardtii. Plant Sci, 66, 1–9.

    Article  CAS  Google Scholar 

  • Balmer, Y., Koller, A., del Val, G., Manieri, W., Schurmann, P. and Buchanan, B.B. (2003) Proteomics gives insight into the regulatory function of chloroplast thioredoxins. Proc Natl Acad Sci U S A, 100, 370–375.

    Article  PubMed  CAS  Google Scholar 

  • Barnes, I., Becker, K.H. and Patroescu, I. (1994) The tropospheric oxidation of dimethyl sulfide: A new source of carbonyl sulfide. Geophys Res Lett, 21, 2389.

    Article  CAS  Google Scholar 

  • Bates, T.S., Cline, J.D., Gammon, R.H. and Kelly-Hansen, S. (1987) Regional and seasonal variations in the flux of oceanic dimethylsulfide to the atmosphere. J Geophys Res, 92, 2930–2938.

    Article  CAS  Google Scholar 

  • Baudouin-Cornu, P., Surdin-Kerjan, Y., Marliere, P. and Thomas, D. (2001) Molecular evolution of protein atomic composition. Science, 293, 297–300.

    Article  PubMed  CAS  Google Scholar 

  • Beeor-Tzahar, T., Ben-Hayyim, G., Holland, D. and Faltin, Z. (1995) A stress-associated citrus protein is a distinct plant phospholipid hydroperoxide glutathione peroxidase. FEBS Lett, 366, 151–155.

    Article  PubMed  CAS  Google Scholar 

  • Benning, C. (1998) Biosynthesis and function of the sulfolipid sulfoquinovosyl diacylglycerol. Annu Rev Plant Physiol Plant Mol Biol, 49, 53–75.

    Article  PubMed  CAS  Google Scholar 

  • Bick, J.A., Dennis, J.J., Zylstra, G.J., Nowack, J. and Leustek, T. (2000) Identification of a new class of 5′-adenylylsulfate (APS) reductases from sulfate-assimilating bacteria. J Bacteriol, 182, 135–142.

    Article  PubMed  CAS  Google Scholar 

  • Bolling, C. and Fiehn, O. (2005) Metabolite profiling of Chlamydomonas reinhardtii under nutrient deprivation. Plant Physiol, 139, 1995–2005.

    Article  PubMed  CAS  Google Scholar 

  • Bouarab, K., Potin, P., Correa, J. and Kloareg, B. (1999) Sulfated oligosaccharides mediate the interaction between a marine red alga and its green algal pathogenic endophyte. Plant Cell, 11, 1635–1650.

    Article  PubMed  CAS  Google Scholar 

  • Buchanan, B.B. and Balmer, Y. (2005) Redox regulation: a broadening horizon. Annu Rev Plant Biol, 56, 187–220.

    Article  PubMed  CAS  Google Scholar 

  • Buchner, P., Takahashi, H. and Hawkesford, M.J. (2004) Plant sulphate transporters: co-ordination of uptake, intracellular and long-distance transport. J Exp Bot, 55, 1765–1773.

    Article  PubMed  CAS  Google Scholar 

  • Buetow, D.E. and Buchanan, P.J. (1964) Isolation of mitochondria from Euglena gracilis. Exp Cell Res, 36, 204–207.

    Article  PubMed  CAS  Google Scholar 

  • Callow, M.E. and Evans, L.V. (1979) Polyphosphate accumulation in sulphur-starved cells of Rhodella maculata. Br Phycol J, 14, 327–337.

    Article  Google Scholar 

  • Cantoni, G.L. and Anderson, D.G. (1956) Enzymatic cleavage of dimethylpropiothetin by Polysiphonia lanosa. J Biol Chem, 222, 171–177.

    PubMed  CAS  Google Scholar 

  • Casagrande, S., Bonetto, V., Fratelli, M., Gianazza, E., Eberini, I., Massignan, T., Salmona, M., Chang, G., Holmgren, A. and Ghezzi, P. (2002) Glutathionylation of human thioredoxin: a possible crosstalk between the glutathione and thioredoxin systems. Proc Natl Acad Sci U S A, 99, 9745–9749.

    Article  PubMed  CAS  Google Scholar 

  • Challenger, F. and Simpson, M.I. (1948) Studies on biological methylation. Part XII. A precursor of dimethyl sulfide evolved by Polysiphonia fastigiata. Dimethyl-2-carboxyethyl sulphonium hydroxide and its salts. J Chem Soc, 1948, 1591–1597.

    Article  Google Scholar 

  • Charlson, R.J., Lovelock, J.E., Andreae, M.O. and Warren, S.G. (1987) Oceanic phytoplankton, atmospheric sulphur, cloud albedo and climate. Nature, 326, 655–661.

    Article  CAS  Google Scholar 

  • Chen, H.C. and Melis, A. (2004) Localization and function of SulP, a nuclear-encoded chloroplast sulfate permease in Chlamydomonas reinhardtii. Planta, 220, 198–210.

    Article  PubMed  CAS  Google Scholar 

  • Chen, H.C., Newton, A.J. and Melis, A. (2005) Role of SulP, a nuclear-encoded chloroplast sulfate permease, in sulfate transport and H2 evolution in Chlamydomonas reinhardtii. Photosynth Res, 84, 289–296.

    Article  PubMed  CAS  Google Scholar 

  • Chen, H.C., Yokthongwattana, K., Newton, A.J. and Melis, A. (2003) SulP, a nuclear gene encoding a putative chloroplast-targeted sulfate permease in Chlamydomonas reinhardtii. Planta, 218, 98–106.

    Article  PubMed  CAS  Google Scholar 

  • Clemens, S. (2006) Evolution and function of phytochelatin synthases. J Plant Physiol, 163, 319–332.

    Article  PubMed  CAS  Google Scholar 

  • Coates, J.B., Medeiros, J.S., Thanh, V.H. and Nielsen, N.C. (1985) Characterization of the subunits of beta-conglycinin. Arch Biochem Biophys, 243, 184–194.

    Article  PubMed  CAS  Google Scholar 

  • Cohen, I., Knopf, J.A., Irihimovitch, V. and Shapira, M. (2005) A proposed mechanism for the inhibitory effects of oxidative stress on Rubisco assembly and its subunit expression. Plant Physiol, 137, 738–746.

    Article  PubMed  CAS  Google Scholar 

  • Cohen, I., Sapir, Y. and Shapira, M. (2006) A conserved mechanism controls translation of Rubisco large subunit in different photosynthetic organisms. Plant Physiol, 141, 1089–1097.

    Article  PubMed  CAS  Google Scholar 

  • Collier, J.L. and Grossman, A.R. (1992) Chlorosis induced by nutrient deprivation in Synechococcus sp. strain PCC 7942: not all bleaching is the same. J Bacteriol, 174, 4718–4726.

    PubMed  CAS  Google Scholar 

  • Collier, J.L. and Grossman, A.R. (1994) A small polypeptide triggers complete degradation of light-harvesting phycobiliproteins in nutrient-deprived cyanobacteria. Embo J, 13, 1039–1047.

    PubMed  CAS  Google Scholar 

  • Copley, S.D. and Dhillon, J.K. (2002) Lateral gene transfer and parallel evolution in the history of glutathione biosynthesis genes. Genome Biol, 3, research0025.

    Google Scholar 

  • Craigie, J. (1990) Cells walls. In Cole, K. and Sheath, R. (eds.), Biology of the Red Algae. Cambridge University Press, Cambridge.

    Google Scholar 

  • Croft, M.T., Lawrence, A.D., Raux-Deery, E., Warren, M.J. and Smith, A.G. (2005) Algae acquire vitamin B12 through a symbiotic relationship with bacteria. Nature, 438, 90–93.

    Article  PubMed  CAS  Google Scholar 

  • Dacey, J.W.H., Howse, F.A., Michaels, A.F. and Wakeham, S.G. (1998) Temporal variability of dimethylsulfide and dimethylsulfoniopropionate in the Sargasso Sea. Deep-Sea Research, 45, 2085–2104.

    Article  CAS  Google Scholar 

  • Danon, A. and Mayfield, S.P. (1991) Light regulated translational activators: identification of chloroplast gene specific mRNA binding proteins. Embo J, 10, 3993–4001.

    PubMed  CAS  Google Scholar 

  • Danon, A. and Mayfield, S.P. (1994a) ADP-dependent phosphorylation regulates RNA-binding in vitro: implications in light-modulated translation. Embo J, 13, 2227–2235.

    PubMed  CAS  Google Scholar 

  • Danon, A. and Mayfield, S.P. (1994b) Light-regulated translation of chloroplast messenger RNAs through redox potential. Science, 266, 1717–1719.

    Article  PubMed  CAS  Google Scholar 

  • Dashwood, R.H. (1998) Indole-3-carbinol: anticarcinogen or tumor promoter in brassica vegetables? Chem Biol Interact 110, 1–5.

    Article  PubMed  CAS  Google Scholar 

  • Davies, J.P., Weeks, D.P. and Grossman, A.R. (1992) Expression of the arylsulfatase gene from the ß2-tubulin promoter in Chlamydomonas reinhardtii. Nucleic Acids Res, 20, 2959–2965.

    Article  PubMed  CAS  Google Scholar 

  • Davies, J.P., Yildiz, F. and Grossman, A.R. (1994) Mutants of chlamydomonas with aberrant responses to sulfur deprivation. Plant Cell, 6, 53–63.

    Article  PubMed  CAS  Google Scholar 

  • Davies, J.P., Yildiz, F.H. and Grossman, A. (1996) Sac1, a putative regulator that is critical for survival of Chlamydomonas reinhardtii during sulfur deprivation. Embo J, 15, 2150–2159.

    PubMed  CAS  Google Scholar 

  • Davies, J.P., Yildiz, F.H. and Grossman, A.R. (1999) Sac3, an Snf1-like serine/threonine kinase that positively and negatively regulates the responses of Chlamydomonas to sulfur limitation. Plant Cell, 11, 1179–1190.

    Article  PubMed  CAS  Google Scholar 

  • de Hostos, E.L., Schilling, J. and Grossman, A.R. (1989) Structure and expression of the gene encoding the periplasmic arylsulfatase of Chlamydomonas reinhardtii. Mol Gen Genet, 218, 229–239.

    Article  PubMed  Google Scholar 

  • de Hostos, E.L., Togasaki, R.K. and Grossman, A.R. (1988) Purification and biosynthesis of a derepressible periplasmic arylsulfatase from Chlamydomonas reinhardtii. J Cell Biol, 106, 29–37.

    Article  PubMed  Google Scholar 

  • de Souza, M.P. and Yoch, D.C. (1995a) Comparative physiology of dimethyl sulfide production by dimethylsulfoniopropionate lyase in Pseudomonas doudoroffii and Alcaligenes sp. strain M3A. Appl Environ Microbiol, 61, 3986–3991.

    PubMed  Google Scholar 

  • de Souza, M.P. and Yoch, D.C. (1995b) Purification and characterization of dimethylsulfoniopropionate lyase from an Alcaligenes-like dimethyl sulfide-producing marine isolate. Appl Environ Microbiol, 61, 21–26.

    PubMed  Google Scholar 

  • de Souza, M.P. and Yoch, D.C. (1996) Differential metabolism of dimethylsulphoniopropionate and acrylate in saline and brackish intertidal sediments. Microbial Ecol, 31, 319–330.

    Article  Google Scholar 

  • Derelle, E., Ferraz, C., Rombauts, S., Rouze, P., Worden, A.Z., Robbens, S., Partensky, F., Degroeve, S., Echeynie, S., Cooke, R., Saeys, Y., Wuyts, J., Jabbari, K., Bowler, C., Panaud, O., Piegu, B., Ball, S.G., Ral, J.P., Bouget, F.Y., Piganeau, G., De Baets, B., Picard, A., Delseny, M., Demaille, J., Van de Peer, Y. and Moreau, H. (2006) Genome analysis of the smallest free-living eukaryote Ostreococcus tauri unveils many unique features. Proc Natl Acad Sci U S A, 103, 11647–11652.

    Article  PubMed  CAS  Google Scholar 

  • Dickson, D.M.J. and Kirst, G.O. (1987) Osmotic adjustment in marine eukaryotic algae: The role of inorganic ions, quaternary ammonium, tertiary sulphonium and carbohydrate solutes. II. Prasinophytes and haptophytes. New Phytologist, 106, 657–666.

    Article  CAS  Google Scholar 

  • Domínguez, M.J., Gutierrez, F., Leon, R., Vilchez, C., Vega, J.M. and Vigara, J. (2003) Cadmium increases the activity levels of glutamate dehydrogenase and cysteine synthase in Chlamydomonas reinhardtii. Plant Physiol Biochem, 41, 828–832.

    Article  CAS  Google Scholar 

  • Eberhard, S., Jain, M., Im, C.S., Pollock, S., Shrager, J., Lin, Y., Peek, A.S. and Grossman, A.R. (2006) Generation of an oligonucleotide array for analysis of gene expression in Chlamydomonas reinhardtii. Curr Genet, 49, 106–124.

    Article  PubMed  CAS  Google Scholar 

  • El-Naggar, A.H. and El-Sheekh, M.M. (1998) Abolishing cadmium toxicity in Chlorella vulgaris by ascorbic acid, calcium, glucose and reduced glutathione. Environ Pollution, 101, 169–174.

    Article  CAS  Google Scholar 

  • Fabregas, J., Garca, D., Fernandez-Alonso, M., Rocha, A.I., Gomez-Puertas, P., Escribano, J.M., Otero, A. and Coll, J.M. (1999) In vitro inhibition of the replication of haemorrhagic septicaemia virus (VHSV) and African swine fever virus (ASFV) by extracts from marine microalgae. Antiviral Research, 44, 67–73.

    Article  PubMed  CAS  Google Scholar 

  • Fahey, R.C., Buschbacher, R.M. and Newton, G.L. (1987) The evolution of glutathione metabolism in phototrophic microorganisms. J Mol Evol, 25, 81–88.

    Article  PubMed  CAS  Google Scholar 

  • Faller, P., Kienzler, K. and Krieger-Liszkay, A. (2005) Mechanism of Cd2+ toxicity: Cd2+ inhibits photoactivation of Photosystem II by competitive binding to the essential Ca2+ site. Biochim Biophys Acta, 1706, 158–164.

    Article  PubMed  CAS  Google Scholar 

  • Ferrari, D.M. and Soling, H.D. (1999) The protein disulphide-isomerase family: unravelling a string of folds. Biochem J, 339 (Pt 1), 1–10.

    Article  PubMed  CAS  Google Scholar 

  • Florencio, F.J., Yee, B.C., Johnson, T.C. and Buchanan, B.B. (1988) An NADP/thioredoxin system in leaves: purification and characterization of NADP-thioredoxin reductase and thioredoxin h from spinach. Arch Biochem Biophys, 266, 496–507.

    Article  PubMed  CAS  Google Scholar 

  • Fong, C.L., Lentz, A. and Mayfield, S.P. (2000) Disulfide bond formation between RNA binding domains is used to regulate mRNA binding activity of the chloroplast poly(A)-binding protein. J Biol Chem, 275, 8275–8278.

    Article  PubMed  CAS  Google Scholar 

  • Fouchard, S., Hemschemeier, A., Caruana, A., Pruvost, J., Legrand, J., Happe, T., Peltier, G. and Cournac, L. (2005) Autotrophic and mixotrophic hydrogen photoproduction in sulfur-deprived chlamydomonas cells. Appl Environ Microbiol, 71, 6199–6205.

    Article  PubMed  CAS  Google Scholar 

  • Fu, L.H., Wang, X.F., Eyal, Y., She, Y.M., Donald, L.J., Standing, K.G. and Ben-Hayyim, G. (2002) A selenoprotein in the plant kingdom. Mass spectrometry confirms that an opal codon (UGA) encodes selenocysteine in Chlamydomonas reinhardtii gluththione peroxidase. J Biol Chem, 277, 25983–25991.

    Article  PubMed  CAS  Google Scholar 

  • Gaber, A., Tamoi, M., Takeda, T., Nakano, Y. and Shigeoka, S. (2001) NADPH-dependent glutathione peroxidase-like proteins (Gpx-1, Gpx-2) reduce unsaturated fatty acid hydroperoxides in Synechocystis PCC 6803. FEBS Lett, 499, 32–36.

    Article  PubMed  CAS  Google Scholar 

  • Gaber, A., Yoshimura, K., Tamoi, M., Takeda, T., Nakano, Y. and Shigeoka, S. (2004) Induction and functional analysis of two reduced nicotinamide adenine dinucleotide phosphate-dependent glutathione peroxidase-like proteins in Synechocystis PCC 6803 during the progression of oxidative stress. Plant Physiol, 136, 2855–2861.

    Article  PubMed  CAS  Google Scholar 

  • Gaffron, H. and Rubin, J. (1942) Fermentation and photochemical production of hydrogen in algae. J Gen Physiol, 26, 219–241.

    Article  CAS  PubMed  Google Scholar 

  • Gage, D.A., Rhodes, D., Nolte, K.D., Hicks, W.A., Leustek, T., Cooper, A.J. and Hanson, A.D. (1997) A new route for synthesis of dimethylsulphoniopropionate in marine algae. Nature, 387, 891–894.

    Article  PubMed  CAS  Google Scholar 

  • Gao, Y., Schofield, O.M. and Leustek, T. (2000) Characterization of sulfate assimilation in marine algae focusing on the enzyme 5′-adenylylsulfate reductase. Plant Physiol, 123, 1087–1096.

    Article  PubMed  CAS  Google Scholar 

  • Gayler, K.R. and Sykes, G.E. (1985) Effects of nutritional stress on the storage proteins of soybeans. Plant Physiol, 78, 582–585.

    Article  PubMed  CAS  Google Scholar 

  • Geigenberger, P., Kolbe, A. and Tiessen, A. (2005) Redox regulation of carbon storage and partitioning in response to light and sugars. J Exp Bot, 56, 1469–1479.

    Article  PubMed  CAS  Google Scholar 

  • Gekeler, W., Grill, E., Winnacker, E.-L. and Zenk, M.H. (1988) Algae sequester heavy metals via synthesis of phytochelatin complexes. Arch Microbiol, 150, 197–202.

    Article  CAS  Google Scholar 

  • Ghirardi, M.L., Zhang, L., Lee, J.W., Flynn, T., Seibert, M., Greenbaum, E. and Melis, A. (2000) Microalgae: a green source of renewable H2. Trends Biotechnol, 18, 506–511.

    Article  PubMed  CAS  Google Scholar 

  • Giordano, M., Pezzoni, V. and Hell, R. (2000) Strategies for the allocation of resources under sulfur limitation in the green alga Dunaliella salina. Plant Physiol, 124, 857–864.

    Article  PubMed  CAS  Google Scholar 

  • Gladyshev, V.N. and Kryukov, G.V. (2001) Evolution of selenocysteine-containing proteins: significance of identification and functional characterization of selenoproteins. Biofactors, 14, 87–92.

    Article  PubMed  CAS  Google Scholar 

  • Gleason, F.K., Whittaker, M.M., Holmgren, A. and Jornvall, H. (1985) The primary structure of thioredoxin from the filamentous cyanobacterium Anabaena sp. 7119. J Biol Chem, 260, 9567–9573.

    PubMed  CAS  Google Scholar 

  • Goodman, N.S. and Schiff, J.A. (1964) Studies of sulfate utilization by algae. 3. Products formed from sulfate by euglena. J Protozool, 11, 120–127.

    PubMed  CAS  Google Scholar 

  • Gounaris, K., Whitford, D. and Barber, J. (1985) Isolation and characterization of a photosystem II reaction center lipoprotein complex. FEBS Lett, 188, 68–72.

    Article  CAS  Google Scholar 

  • Green, L.S. and Grossman, A.R. (1988) Changes in sulfate transport characteristics and protein composition of Anacystis nidulans R2 during sulfur deprivation. J Bacteriol, 170, 583–587.

    PubMed  CAS  Google Scholar 

  • Green, L.S., Laudenbach, D.E. and Grossman, A.R. (1989) A region of a cyanobacterial genome required for sulfate transport. Proc Natl Acad Sci U S A, 86, 1949–1953.

    Article  PubMed  CAS  Google Scholar 

  • Grillo, J.F. and Gibson, J. (1979) Regulation of phosphate accumulation in the unicellular cyanobacterium Synechococcus. J Bacteriol, 140, 508–517.

    PubMed  CAS  Google Scholar 

  • Groene, T. (1995) Biogenic production and consumption of dimethylsulfide (DMS) and dimethylsulfoniopropionate (DMSP) in the marine epipelagic zone: a review. J Marine Systems, 6, 191–209.

    Article  Google Scholar 

  • Gromer, S., Johansson, L., Bauer, H., Arscott, L.D., Rauch, S., Ballou, D.P., Williams, C.H., Jr., Schirmer, R.H. and Arner, E.S. (2003) Active sites of thioredoxin reductases: why selenoproteins? Proc Natl Acad Sci U S A, 100, 12618–12623.

    Article  PubMed  CAS  Google Scholar 

  • Gröne, T. and Kirst, G.O (1992) The effect of nitrogen deficiency, methionine and inhibitors of methionine metabolism on the DMSP contents of Tetraselmis subcordiformis (Stein).. Mar Biol, 112, 497–503.

    Article  Google Scholar 

  • Grossman, A. and Takahashi, H. (2001) Macronutrient utilization by photosynthetic eukaryotes and the fabric of interactions. Annu Rev Plant Physiol Plant Mol Biol, 52, 163–210.

    Article  PubMed  CAS  Google Scholar 

  • Grossman, A.R. (2005) Paths toward algal genomics. Plant Physiol, 137, 410–427.

    Article  PubMed  CAS  Google Scholar 

  • Grossman, A.R., Harris, E.E., Hauser, C., Lefebvre, P.A., Martinez, D., Rokhsar, D., Shrager, J., Silflow, C.D., Stern, D., Vallon, O. and Zhang, Z. (2003) Chlamydomonas reinhardtii at the crossroads of genomics. Eukaryot Cell, 2, 1137–1150.

    Article  PubMed  CAS  Google Scholar 

  • Guler, S., Seeliger, A., Hartel, H., Renger, G. and Benning, C. (1996) A null mutant of Synechococcus sp. PCC7942 deficient in the sulfolipid sulfoquinovosyl diacylglycerol. J Biol Chem, 271, 7501–7507.

    Article  PubMed  CAS  Google Scholar 

  • Gutman, B.L. and Niyogi, K.K. (2004) Chlamydomonas and Arabidopsis. A dynamic duo. Plant Physiol, 135, 607–610.

    Article  PubMed  CAS  Google Scholar 

  • Habicht, K.S., Gade, M., Thamdrup, B., Berg, P. and Canfield, D.E. (2002) Calibration of sulfate levels in the archean ocean. Science, 298, 2372–2374.

    Article  PubMed  CAS  Google Scholar 

  • Hamilton, B.S., Nakamura, K. and Roncari, D.A. (1992) Accumulation of starch in Chlamydomonas reinhardtii flagellar mutants. Biochem Cell Biol, 70, 255–258.

    Article  PubMed  CAS  Google Scholar 

  • Harada, E., von Roepenack-Lahaye, E. and Clemens, S. (2004) A cyanobacterial protein with similarity to phytochelatin synthases catalyzes the conversion of glutathione to gamma-glutamylcysteine and lacks phytochelatin synthase activity. Phytochemistry, 65, 3179–3185.

    Article  PubMed  CAS  Google Scholar 

  • Harold, F.M. and Sylvan, S. (1963) Accumulation of inorganic polyphosphate in Aerobacter aerogenes II. Environmental control and the role of sulfur compounds. J Bacteriol, 86, 222–231.

    PubMed  CAS  Google Scholar 

  • Harrison, A., Sakato, M., Tedford, H.W., Benashski, S.E., Patel-King, R.S. and King, S.M. (2002) Redox-based control of the gamma heavy chain ATPase from Chlamydomonas outer arm dynein. Cell Motil Cytoskeleton, 52, 131–143.

    Article  PubMed  CAS  Google Scholar 

  • Harwood, J.L. and Nicholls, R.G. (1979) The plant sulpholipid–a major component of the sulphur cycle. Biochem Soc Trans, 7, 440–447.

    PubMed  CAS  Google Scholar 

  • Hetland, G. (2003) Anti-infective action of immuno-modulating polysaccharides (-glucan and Plantago Major L. Pectin) against intracellular (Mycobacteria sp.) and extracellular (Streptococcus Pneumoniae sp.) respiratory pathogens. Current Med Chem–Anti-Infective Agents, 2, 135–146.

    Article  CAS  Google Scholar 

  • Hirata, K., Tsujimoto, Y., Namba, T., Ohta, T., Hirayanagi, N., Miyasaka, H., Zenk, M.H. and Miyamoto, K. (2001) Strong induction of phytochelatin synthesis by zinc in marine green alga, Dunaliella tertiolecta. J Biosci Bioeng, 92, 24–29.

    Article  PubMed  CAS  Google Scholar 

  • Hodson, R.C. and Schiff, J.A. (1971a) Studies of sulfate utilization by algae: 8. The ubiquity of sulfate reduction to thiosulfate. Plant Physiol, 47, 296–299.

    Article  PubMed  CAS  Google Scholar 

  • Hodson, R.C. and Schiff, J.A. (1971b) Studies of sulfate utilization by algae: 9. Fractionation of a cell-free system from Chlorella into two activities necessary for the reduction of adenosine 3′-phosphate 5′-phosphosulfate to acid-volatile radioactivity. Plant Physiol, 47, 300–305.

    Article  PubMed  CAS  Google Scholar 

  • Hodson, R.C., Schiff, J.A. and Mather, J.P. (1971) Studies of sulfate utilization by algae: 10. Nutritional and enzymatic characterization of Chlorella mutants impaired for sulfate utilization. Plant Physiol, 47, 306–311.

    Article  PubMed  CAS  Google Scholar 

  • Howe, G. and Merchant, S. (1992) Heavy metal-activated synthesis of peptides in Chlamydomonas reinhardtii. Plant Physiol, 98, 127–136.

    Article  PubMed  CAS  Google Scholar 

  • Hu, S., Lau, K.W.K. and Wu, M. (2001) Cadmium sequestration in Chlamydomonas reinhardtii. Plant Sci, 161, 987–996.

    Article  CAS  Google Scholar 

  • Huleihel, M., Ishanu, V., Tal, J. and Arad, S. (2002) Activity of Porphyridium sp. against herpes simplex viruses in vitro and in vivo. J Biochem Biophys Methods, 50, 189–200.

    Article  Google Scholar 

  • Huppe, H.C., de Lamotte-Guery, F., Jacquot, J.P. and Buchanan, B.B. (1990) The ferredoxin-thioredoxin system of a green alga, Chlamydomonas reinhardtii: identification and characterization of thioredoxins and ferredoxin-thioredoxin reductase components. Planta, 180, 341–351.

    Article  PubMed  CAS  Google Scholar 

  • Huppe, H.C., Picaud, A., Buchanan, B.B. and Miginiac-Maslow, M. (1991) Identification of an NADP/thioredoxin system in Chlamydomonas reinhardtii. Planta, 186, 115–121.

    Article  PubMed  CAS  Google Scholar 

  • Irihimovitch, V. and Shapira, M. (2000) Glutathione redox potential modulated by reactive oxygen species regulates translation of Rubisco large subunit in the chloroplast. J Biol Chem, 275, 16289–16295.

    Article  PubMed  CAS  Google Scholar 

  • Irihimovitch, V. and Stern, D.B. (2006) The sulfur acclimation SAC3 kinase is required for chloroplast transcriptional repression under sulfur limitation in Chlamydomonas reinhardtii. Proc Natl Acad Sci U S A, 103, 7911–7916.

    Article  PubMed  CAS  Google Scholar 

  • Ito, H., Iwabuchi, M. and Ogawa, K. (2003) The sugar-metabolic enzymes aldolase and triose-phosphate isomerase are targets of glutathionylation in Arabidopsis thaliana: detection using biotinylated glutathione. Plant Cell Physiol, 44, 655–660.

    Article  PubMed  CAS  Google Scholar 

  • James, F., Paquet, L., Sparace, S.A., Gage, D.A. and Hanson, A.D. (1995) Evidence implicating dimethylsulfoniopropionaldehyde as an intermediate in dimethylsulfoniopropionate biosynthesis. Plant Physiol, 108, 1439–1448.

    Article  PubMed  CAS  Google Scholar 

  • Jeanjean, R. and Broda, E. (1977) Dependence of sulphate uptake by Anacystis nidulans on energy, on osmotic shock and on sulphate stravation. Arch Microbiol, 114, 19–23.

    Article  PubMed  CAS  Google Scholar 

  • Jensen, T.E. and Rachlin, J.W. (1984) Effect of varying sulphur deficiency on structural components of a cyanobacterium Synechococcus leopoliiensis: a morphometric study. Cytobios, 41, 35–46.

    CAS  Google Scholar 

  • Jez, J.M., Cahoon, R.E. and Chen, S. (2004) Arabidopsis thaliana glutamate-cysteine ligase: functional properties, kinetic mechanism, and regulation of activity. J Biol Chem, 279, 33463–33470.

    Article  PubMed  CAS  Google Scholar 

  • Jo, J.H., Lee, D.S. and Park, J.M. (2006) Modeling and optimization of photosynthetic hydrogen gas production by green alga Chlamydomonas reinhardtii in sulfur-deprived circumstance. Biotechnol Prog, 22, 431–437.

    Article  PubMed  CAS  Google Scholar 

  • Jordan, P.A. and Gibbins, J.M. (2006) Extracellular disulfide exchange and the regulation of cellular function. Antioxid Redox Signal, 8, 312–324.

    Article  PubMed  CAS  Google Scholar 

  • Kanno, N., Nagahisa, E., Sato, M. and Sato, Y. (1996) Adenosine 5-prime-phosphosulfate sulfotransferase from the marine macroalga Porphyra yezoensis Ueda (Rhodophyta): stabilization, purification, and properties. Planta, 198, 440–446.

    Article  CAS  Google Scholar 

  • Kaplan, D., Heimer, Y.M., Abeliovich, A. and Goldbrough, P.B. (1995) Cadmium toxicity and resistance in Chlorella sp. Plant Sci, 109, 129–137.

    Article  CAS  Google Scholar 

  • Karsten, U., Wiencke, C. and G.O., K. (1992) Dimethylsulphoniopropionate (DMSP) accumulation in green macroalgae from polar to temperate regions: interactive effects of light versus salinity and light versus temperature. Pol Biol, 12, 603–607.

    Article  Google Scholar 

  • Karsten, U., Wiencke, C. and Kirst, G.O. (1990) The effect of light intensity and daylength on the β-dimethylsulphoniopropionate (DMSP) content of marine green macroalgae from Antarctica. Plant Cell Environ, 12, 989–993.

    Article  Google Scholar 

  • Kathir, P., LaVoie, M., Brazelton, W.J., Haas, N.A., Lefebvre, P.A. and Silflow, C.D. (2003) Molecular map of the Chlamydomonas reinhardtii nuclear genome. Eukaryot Cell, 2, 362–379.

    Article  PubMed  CAS  Google Scholar 

  • Kawaguchi, H., Hashimoto, K., Hirata, K. and Miyamoto, K. (2001) H2 production from algal biomass by a mixed culture of Rhodobium marinum A-501 and Lactobacillus amylovorus. J Biosci Bioeng, 91, 277–282.

    Article  PubMed  CAS  Google Scholar 

  • Keller, M.D., Kiene, R.P., Matrai, P.A. and Bellows, W.K. (1999) Production of glycine betaine and dimethylsulfoniopropionate in marine phytoplankton. II. N-limited chemostat cultures. Mar Biol, 135, 249–257.

    Article  CAS  Google Scholar 

  • Kieber, D.J., Jiao, J., Kiene, R.P. and Bates, T.S. (1996) Impact of dimethylsulfide photochemistry on methyl sulfur cycling in the equatorial Pacific ocean. J Geophys Res, 101, 3715–3722.

    Article  CAS  Google Scholar 

  • Kim, J. and Mayfield, S.P. (1997) Protein disulfide isomerase as a regulator of chloroplast translational activation. Science, 278, 1954–1957.

    Article  PubMed  CAS  Google Scholar 

  • Kim, J. and Mayfield, S.P. (2002) The active site of the thioredoxin-like domain of chloroplast protein disulfide isomerase, RB60, catalyzes the redox-regulated binding of chloroplast poly(A)-binding protein, RB47, to the 5′ untranslated region of psbA mRNA. Plant Cell Physiol, 43, 1238–1243.

    Article  PubMed  CAS  Google Scholar 

  • Kirst, G., Thiel, C., Wolff, H., Nothnagel, J., Wanzek, M. and Ulmke, R. (1991) Dimethylsulfoniopropionate (DMSP) in ice-algae and its possible biological role. Mar Chem, 35, 381–388.

    Article  CAS  Google Scholar 

  • Klein, U. (1987) Intracellular carbon partitioning in Chlamydomonas reinhardtii. Plant Physiol, 85, 892–897.

    Article  PubMed  CAS  Google Scholar 

  • Kloareg, B. and Quatrano, R.S. (1988) Structure of the cell walls of marine algae and ecophysiological functions of the matrix polysaccharides. Oceanogr Mar Biol Annu Res, 26, 259–315.

    Google Scholar 

  • Kobayashi, I., Fujiwara, S., Saegusa, H., Inouhe, M., Matsumoto, H. and Tsuzuki, M. (2006) Relief of arsenate toxicity by Cd-stimulated phytochelatin synthesis in the green alga Chlamydomonas reinhardtii. Mar Biotechnol (NY), 8, 94–101.

    Article  CAS  Google Scholar 

  • Kocsis, M.G., Nolte, K.D., Rhodes, D., Shen, T.L., Gage, D.A. and Hanson, A.D. (1998) Dimethylsulfoniopropionate biosynthesis in Spartina alterniflora1. Evidence that S-methylmethionine and dimethylsulfoniopropylamine are intermediates. Plant Physiol, 117, 273–281.

    Article  PubMed  CAS  Google Scholar 

  • Kopriva, S., Buchert, T., Fritz, G., Suter, M., Benda, R., Schunemann, V., Koprivova, A., Schurmann, P., Trautwein, A.X., Kroneck, P.M. and Brunold, C. (2002) The presence of an iron-sulfur cluster in adenosine 5′-phosphosulfate reductase separates organisms utilizing adenosine 5′-phosphosulfate and phosphoadenosine 5′-phosphosulfate for sulfate assimilation. J Biol Chem, 277, 21786–21791.

    Article  PubMed  CAS  Google Scholar 

  • Kopriva, S., Buchert, T., Fritz, G., Suter, M., Weber, M., Benda, R., Schaller, J., Feller, U., Schurmann, P., Schunemann, V., Trautwein, A.X., Kroneck, P.M. and Brunold, C. (2001) Plant adenosine 5′-phosphosulfate reductase is a novel iron-sulfur protein. J Biol Chem, 276, 42881–42886.

    Article  PubMed  CAS  Google Scholar 

  • Kopriva, S. and Koprivova, A. (2004) Plant adenosine 5′-phosphosulphate reductase: the past, the present, and the future. J Exp Bot, 55, 1775–1783.

    Article  PubMed  CAS  Google Scholar 

  • Kruse, O., Hankamer, B., Konczak, C., Gerle, C., Morris, E., Radunz, A., Schmid, G.H. and Barber, J. (2000) Phosphatidylglycerol is involved in the dimerization of photosystem II. J Biol Chem, 275, 6509–6514.

    Article  PubMed  CAS  Google Scholar 

  • Kugita, M., Kaneko, A., Yamamoto, Y., Takeya, Y., Matsumoto, T. and Yoshinaga, K. (2003) The complete nucleotide sequence of the hornwort (Anthoceros formosae) chloroplast genome: insight into the earliest land plants. Nucleic Acids Res, 31, 716–721.

    Article  PubMed  CAS  Google Scholar 

  • Kurvari, V., Qian, F. and Snell, W.J. (1995) Increased transcript levels of a methionine synthase during adhesion-induced activation of Chlamydomonas reinhardtii gametes. Plant Mol Biol, 29, 1235–1252.

    Article  PubMed  CAS  Google Scholar 

  • Lauchli, A. (1993) Selenium in plants: Uptake, functions, and environmental toxicity. Bot Acta, 106, 455–468.

    CAS  Google Scholar 

  • Laudenbach, D.E. and Grossman, A.R. (1991) Characterization and mutagenesis of sulfur-regulated genes in a cyanobacterium: evidence for function in sulfate transport. J Bacteriol, 173, 2739–2750.

    PubMed  CAS  Google Scholar 

  • Lawry, N.H. and Jensen, T.E. (1979) Deposition of condensed phosphate as an effect of varying sulfur deficiency in the cyanobacterium Synechococcus sp. (Anacystis nidulans). Arch Microbiol, 120, 1–7.

    Article  CAS  Google Scholar 

  • Lawry, N.H. and Simon, R.D. (1982) The normal and induced occurrence of cyanophycin inclusion bodies in several blue-green algae. J Phycol, 18, 391–399.

    Article  CAS  Google Scholar 

  • Le Faucheur, S., Behra, R. and Sigg, L. (2005) Phytochelatin induction, cadmium accumulation, and algal sensitivity to free cadmium ion in Scenedesmus vacuolatus. Environ Toxicol Chem, 24, 1731–1737.

    Article  PubMed  CAS  Google Scholar 

  • Ledford, H.K., Baroli, I., Shin, J.W., Fischer, B.B., Eggen, R.I. and Niyogi, K.K. (2004) Comparative profiling of lipid-soluble antioxidants and transcripts reveals two phases of photo-oxidative stress in a xanthophyll- deficient mutant of Chlamydomonas reinhardtii. Mol Genet Genomics, 272, 470–479.

    Article  PubMed  CAS  Google Scholar 

  • LeDuc, D.L., Tarun, A.S., Montes-Bayon, M., Meija, J., Malit, M.F., Wu, C.P., AbdelSamie, M., Chiang, C.Y., Tagmount, A., deSouza, M., Neuhierl, B., Bock, A., Caruso, J. and Terry, N. (2004) Overexpression of selenocysteine methyltransferase in Arabidopsis and Indian mustard increases selenium tolerance and accumulation. Plant Physiol, 135, 377–383.

    Article  PubMed  CAS  Google Scholar 

  • Lee, S. and Leustek, T. (1998) APS kinase from Arabidopsis thaliana: genomic organization, expression, and kinetic analysis of the recombinant enzyme. Biochem Biophys Res Commun, 247, 171–175.

    Article  PubMed  CAS  Google Scholar 

  • Lefebvre, P.A. and Silflow, C.D. (1999) Chlamydomonas: the cell and its genomes. Genetics, 151, 9–14.

    PubMed  CAS  Google Scholar 

  • Leisinger, U., Rufenacht, K., Fischer, B., Pesaro, M., Spengler, A., Zehnder, A.J. and Eggen, R.I. (2001) The glutathione peroxidase homologous gene from Chlamydomonas reinhardtii is transcriptionally up-regulated by singlet oxygen. Plant Mol Biol, 46, 395–408.

    Article  PubMed  CAS  Google Scholar 

  • Lemaire, S., Keryer, E., Stein, M., Schepens, I.I., Issakidis-Bourguet, E., Gerard Hirni, C., Miginiac-Maslow, M. and Jacquot, J.P. (1999a) Heavy-metal regulation of thioredoxin gene expression in Chlamydomonas reinhardtii. Plant Physiol, 120, 773–778.

    Article  PubMed  CAS  Google Scholar 

  • Lemaire, S.D. (2004) The glutaredoxin family in oxygenic photosynthetic organisms. Photosynth Res, 79, 305–318.

    Article  PubMed  CAS  Google Scholar 

  • Lemaire, S.D., Guillon, B., Le Marechal, P., Keryer, E., Miginiac-Maslow, M. and Decottignies, P. (2004) New thioredoxin targets in the unicellular photosynthetic eukaryote Chlamydomonas reinhardtii. Proc Natl Acad Sci U S A, 101, 7475–7480.

    Article  PubMed  CAS  Google Scholar 

  • Lemaire, S.D. and Miginiac-Maslow, M. (2004) The thioredoxin superfamily in Chlamydomonas reinhardtii. Photosynth Res, 82, 203–220.

    Article  PubMed  CAS  Google Scholar 

  • Lemaire, S.D., Quesada, A., Merchan, F., Corral, J.M., Igeno, M.I., Keryer, E., Issakidis-Bourguet, E., Hirasawa, M., Knaff, D.B. and Miginiac-Maslow, M. (2005) NADP-malate dehydrogenase from unicellular green alga Chlamydomonas reinhardtii. A first step toward redox regulation? Plant Physiol, 137, 514–521.

    Article  PubMed  CAS  Google Scholar 

  • Lemaire, S.D., Stein, M., Issakidis-Bourguet, E., Keryer, E., Benoit, V.V., Pineau, B., Gerard-Hirne, C., Miginiac-Maslow, M. and Jacquot, J.P. (1999b) The complex regulation of ferredoxin/thioredoxin-related genes by light and the circadian clock. Planta, 209, 221–229.

    Article  PubMed  CAS  Google Scholar 

  • Lemieux, C., Otis, C. and Turmel, M. (2000) Ancestral chloroplast genome in Mesostigma viride reveals an early branch of green plant evolution. Nature, 403, 649–652.

    Article  PubMed  CAS  Google Scholar 

  • Levitan, A., Trebitsh, T., Kiss, V., Pereg, Y., Dangoor, I. and Danon, A. (2005) Dual targeting of the protein disulfide isomerase RB60 to the chloroplast and the endoplasmic reticulum. Proc Natl Acad Sci U S A, 102, 6225–6230.

    Article  PubMed  CAS  Google Scholar 

  • Li, J.J., Saidha, T. and Schiff, J.A. (1991) Purification and properties of two forms of ATP sulfurylase from Euglena. Biochim Biophys Acta, 1078, 68–76.

    PubMed  CAS  Google Scholar 

  • Li, J.Y. and Schiff, J.A. (1991) Purification and properties of adenosine 5′-phosphosulphate sulphotransferase from Euglena. Biochem J, 274 (Pt 2), 355–360.

    PubMed  CAS  Google Scholar 

  • Libessart, N., Maddelein, M.L., Koornhuyse, N., Decq, A., Delrue, B., Mouille, G., D’Hulst, C. and Ball, S. (1995) Storage, photosynthesis, and growth: The conditional nature of mutations affecting starch synthesis and structure in Chlamydomonas. Plant Cell, 7, 1117–1127.

    Article  PubMed  CAS  Google Scholar 

  • Lien, T. and Schreiner, Ø. (1975) Purification of a derepressible arylsulfatase from Chlamydomonas reinhardtii. Properties of the enzyme in intact cells and in purified state. Biochim Biophys Acta, 384, 168–179.

    PubMed  CAS  Google Scholar 

  • Lindahl, M. and Florencio, F.J. (2003) Thioredoxin-linked processes in cyanobacteria are as numerous as in chloroplasts, but targets are different. Proc Natl Acad Sci U S A, 100, 16107–16112.

    Article  PubMed  CAS  Google Scholar 

  • Loewus, F., Wagner, G., Schiff, J.A. and Weistrop, J. (1971) The incorporation of 35S-labeled sulfate into carrageenan in Chondrus crispus. Plant Physiol, 48, 373–375.

    Article  PubMed  CAS  Google Scholar 

  • Loll, B., Kern, J., Saenger, W., Zouni, A. and Biesiadka, J. (2005) Towards complete cofactor arrangement in the 3.0 A resolution structure of photosystem II. Nature, 438, 1040–1044.

    Article  PubMed  CAS  Google Scholar 

  • Lomans, B.P., van der Drift, C., Pol, A. and Op den Camp, H.J. (2002) Microbial cycling of volatile organic sulfur compounds. Cell Mol Life Sci, 59, 575–588.

    Article  PubMed  CAS  Google Scholar 

  • Lovelock, J.E. (1972) Gaia as seen through the atmosphere. Atmos Environ, 6, 579–580.

    Article  Google Scholar 

  • Lyi, S.M., Heller, L.I., Rutzke, M., Welch, R.M., Kochian, L.V. and Li, L. (2005) Molecular and biochemical characterization of the selenocysteine Se-methyltransferase gene and Se-methylselenocysteine synthesis in broccoli. Plant Physiol, 138, 409–420.

    Article  PubMed  CAS  Google Scholar 

  • Malea, P., Rijstenbil, J.W. and Haritonidis, S. (2006) Effects of cadmium, zinc and nitrogen status on nonprotein thiols in the macroalgae Enteromorpha spp. from the Scheldt Estuary (SW Netherlands, Belgium) and Thermaikos Gulf (Greece, N Aegean Sea). Marine Environ Res, 62, 45–60.

    Article  CAS  Google Scholar 

  • Malin, G. and Kirst, G.O. (1997) Algal production of dimethyl sulfide and its atmospheric role. J Phycol, 33, 889–896.

    Article  CAS  Google Scholar 

  • Marrs, K.A. (1996) The functions and regulation of glutathione S-transferase in plants. Annu Rev Plant Physiol Plant Mol Biol, 47, 127–158.

    Article  PubMed  CAS  Google Scholar 

  • Maruyama-Nakashita, A., Inoue, E., Watanabe-Takahashi, A., Yamaya, T. and Takahashi, H. (2003) Transcriptome profiling of sulfur-responsive genes in Arabidopsis reveals global effects of sulfur nutrition on multiple metabolic pathways. Plant Physiol, 132, 597–605.

    Article  PubMed  CAS  Google Scholar 

  • Maruyama-Nakashita, A., Nakamura, Y., Yamaya, T. and Takahashi, H. (2004) Regulation of high-affinity sulphate transporters in plants: towards systematic analysis of sulphur signalling and regulation. J Exp Bot, 55, 1843–1849.

    Article  PubMed  CAS  Google Scholar 

  • Matagne, R.F., Loppes, R. and Deltour, R. (1976) Phosphatase of Chlamydomonas reinhardi: biochemical and cytochemical approach with specific mutants. J Bacteriol, 126, 937–950.

    PubMed  CAS  Google Scholar 

  • Matrai, P.A. and Keller, M.D. (1994) Total organic sulfur and dimethylsulfoniopropionate (DMSP) in marine phytoplankton: Intracellular variation. Mar Biol, 119, 61–68.

    Article  CAS  Google Scholar 

  • Matsuzaki, M., Misumi, O., Shin, I.T., Maruyama, S., Takahara, M., Miyagishima, S.Y., Mori, T., Nishida, K., Yagisawa, F., Nishida, K., Yoshida, Y., Nishimura, Y., Nakao, S., Kobayashi, T., Momoyama, Y., Higashiyama, T., Minoda, A., Sano, M., Nomoto, H., Oishi, K., Hayashi, H., Ohta, F., Nishizaka, S., Haga, S., Miura, S., Morishita, T., Kabeya, Y., Terasawa, K., Suzuki, Y., Ishii, Y., Asakawa, S., Takano, H., Ohta, N., Kuroiwa, H., Tanaka, K., Shimizu, N., Sugano, S., Sato, N., Nozaki, H., Ogasawara, N., Kohara, Y. and Kuroiwa, T. (2004) Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D. Nature, 428, 653–657.

    Article  PubMed  CAS  Google Scholar 

  • Melis, A. and Chen, H.C. (2005) Chloroplast sulfate transport in green algae – genes, proteins and effects. Photosynth Res, 86, 299–307.

    Article  PubMed  CAS  Google Scholar 

  • Melis, A. and Happe, T. (2001) Hydrogen production. Green algae as a source of energy. Plant Physiol, 127, 740–748.

    Article  PubMed  CAS  Google Scholar 

  • Melis, A. and Happe, T. (2004) Trails of green alga hydrogen research – from hans gaffron to new frontiers. Photosynth Res, 80, 401–409.

    Article  PubMed  CAS  Google Scholar 

  • Melis, A., Seibert, M. and Happe, T. (2004) Genomics of green algal hydrogen research. Photosynth Res, 82, 277–288.

    Article  PubMed  CAS  Google Scholar 

  • Meyer, A.J. and Hell, R. (2005) Glutathione homeostasis and redox regulation of sulfhydryl groups. Photosyn Res, 86, 435–457.

    Article  PubMed  CAS  Google Scholar 

  • Michelet, L., Zaffagnini, M., Marchand, C., Collin, V., Decottignies, P., Tsan, P., Lancelin, J.M., Trost, P., Miginiac-Maslow, M., Noctor, G. and Lemaire, S.D. (2005) Glutathionylation of chloroplast thioredoxin f is a redox signaling mechanism in plants. Proc Natl Acad Sci U S A, 102, 16478–16483.

    Article  PubMed  CAS  Google Scholar 

  • Morelli, E., Cruz, B.H., Somovigo, S. and Scarano, G. (2002) Speciation of cadmium-glutamyl peptides complexes in cells of the marine microagla Phaeodactylum tricornutum. Plant Sci, 163, 807–813.

    Article  CAS  Google Scholar 

  • Morelli, E. and Scarano, G. (2001) Synthesis and stability of phytochelatins induced by cadmium and lead in the marine diatom Phaeodactylum tricornutum. Marine Environ Res, 52, 383–395.

    Article  CAS  Google Scholar 

  • Moseley, J.L., Chang, C.W. and Grossman, A.R. (2006) Genome-based approaches to understanding phosphorus deprivation responses and PSR1 control in Chlamydomonas reinhardtii. Eukaryot Cell, 5, 26–44.

    Article  PubMed  CAS  Google Scholar 

  • Munavalli, S., Parker, D.V. and Hamilton, F.D. (1975) Identification of NADPH-thioredoxin reductase system in Euglena gracillis. Proc Natl Acad Sci U S A, 72, 4233–4237.

    Article  PubMed  CAS  Google Scholar 

  • Murata, N., Higashi, S.I. and Fujimura, Y. (1990) Glycerolipids in. various preparations of photosystem II from spinach chloroplasts. Biochim Biophys Acta, 1019, 261–268.

    Article  CAS  Google Scholar 

  • Murata, N. and Sato, N. (1983) Analysis of lipids in Prochloron. sp.: occurrence of monoglucosyl diacylglycerol. Plant Cell Physiol, 24, 133–138.

    CAS  Google Scholar 

  • Nagel, K., Adelmeier, U. and Voigt, J. (1996) Subcellular distribution of. cadmium in the unicellular green alga Chlamydomonas reinhardtii. J Plant Physiol, 149, 86–90.

    CAS  Google Scholar 

  • Nagel, K. and Voigt, J. (1995) Impaired photosynthesis in a cadmium-tolerant Chlamydomonas mutant strain. Microbiol Res, 150, 105–110.

    CAS  Google Scholar 

  • Navarro, F. and Florencio, F.J. (1996) The cyanobacterial thioredoxin gene is required for both photoautotrophic and heterotrophic growth. Plant Physiol, 111, 1067–1075.

    Article  PubMed  CAS  Google Scholar 

  • Nicholson, M.L., Gaasenbeek, M. and Laudenbach, D.E. (1995) Two enzymes together capable of cysteine biosynthesis are encoded on a cyanobacterial plasmid. Mol Gen Genet, 247, 623–632.

    Article  PubMed  CAS  Google Scholar 

  • Nicholson, M.L. and Laudenbach, D.E. (1995) Genes encoded on a cyanobacterial plasmid are transcriptionally regulated by sulfur availability and CysR. J Bacteriol, 177, 2143–2150.

    PubMed  CAS  Google Scholar 

  • Nishiguchi, M.K. and Somero, G.N. (1992) Temperature- and concentration-dependence of compatibility of the organic osmolyte beta-dimethylsulfoniopropionate. Cryobiology, 29, 118–124.

    Article  PubMed  CAS  Google Scholar 

  • Nishikawa, K., Onodera, A. and Tominaga, N. (2006) Phytochelatins do not correlate with the level of Cd accumulation in Chlamydomonas spp. Chemosphere, 63, 1553–1559.

    Article  PubMed  CAS  Google Scholar 

  • Noctor, G. and Foyer, C.H. (1998) Ascorbate and Glutathione: Keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol, 49, 249–279.

    Article  PubMed  CAS  Google Scholar 

  • Novoselov, S.V., Rao, M., Onoshko, N.V., Zhi, H., Kryukov, G.V., Xiang, Y., Weeks, D.P., Hatfield, D.L. and Gladyshev, V.N. (2002) Selenoproteins and selenocysteine insertion system in the model plant cell system, Chlamydomonas reinhardtii. Embo J, 21, 3681–3693.

    Article  PubMed  CAS  Google Scholar 

  • Ohta, N., Matsuzaki, M., Misumi, O., Miyagishima, S.Y., Nozaki, H., Tanaka, K., Shin, I.T., Kohara, Y. and Kuroiwa, T. (2003) Complete sequence and analysis of the plastid genome of the unicellular red alga Cyanidioschyzon merolae. DNA Res, 10, 67–77.

    Article  PubMed  CAS  Google Scholar 

  • Ohyama, K., Fukuzawa, H., Kohchi, T., Sano, T., Sano, S., Shirai, H., Umesono, K., Shiki, Y., Takeuchi, M., Chang, Z. and et al. (1988) Structure and organization of Marchantia polymorpha chloroplast genome. I. Cloning and gene identification. J Mol Biol, 203, 281–298.

    Article  PubMed  CAS  Google Scholar 

  • Omata, T. and Murata, N. (1983) Isolation and characterization of the cytoplasmic membranes from the blue-green. alga (cyanobacterium) Anacystis nidulans. Plant Cell Physiol, 24, 1101–1112.

    CAS  Google Scholar 

  • Perez-Rama, M., Torres Vaamonde, E. and Abalde Alonso, J. (2006) Composition and production of thiol constituents induced by cadmium in the marine microalga Tetraselmis suecica. Environ Toxicol Chem, 25, 128–136.

    Article  PubMed  CAS  Google Scholar 

  • Plumley, F.G. and Schmidt, G.W. (1989) Nitrogen-dependent regulation of photosynthetic gene expression. Proc Natl Acad Sci U S A, 86, 2678–2682.

    Article  PubMed  CAS  Google Scholar 

  • Pollock, S.V., Pootakham, W., Shibagaki, N., Moseley, J.L. and Grossman, A.R. (2005) Insights into the acclimation of Chlamydomonas reinhardtii to sulfur deprivation. Photosynth Res, 86, 475–489.

    Article  PubMed  CAS  Google Scholar 

  • Posewitz, M.C., King, P.W., Smolinski, S.L., Zhang, L., Seibert, M. and Ghirardi, M.L. (2004a) Discovery of two novel radical S-adenosylmethionine proteins required for the assembly of an active [Fe] hydrogenase. J Biol Chem, 279, 25711–25720.

    Article  PubMed  CAS  Google Scholar 

  • Posewitz, M.C., Smolinski, S.L., Kanakagiri, S., Melis, A., Seibert, M. and Ghirardi, M.L. (2004b) Hydrogen photoproduction is attenuated by disruption of an isoamylase gene in Chlamydomonas reinhardtii. Plant Cell, 16, 2151–2163.

    Article  PubMed  CAS  Google Scholar 

  • Quisel, J.D., Wykoff, D.D. and Grossman, A.R. (1996) Biochemical characterization of the extracellular phosphatases produced by phosphorus-deprived Chlamydomonas reinhardtii. Plant Physiol, 111, 839–848.

    Article  PubMed  CAS  Google Scholar 

  • Ramus, J. (1974) In vivo molybdate inhibition of sulfate transfer to porphyridium capsular polysaccharide. Plant Physiol, 54, 945–949.

    Article  PubMed  CAS  Google Scholar 

  • Ramus, J. and Groves, S.T. (1972) Incorporation of sulfate into the capsular polysaccharide of the red alga Porphyridium. J Cell Biol, 54, 399–407.

    Article  PubMed  CAS  Google Scholar 

  • Ravina, C.G., Barroso, C., Vega, J.M. and Gotor, C. (1999) Cysteine biosynthesis in Chlamydomonas reinhardtii. Molecular cloning and regulation of O-acetylserine (thiol) lyase. Eur J Biochem, 264, 848–853.

    Article  PubMed  CAS  Google Scholar 

  • Ravina, C.G., Chang, C.I., Tsakraklides, G.P., McDermott, J.P., Vega, J.M., Leustek, T., Gotor, C. and Davies, J.P. (2002) The sac mutants of Chlamydomonas reinhardtii reveal transcriptional and posttranscriptional control of cysteine biosynthesis. Plant Physiol, 130, 2076–2084.

    Article  PubMed  CAS  Google Scholar 

  • Rea, P.A., Vatamaniuk, O.K. and Rigden, D.J. (2004) Weeds, worms, and more. Papain’s long-lost cousin, phytochelatin synthase. Plant Physiol, 136, 2463–2474.

    Article  PubMed  CAS  Google Scholar 

  • Reed, R. (1983) Measurement and osmotic significance of β-dimethylsulfoniopropionate in marine microalgae. Mar Biol Lett, 34, 173–181.

    Google Scholar 

  • Riekhof, W.R., Ruckle, M.E., Lydic, T.A., Sears, B.B. and Benning, C. (2003) The sulfolipids 2′-O-acyl-sulfoquinovosyldiacylglycerol and sulfoquinovosyldiacylglycerol are absent from a Chlamydomonas reinhardtii mutant deleted in SQD1. Plant Physiol, 133, 864–874.

    Article  PubMed  CAS  Google Scholar 

  • Rijstenbil, J.W., Sandee, A., Van Drie, J. and Wijnholds, J.A. (1994) Interaction of toxic trace metals and mechanisms of detoxification in the planktonic diatoms Ditylum brightwellii and Thalassiosira pseudonana. FEMS Microbiol Rev, 14, 387–396.

    Article  PubMed  CAS  Google Scholar 

  • Romanyuk, N.D., Rigden, D.J., Vatamaniuk, O.K., Lang, A., Cahoon, R.E., Jez, J.M. and Rea, P.A. (2006) Mutagenic definition of a papain-like catalytic triad, sufficiency of the N-terminal domain for single-site core catalytic enzyme acylation, and C-terminal domain for augmentative metal activation of a eukaryotic phytochelatin synthase. Plant Physiol, 141, 858–869.

    Article  PubMed  CAS  Google Scholar 

  • Ruiz, F.A., Marchesini, N., Seufferheld, M., Govindjee and Docampo, R. (2001) The polyphosphate bodies of Chlamydomonas reinhardtii possess a proton-pumping pyrophosphatase and are similar to acidocalcisomes. J Biol Chem, 276, 46196–46203.

    Article  PubMed  CAS  Google Scholar 

  • Ryan, J., McKillen, M. and Mason, J. (1987) Sulphate/molybdate interactions: in vivo and in vitro studies on the group VI oxyanion transport system in ovine renal tubule epithelial cells. Ann Rech Vet, 18, 47–55.

    PubMed  CAS  Google Scholar 

  • Saito, K. (2000) Regulation of sulfate transport and synthesis of sulfur-containing amino acids. Curr Opin Plant Biol, 3, 188–195.

    PubMed  CAS  Google Scholar 

  • Sato, N. (2004) Roles of the acidic lipids sulfoquinovosyl diacylglycerol and phosphatidylglycerol in photosynthesis: their specificity and evolution. J Plant Res, 117, 495–505.

    Article  PubMed  CAS  Google Scholar 

  • Sato, N., Sonoike, K., Tsuzuki, M. and Kawaguchi, A. (1995) Impaired photosystem II in a mutant of Chlamydomonas reinhardtii defective in sulfoquinovosyl diacylglycerol. Eur J Biochem, 234, 16–23.

    Article  PubMed  CAS  Google Scholar 

  • Sato, N., Sugimoto, K., Meguro, A. and Tsuzuki, M. (2003) Identification of a gene for UDP-sulfoquinovose synthase of a green alga, Chlamydomonas reinhardtii, and its phylogeny. DNA Res, 10, 229–237.

    Article  PubMed  CAS  Google Scholar 

  • Schiff, J.A. (1959) Studies on sulfate utilization by Chlorella pyrenoidosa using sulfate-S; the occurrence of S-adenosyl methionine. Plant Physiol, 34, 73–80.

    Article  PubMed  CAS  Google Scholar 

  • Schiff, J.A. (1979) Pathways of assimilatory sulphate reduction in plants and microorganisms. Ciba Found Symp, 49–69.

    Google Scholar 

  • Schmidt, A. (1972) An APS-sulfotransferase from Chlorella. Arch Mikrobiol, 84, 77–86.

    Article  PubMed  CAS  Google Scholar 

  • Schmidt, A. (1973) Sulfate reduction in a cell-free system of Chlorella. The ferredoxin-dependent reduction of a protein-bound intermediate by a thiosulfonate reductase. Arch Microbiol, 93, 29–52.

    CAS  Google Scholar 

  • Schmidt, A. and Trüper, H. (1977) Reduction of adenylylsulfate and 3′-phosphoadenylylsulfate in phototrophic bacteria. Experientia, 33, 1008–1009.

    Article  PubMed  CAS  Google Scholar 

  • Schoeler, B., Delorme, N., Doench, I., Sukhorukov, G.B., Fery, A. and Glinel, K. (2006) Polyelectrolyte films based on polysaccharides of different conformations: effects on multilayer structure and mechanical properties. Biomacromolecules, 7, 2065–2071.

    Article  PubMed  CAS  Google Scholar 

  • Schreiner, Ø., Lien, T. and Knutsen, G. (1975) The capacity for arylsulfatase synthesis in synchronous and synchronized cultures of Chlamydomonas reinhardtii. Biochim Biophys Acta, 384, 180–193.

    PubMed  CAS  Google Scholar 

  • Schultze, M., Quiclet-Sire, B., Kondorosi, E., Virelizer, H., Glushka, J.N., Endre, G., Gero, S.D. and Kondorosi, A. (1992) Rhizobium meliloti produces a family of sulfated lipooligosaccharides exhibiting different degrees of plant host specificity. Proc Natl Acad Sci U S A, 89, 192–196.

    Article  PubMed  CAS  Google Scholar 

  • Selstam, E. and Campbell, D. (1996) Membrane lipid composition of the unusual cyanobacterium Gloeobacter violaceus sp. PCC 7421, which lacks sulfoquinovosyl. Arch Microbiol, 166, 132–135.

    Article  CAS  Google Scholar 

  • Shapira, M., Lers, A., Heifetz, P.B., Irihimovitz, V., Osmond, C.B., Gillham, N.W. and Boynton, J.E. (1997) Differential regulation of chloroplast gene expression in Chlamydomonas reinhardtii during photoacclimation: light stress transiently suppresses synthesis of the Rubisco LSU protein while enhancing synthesis of the PS II D1 protein. Plant Mol Biol, 33, 1001–1011.

    Article  PubMed  CAS  Google Scholar 

  • Shrager, J., Hauser, C., Chang, C.W., Harris, E.H., Davies, J., McDermott, J., Tamse, R., Zhang, Z. and Grossman, A.R. (2003) Chlamydomonas reinhardtii genome project. A guide to the generation and use of the cDNA information. Plant Physiol, 131, 401–408.

    Article  PubMed  Google Scholar 

  • Sieburth, J.M. (1960) Acrylic acid, an “antibiotic” principle in Phaeocystis blooms in antarctic waters. Science, 132, 676–677.

    Article  PubMed  CAS  Google Scholar 

  • Sigrist, M., Zwilliengerg, C., Giroud, C.H., Eichenberger, W. and Boschetti, A. (1988) Sulfolipid associated with the light-harvesting complex associated with photosystem II apoproteins of Chlamydomonas reinhardtii. Plant Sci, 58, 15–23.

    Article  CAS  Google Scholar 

  • Simo, R. and Pedros-Alio, C. (1999) Role of vertical mixing in controlling the oceanic production of dimethyl sulphide. Nature, 402, 396–399.

    Article  CAS  Google Scholar 

  • Siripornadulsil, S., Traina, S., Verma, D.P. and Sayre, R.T. (2002) Molecular mechanisms of proline-mediated tolerance to toxic heavy metals in transgenic microalgae. Plant Cell, 14, 2837–2847.

    Article  PubMed  CAS  Google Scholar 

  • Smith, I.W., Wilkinson, J.F. and Duguid, J.P. (1954) Volutin production in Aerobacter aerogenes due to nutrient imbalance. J Bacteriol, 68, 450–463.

    PubMed  CAS  Google Scholar 

  • Stauber, E.J. and Hippler, M. (2004) Chlamydomonas reinhardtii proteomics. Plant Physiol Biochem, 42, 989–1001.

    Article  PubMed  CAS  Google Scholar 

  • Stefels, J. (2000) Physiological aspects of the production and conversion of DMSP in marine algae and higher plants. J Sea Res, 43, 183–197.

    Article  CAS  Google Scholar 

  • Stefels, J. and van Boekel, W.H.M. (1993) Production of DMS from dissolved DMSP in axenic cultures of the marine phytoplankton species Phaeocystis sp. Mar Ecol Prog Ser, 97, 11–18.

    Article  CAS  Google Scholar 

  • Sugimoto, K., Sato, N., Watanabe, A. and Tsuzuki, M. (2005) Effects of sulfur deprivation on sulfolipid metabolism in Chlamydomonas reinhardtii. In Saito, K., De Kok, L.J., Stulen, I., Hawksford, M.J., Schnug, E. and Rennenberg, H. (eds.), Sulfur Transport and Assimilation in Plants in the Postgenomic Era. Backhuys Publishers, Leiden.

    Google Scholar 

  • Summers, P.S., Nolte, K.D., Cooper, A.J.L., Borgeas, H., Leustek, T., Rhodes, D. and Hanson, A.D. (1998) Identification and stereospecificity of the first three enzymes of 3-dimethylsulfoniopropionate biosynthesis in a chlorophyte alga. Plant Physiol, 116, 369–378.

    Article  CAS  Google Scholar 

  • Sunda, W., Kieber, D.J., Kiene, R.P. and Huntsman, S. (2002) An antioxidant function for DMSP and DMS in marine algae. Nature, 418, 317–320.

    Article  PubMed  CAS  Google Scholar 

  • Tabe, L. and Higgins, T.J.V. (1998) Engineering plant protein composition for improved nutrition. Trends in Plant Science, 3, 282–286.

    Article  Google Scholar 

  • Takahashi, H., Braby, C.E. and Grossman, A.R. (2001) Sulfur economy and cell wall biosynthesis during sulfur limitation of Chlamydomonas reinhardtii. Plant Physiol, 127, 665–673.

    Article  PubMed  CAS  Google Scholar 

  • Takahashi, H., Noji, M., Hirai, M.Y. and Saito, K. (2003) [Molecular regulation of assimilatory sulfur metabolism in plants]. Tanpakushitsu Kakusan Koso, 48, 2121–2129.

    PubMed  CAS  Google Scholar 

  • Takeda, T., Miyao, K., Tamoi, M., Kanaboshi, H., Miyasaka, H. and Shigeoka, S. (2003) Molecular characterization of glutathione peroxidase-like protein in halotolerant Chlamydomonas sp. W80. Physiol Plant, 117, 467–475.

    Article  PubMed  CAS  Google Scholar 

  • Torricelli, E., Gorbi, G., Pawlik-Skowronska, B., Sanità di Toppi, L. and Grazia Corradi, M. (2004) Cadmium tolerance, cysteine and thiol peptide levels in wild type and chromium-tolerant strains of Scenedesmus acutus (Chlorophyceae). Aquatic Toxicol, 68, 315–323.

    Article  CAS  Google Scholar 

  • Trebitsh, T., Levitan, A., Sofer, A. and Danon, A. (2000) Translation of chloroplast psbA mRNA is modulated in the light by counteracting oxidizing and reducing activities. Mol Cell Biol, 20, 1116–1123.

    Article  PubMed  CAS  Google Scholar 

  • Trebitsh, T., Meiri, E., Ostersetzer, O., Adam, Z. and Danon, A. (2001) The protein disulfide isomerase-like RB60 is partitioned between stroma and thylakoids in Chlamydomonas reinhardtii chloroplasts. J Biol Chem, 276, 4564–4569.

    Article  PubMed  CAS  Google Scholar 

  • Trémoliéres, A., Dainese, P. and Bassi, R. (1994) Heterogeneous lipid distribution among chloroplast-binding proteins of photosystem II in maize mesophyll chloroplasts. Eur J Biochem, 221, 721–730.

    Article  PubMed  Google Scholar 

  • Trossat, C., Rathinasabapathi, B., Weretilnyk, E.A., Shen, T.L., Huang, Z.H., Gage, D.A. and Hanson, A.D. (1998) Salinity promotes accumulation of 3-dimethylsulfoniopropionate and its precursor S-methylmethionine in chloroplasts. Plant Physiol, 116, 165–171.

    Article  PubMed  CAS  Google Scholar 

  • Tsang, M.L. (1981) Thioredoxin/glutaredoxin system of Chlorella: Chlorella adenosine 5′-phosphosulfate sulfotransferase cannot use thioredoxin or glutaredoxin as cofactors. Plant Physiol, 68, 1098–1104.

    Article  PubMed  CAS  Google Scholar 

  • Tsuji, N., Hirayanagi, N., Iwabe, O., Namba, T., Tagawa, M., Miyamoto, S., Miyasaka, H., Takagi, M., Hirata, K. and Miyamoto, K. (2003) Regulation of phytochelatin synthesis by zinc and cadmium in marine green alga, Dunaliella tertiolecta. Phytochemistry, 62, 453–459.

    Article  PubMed  CAS  Google Scholar 

  • Tsuji, N., Nishikori, S., Iwabe, O., Matsumoto, S., Shiraki, K., Miyasaka, H., Takagi, M., Miyamoto, K. and Hirata, K. (2005) Comparative analysis of the two-step reaction catalyzed by prokaryotic and eukaryotic phytochelatin synthase by an ion-pair liquid chromatography assay. Planta, 222, 181–191.

    Article  PubMed  CAS  Google Scholar 

  • Tsuji, N., Nishikori, S., Iwabe, O., Shiraki, K., Miyasaka, H., Takagi, M., Hirata, K. and Miyamoto, K. (2004) Characterization of phytochelatin synthase-like protein encoded by alr0975 from a prokaryote, Nostoc sp. PCC 7120. Biochem Biophys Res Commun, 315, 751–755.

    Article  PubMed  CAS  Google Scholar 

  • Turmel, M., Otis, C. and Lemieux, C. (1999) The complete chloroplast DNA sequence of the green alga Nephroselmis olivacea: insights into the architecture of ancestral chloroplast genomes. Proc Natl Acad Sci U S A, 96, 10248–10253.

    Article  PubMed  CAS  Google Scholar 

  • Turmel, M., Otis, C. and Lemieux, C. (2005) The complete chloroplast DNA sequences of the charophycean green algae Staurastrum and Zygnema reveal that the chloroplast genome underwent extensive changes during the evolution of the Zygnematales. BMC Biol, 3, 22.

    Article  PubMed  CAS  Google Scholar 

  • Utkilen, H.C. (1976) Thiosulphate as electron donor in the blue-green alga Anacystis nidulans. J Gen Microbiol, 95, 177–180.

    PubMed  CAS  Google Scholar 

  • van Waasbergen, L.G., Dolganov, N. and Grossman, A.R. (2002) nblS, a gene involved in controlling photosynthesis-related gene expression during high light and nutrient stress in Synechococcus elongatus PCC 7942. J Bacteriol, 184, 2481–2490.

    Article  PubMed  CAS  Google Scholar 

  • Visviki, I. and Rachlin, J.W. (1994) Acute and chronic exposure of Dunaliella salina and Chlamydomonas bullosa to copper and cadmium: effects of ultrastructure. Arch Environ Contam Toxicol, 26, 154–162.

    PubMed  CAS  Google Scholar 

  • Vivares, D., Arnoux, P. and Pignol, D. (2005) A papain-like enzyme at work: native and acyl-enzyme intermediate structures in phytochelatin synthesis. Proc Natl Acad Sci U S A, 102, 18848–18853.

    Article  PubMed  CAS  Google Scholar 

  • Vlamis-Gardikas, A. and Holmgren, A. (2002) Thioredoxin and glutaredoxin isoforms. Methods Enzymol, 347, 286–296.

    Article  PubMed  CAS  Google Scholar 

  • Wagner, V., Gessner, G., Heiland, I., Kaminski, M., Hawat, S., Scheffler, K. and Mittag, M. (2006) Analysis of the phosphoproteome of Chlamydomonas reinhardtii provides new insights into various cellular pathways. Eukaryot Cell, 5, 457–468.

    Article  PubMed  CAS  Google Scholar 

  • Wagner, W. and Follmann, H. (1977) A thioredoxin from green algae. Biochem Biophys Res Commun, 77, 1044–1051.

    Article  CAS  Google Scholar 

  • Wakasugi, T., Nagai, T., Kapoor, M., Sugita, M., Ito, M., Ito, S., Tsudzuki, J., Nakashima, K., Tsudzuki, T., Suzuki, Y., Hamada, A., Ohta, T., Inamura, A., Yoshinaga, K. and Sugiura, M. (1997) Complete nucleotide sequence of the chloroplast genome from the green alga Chlorella vulgaris: the existence of genes possibly involved in chloroplast division. Proc Natl Acad Sci U S A, 94, 5967–5972.

    Article  PubMed  CAS  Google Scholar 

  • Watanabe, M. and Suzuki, T. (2004) Cadmium induced synthesis of HSP70 and a role of glutathione in Euglena gracilis. Redox Report, 9, 349–353.

    Article  PubMed  CAS  Google Scholar 

  • Weber, M., Suter, M., Brunold, C. and Kopriva, S. (2000) Sulfate assimilation in higher plants: characterization of a stable intermediate in the adenosine 5′-phosphosulfate reductase reaction. European Journal of Biochemistry, 267, 3647–3653.

    Article  PubMed  CAS  Google Scholar 

  • Whittaker, M.M. and Gleason, F.K. (1984) Isolation and characterization of thioredoxin f from the filamentous cyanobacterium, Anabaena sp. 7119. J Biol Chem, 259, 14088–14093.

    PubMed  CAS  Google Scholar 

  • Wilkinson, B. and Gilbert, H.F. (2004) Protein disulfide isomerase. Biochim Biophys Acta, 1699, 35–44.

    PubMed  CAS  Google Scholar 

  • Wolfe, G.V., Steinke, M. and Kirst, G.O. (1997) Grazing-activated chemical defence in a unicellular marine alga. Nature, 387, 894–897.

    Article  CAS  Google Scholar 

  • Wykoff, D.D., Davies, J.P., Melis, A. and Grossman, A.R. (1998) The regulation of photosynthetic electron transport during nutrient deprivation in Chlamydomonas reinhardtii. Plant Physiol, 117, 129–139.

    Article  PubMed  CAS  Google Scholar 

  • Wykoff, D.D., Grossman, A.R., Weeks, D.P., Usuda, H. and Shimogawara, K. (1999) Psr1, a nuclear localized protein that regulates phosphorus metabolism in Chlamydomonas. Proc Natl Acad Sci U S A, 96, 15336–15341.

    Article  PubMed  CAS  Google Scholar 

  • Yamanaka, G., Glazer, A.N. and Williams, R.C. (1980) Molecular architecture of a light-harvesting antenna. Comparison of wild type and mutant Synechococcus 6301 phycobilisomes. J Biol Chem, 255, 11104–11110.

    PubMed  CAS  Google Scholar 

  • Yildiz, F.H., Davies, J.P. and Grossman, A. (1996) Sulfur availability and the SAC1 gene control adenosine triphosphate sulfurylase gene expression in Chlamydomonas reinhardtii. Plant Physiol, 112, 669–675.

    Article  PubMed  CAS  Google Scholar 

  • Yildiz, F.H., Davies, J.P. and Grossman, A.R. (1994) Characterization of sulfate transport in Chlamydomonas reinhardtii during sulfur-Limited and sulfur-sufficient growth. Plant Physiol, 104, 981–987.

    PubMed  CAS  Google Scholar 

  • Yoch, D.C., Ansede, J.H. and Rabinowitz, K.S. (1997) Evidence for intracellular and extracellular dimethylsulfoniopropionate (DMSP) lyases and DMSP uptake sites in two species of marine bacteria. Appl Environ Microbiol, 63, 3182–3188.

    PubMed  CAS  Google Scholar 

  • Yokota, A., Shigeoka, S., Onishi, T. and Kitaoka, S. (1988) Selenium as inducer of glutathione peroxidase in low-CO2-grown Chlamydomonas reinhardtii. Plant Physiol, 86, 649–651.

    Article  PubMed  CAS  Google Scholar 

  • Yosef, I., Irihimovitch, V., Knopf, J.A., Cohen, I., Orr-Dahan, I., Nahum, E., Keasar, C. and Shapira, M. (2004) RNA binding activity of the ribulose-1,5-bisphosphate carboxylase/oxygenase large subunit from Chlamydomonas reinhardtii. J Biol Chem, 279, 10148–10156.

    Article  PubMed  CAS  Google Scholar 

  • Yoshimura, K., Miyao, K., Gaber, A., Takeda, T., Kanaboshi, H., Miyasaka, H. and Shigeoka, S. (2004) Enhancement of stress tolerance in transgenic tobacco plants overexpressing Chlamydomonas glutathione peroxidase in chloroplasts or cytosol. Plant J, 37, 21–33.

    Article  PubMed  CAS  Google Scholar 

  • Zhang, L., Happe, T. and Melis, A. (2002) Biochemical and morphological characterization of sulfur-deprived and H2-producing Chlamydomonas reinhardtii (green alga). Planta, 214, 552–561.

    Article  PubMed  CAS  Google Scholar 

  • Zhang, L. and Melis, A. (2002) Probing green algal hydrogen production. Philos Trans R Soc Lond B Biol Sci, 357, 1499–1507; discussion 1507–1411.

    Article  PubMed  CAS  Google Scholar 

  • Zhang, Z., Shrager, J., Jain, M., Chang, C.W., Vallon, O. and Grossman, A.R. (2004) Insights into the survival of Chlamydomonas reinhardtii during sulfur starvation based on microarray analysis of gene expression. Eukaryot Cell, 3, 1331–1348.

    Article  PubMed  CAS  Google Scholar 

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  1. Department of Plant Biology, Carnegie Institution, 94305, Stanford, CA, USA

    Nakako Shibagaki & Arthur Grossman

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Shibagaki, N., Grossman, A. (2008). The State of Sulfur Metabolism in Algae: From Ecology to Genomics. In: Hell, R., Dahl, C., Knaff, D., Leustek, T. (eds) Sulfur Metabolism in Phototrophic Organisms. Advances in Photosynthesis and Respiration, vol 27. Springer, Dordrecht. https://doi.org/10.1007/978-1-4020-6863-8_13

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