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Allocation of Sulfur to Sulfonium Compounds in Microalgae

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Sulfur Assimilation and Abiotic Stress in Plants

Many algae are able to use S surplus to produce sulfonium compounds with different functions. Among these, dimethylsulfoniopropionate (DMSP) has attracted the attention of the scientific community for its multiple functions. DMSP is produced by some salt-tolerant angiosperms and by many marine algae. Different phytoplankton groups show different abilities to produce this compound: dinoflagellates, diatoms, and coccolithophores usually produce large amounts of DMSP, while Chlorophytes and cyanobacteria tend to produce very little DMSP, if any. DMSP has been proposed to act as thermoprotectant, osmoprotectant, antioxidant, and antigrazing agent. The antigrazing activity of DMSP requires its cleavage by a specific lyase to produce dimethylsulfide (DMS) and acrylate, the latter being the antigrazing agent. DMS has been suggested to play an important role in climate control. This review discusses the allocation of sulfur to different sulfonium compounds, mostly focusing on the role played by DMSP in response to abiotic and biotic stresses and on their implications in the ecology and evolution of phytoplankton.

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References

  • Anbar AD, Knoll AH (2002) Proterozoic ocean chemistry and evolution: a bioinorganic bridge? Science 297:1137–42

    Article  PubMed  CAS  Google Scholar 

  • Anderson R, Kates M, Volcani BE (1978a) Identification of the sulfolipids in the non-photosynthetic diatom Nitzschia alba. Biochim Biophys Acta 528:89–106

    PubMed  CAS  Google Scholar 

  • Anderson R, Livermore BP, Kates M, Volcani BE (1978b) The lipid composition of the non-photosynthetic diatom Nitzschia alba. Biochim Biophys Acta 528:77–88

    PubMed  CAS  Google Scholar 

  • Bambach RK (1993) Seafood through time: changes in biomass, energetics, and productivity in the marine ecosystem. Paleobiol 19:372–97

    Google Scholar 

  • Basic MK, Yoch DC (1998) In vivo characterization of dimethylsulfonioproprionate lyase in the fungus Fusarium lateritium. Appl Environ Microbiol 64:106–11

    Google Scholar 

  • Bates TS, Charlson RJ, Gammon RH (1987) Evidence for the climatic role of marine biogenic sulfur. Nature 329:319–21

    Article  CAS  Google Scholar 

  • Baumann MEM, Brandini FP, Staubes R (1994) The influence of light and temperature on carbon-specific DMS release by culture of Phaeocystis aantarctica and three Antarctic diatoms. Mar Chem 45:129–36

    Article  CAS  Google Scholar 

  • Belviso S, Kim SK, Rassoulzadegan, Krajka B, Nguyen BC, Mihalopoulos N, Buat-Menard P (1990) Production of dimethylsulfonio propionate (DMSP) and dimethylsulfide (DMS) by a microbial food web. Limnol Oceanogr 35:1810–21

    Article  CAS  Google Scholar 

  • Berges JA, Falkowski PG (1998) Physiological stress and cell death in marine phytoplankton: Induction of proteases in response to nitrogen or light limitation. Limnol Oceanogr 43:129–35

    Article  CAS  Google Scholar 

  • Bick JA, Leustek T (1998) Plant sulfur metabolism-the reduction of sulfate to sulfite. Curr Opin Plant Biol 1:240–4

    Article  PubMed  CAS  Google Scholar 

  • Bisseret P, Ito S, Tremblay PA, Volcani BE, Dessort D, Kates M (1984) Occurrence of phosphatidylsulfocholine, the sulfonium analog of phosphatidylcoline in some diatoms and algae. Biochim Biophys Acta 796:320–7

    PubMed  CAS  Google Scholar 

  • Booth E, Walker K (1997) The effectiveness of foliar glucosinolate content raised by sulfur application on disease control in oilseed rape. In: Cram WJ, De Kok LJ, Stulen I, Brunold C, Rennenberg H (eds) Sulphur metabolism in higher plants, Backhuys Publisher, Leiden, The Netherlands, pp. 327–9

    Google Scholar 

  • Bork C, Schwenn J-D, Hell R (1998) Isolation and characterization of a gene for assimilaory sulfite reductase from Arabidopsis thaliana. Gene 212:147–53

    Article  PubMed  CAS  Google Scholar 

  • Borowitzka LJ (1981) Solute accumulation and regulation of cell water activity. In Paleg LG, Aspinall D (eds) Physiology and biochemistry of drought resistance in plants, Academic Press, Melbourne, pp. 97–30

    Google Scholar 

  • Bratbak G, Levasseur M, Michaud S, Cantin G, Fernández E, Heimdal BR, Heldal M (1995) Viral activity in relation to Emiliania huxleyi blooms: a mechanism of DMSP release? Mar Ecol Prog Ser 128:133–42

    Article  CAS  Google Scholar 

  • Bucciarelli E, Sunda WG (2003) Influence of CO2, nitrate, phosphate, and silicate limitation on intracellular dimethylsulfoniopropionate in batch cultures of the coastal diatom Thalassiosira pseudonana. Limnol Oceanogr 48:2256–65

    CAS  Google Scholar 

  • Canfield DE (1998) A new model for Proterozoic ocean chemistry. Nature 396:450–3

    Article  CAS  Google Scholar 

  • Cantoni GL (1952) The nature of the active methyl donor formed enzymatically form L-methionine and adenosinetriphosphate. J Am Chem Soc 74:2942–3

    Article  CAS  Google Scholar 

  • Cantoni GL (1953) S-Adenosylmethionine: a new intermediate formed enzymatically from L-methionine and adenosinetriophosphate. J Biol Chem 204:403–6

    CAS  Google Scholar 

  • Charlson RJ, Lovelock JE, Andreae MO, Warren SG (1987) Oceanic phytoplankton, atmospheric sulphur, cloud albedo and climate. Nature 326:655–61

    Article  CAS  Google Scholar 

  • Chen HC, 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 HC, Newton AJ, Melis A (2005) Role of SulP, a nuclear-encoded chloroplast sulfate permease, in sulfate transport and H2 evolution in Chlamydomonas reinhardtii. Photosynth Res 84:289–96

    Article  PubMed  CAS  Google Scholar 

  • Chen HC, Yokthongwattana K, Newton AJ, Melis A (2003) SulP, a nuclear gene encoding a putative chloroplast-targeted sulfate permease in Clamydomonas reinhardtii. Planta 218:98–106

    Article  PubMed  CAS  Google Scholar 

  • Chou T-C, Talalay P (1972) The mechanism of S-adenosyl-L-methionine synthesis by purified preparations of baker’s yeast. Biochem 11:1065–73

    Article  CAS  Google Scholar 

  • Cooper AJL (1996) Chemical and biochemical properties of sulfonium compounds. In Kiene RP, Visscher PT, Keller MD, Kirst GO (eds) Biological and environmental chemistry of DMSP and related sulfonium compounds, Plenum Press, New York, pp. 75–86

    Google Scholar 

  • Dacey JWH, King GM, Wakeham SG (1987) Factors controlling emission of dimethylsulphide from salt marshes. Nature 330:643–5

    Article  CAS  Google Scholar 

  • Dacey JWH, Wakeham SG (1986) Oceanic dimethylsulfide: production during zooplankton grazing on phytoplankton. Science 233:1314–15

    Article  PubMed  CAS  Google Scholar 

  • de Hostos E, Schilling J, Grossman AR (1989) Structure and expression of the gene encoding the periplasmic arylsulfatase in Chlamydomonas reinhardtii. Mol Gen Genet 218:229–39

    Article  PubMed  Google Scholar 

  • de Hostos E, Togasaki RK, Grossman Ar (1988) Purification and biosynthesis of derepressible periplasmic arylsulfatase from Chlamydomonas reinhardtii. J Cell Biol 106:29–37

    Article  PubMed  Google Scholar 

  • de Souza MP, Chen YP, Yoch DC (1996) Dimethylsulfoniopropionate lyase from the marine macroalga Ulva curvata: purification and characterization of the enzyme. Planta 199:433–8

    Article  Google Scholar 

  • de Souza MP, Yoch DC (1995a) Comparative physiology of dimethyl sulphide production by dimethylsulfoniopropionate lyase in Pseudomonas doudoroffii and Alcaligenes sp. strain M3A. Appl Environ Microbiol 61:3986–91

    PubMed  Google Scholar 

  • de Souza MP, Yoch DC (1995b) Purification and characterization of dimethylsulfoniopropionate lyase from an Alcaligenes-like dimethyl sulphide-producing marine isolate. Appl Environ Microbiol 61:21–6

    PubMed  Google Scholar 

  • Dickson DJJ, Kirst GO (1986) The role of dimethylsulphonioproprionate, glycine betaine and homarine in the osmoacclimation of Platymonas subcordiformis. Planta 167:536–43

    Article  CAS  Google Scholar 

  • Dickson DM, Kirst GO (1987a) Osmotic adjustment in marine eukaryotic algae, the role of inorganic ions, quaternary ammonium, tertiary sulphonium and carbohydrate solutes. I. Diatoms and Rhodophyte. New Phytol 106:645–55

    Article  CAS  Google Scholar 

  • Dickson DM, Kirst GO (1987b) Osmotic adjustment in marine eukaryotic algae, the role of inorganic ions, quaternary ammonium, tertiary sulphonium and carbohydrate solutes. II. Prasinophytes and Haptophytes. New Phytol 106:657–66

    Article  CAS  Google Scholar 

  • Eichel J, Gonzales JC, Hotze M, Matthews RG, Schröder J (1995) Vitamin-B12-independent methionine synthase from a higher plant (Catharantus roseus). Molecular characterization, regulation, heterologous expression, and enzyme properties. Eur J Biochem 230:1053–8

    Article  PubMed  CAS  Google Scholar 

  • Evans JR, Terashima I (1987) Effects of nitrogen nutrition on electron transport components and photosynthesis in spinach. Aust J Plant Physiol 14:59–68

    Article  CAS  Google Scholar 

  • Falkowski PG, Katz ME, Knoll A, Quigg A, Raven JA, Schofield O, Taylor FJR (2004) The evolution of modern eukaryotic phytoplankton. Science 305:354–60

    Article  PubMed  CAS  Google Scholar 

  • Farias WRL, Valente AP, Pereira MS, Mourão PAS (2000) Structure and anticoagulant activity of sulfated galactans. Isolation of a unique sulfated galactan from the red algae Botryocladia occidentalis and comparison of its anticoagulant action with that of sulfated galactans from invertebrates. J Biol Chem 275:29299–397

    Article  PubMed  CAS  Google Scholar 

  • Freidig AP, Verhaar HJM, Hermens JLM (1999) Comparing the potency of chemicals with multiple modes of action in aquatic toxicology: acute toxicity due to narcosis versus reactive toxicity of acrylic compounds. Environ Sci Technol 33:3038–43

    Article  CAS  Google Scholar 

  • Gage DA, Rhodes D, Nolte KD, Hicks WA, Leustek T, Cooper AJL, Hanson AD (1997) A new route for synthesis of dimethylsulphonioproprionate in marine algae. Nature 387:891–4

    Article  PubMed  CAS  Google Scholar 

  • Gao Y, Schofield OME, Leustek T (2000) Characterization of sulfate assimilation in marine algae focusing on the enzyme 50-adenylylsulfate reductase. Plant Physiol 123:1087–96

    Article  PubMed  CAS  Google Scholar 

  • Giordano M, Norici A, Hell R (2005) Sulfur and phytoplankton: acquisition, metabolism and impact on the environment. New Phytol 166:371–82

    Article  PubMed  CAS  Google Scholar 

  • Giordano M, Norici A, Ratti S, Raven JAR. (2008) Role of sulfur for phytoplankton: acquisition, metabolism and ecology. In: Hell R, Leustek T, Knaff D, Dahl C (eds.), Advances in Photosynthesis Research Vol. 27: Sulfur metabolism in phototrophic organisms, Govindjee (series ed.), Springer, Berlin, Germany, pp. 405–423

    Google Scholar 

  • Giovanelli J, Mudd SH, Datko AH (1985) Quantitative analysis of pathways of methionine metabolism and their regulation in Lemna. Plant Physiol 78:555–60

    Article  PubMed  CAS  Google Scholar 

  • Gröne T, Kirst GO (1991) Aspects of dimethylsulfoniopropionate effects on enzymes isolated from the marine phytoplankter Tetraselmis subcordiformis (Stein). J Plant Physiol 138:85–91

    Google Scholar 

  • Gröne T, Kirst GO (1992) The effect of nitrogen deficiency, methionine and inhibitors of methionine metabolism on the DMSPp contents of Tetraselmis subcordiformis (Stein). Mar Bio 112:497–503

    Article  Google Scholar 

  • Hanson AD, Gage DA (1996) 3-dimethylsulfonioproprionate biosynthesis and use by flowering plants. In Kiene RP, Visscher PT, Keller MD, Kirst GO (eds) Biological and environmental chemistry of DMSP and related sulfonium compounds, Plenum Press, New York, pp. 75–86

    Google Scholar 

  • Hawkesford MJ, Wray JL (2000) Molecular genetics of sulfur assimilation. Adv Bot Res 33:159–23

    Article  CAS  Google Scholar 

  • Heldal M, Scanlan DJ, Norland S, Thingstad F and Mann NH (2003) Elemental composition of single cells of various strains of marine Prochlorococcus and Synechococcus using X-ray microanalysis. Limnol Oceanogr 48:1732–43

    Article  CAS  Google Scholar 

  • Hell R (1997) Molecular physiology of plant sulfur metabolism. Planta 202:138–48

    Article  PubMed  CAS  Google Scholar 

  • Hill RW, White BA, Cottrell M, Dacey JWH (1998) Virus-mediated total release of dimethylsulfoniopropionate from marine phytoplankton: a potential climate process. Aquat Microb Ecol 14:1–6

    Article  Google Scholar 

  • Ho T-Y, Quigg A, Finkel ZV, Milligan AJ, Wyman K, Falkowski PG and Morel FMM (2003) The elemental composition of some marine phytoplankton. J Phycol 39:145–59

    Article  Google Scholar 

  • Holmer M, Storkholm P (2001) Sulfate reduction and sulfur cycling in lake sediments: a review. Freshwater Biol 46:431–51

    Article  CAS  Google Scholar 

  • Jakob B, Heber U (1996) Photoproduction and detoxification of hydroxyl radicals in chloroplasts and leaves and (its) relation to photoinactivation of photosystem I and II. Plant Cell Physiol 37:625–9

    Google Scholar 

  • Karsten U, Kuck K, Vogt C, Kirst GO (1996) Dimethylsulfoniopropionate production in phototrophic organisms and its physiological function as a cryoprotectant. In Kiene RP, Visscher PT, Keller MD, Kirst GO (eds) Biological and environmental chemistry of DMSP and related sulfonium compounds, Plenum Press, New York, pp. 143–53

    Google Scholar 

  • Karsten U, Wiencke C, Kirst GO (1990) The effect of light intensity and daylenght on the )-dimethylsulphonio-propionate (DMSP) content of green macroalgae at different irradiances. Plant Cell Environ 13:989–93

    Article  CAS  Google Scholar 

  • Karsten U, Wiencke C, Kirst GO (1992) Dimethylsulfioniopropionate (DMSP) accumulation in green macroalgae from polar to temperate regions: interactive effect of light versus salinity and light versus temperature. Polar Biol 12:603–60

    Article  Google Scholar 

  • Kasamatsu N, Hirano T, Kudoh S, Odate T, Fukuchi M (2004a) Dimethylsulfonioproprionate production by psychrophylic diatom isolates. J Phycol 40:874–8

    Article  CAS  Google Scholar 

  • Kasamatsu N, Kawaguchi S, Watanabe S, Odate T, Fukuchi M (2004b) Possible impacts of zooplankton grazing on dimethylsulfide production in the Antarctic Ocean. Can J Fish Aquat Sci 61:736–43

    Article  CAS  Google Scholar 

  • Kates and Volcani (1966) Lipids of diatoms. Biochim Biophys Acta 116:264–76

    PubMed  CAS  Google Scholar 

  • Kates M, Volcani BE (1996) Biosynthetic patways for phosphatidylsulfocholine, the sulfonium analogue of phoaphatidylcholine, in diatoms. In Kiene RP, Visscher PT, Keller MD, Kirst GO (eds) Biological and environmental chemistry of DMSP and related sulfonium compounds, Plenum Press, New York, pp. 109–19

    Google Scholar 

  • Katz ME, Finkel ZV, Grzebyk D, Knoll AH, Falkowski PG (2004) Evolutionary trajectories and biogeochemical impacts of marine eukaryotic phytoplankton. Annu Rev Ecol Evol Syst 35:523–56

    Article  Google Scholar 

  • Keller MD (1991) Dimethylsulphide production and marine phytoplankton: the importance of species composition and cell size. Biol Oceanogr 6:375–82

    Google Scholar 

  • Keller MD, Bellows WK, Guillard RRL (1989) Dimethyl sulfide production in marine phytoplantkon. In Saltzman ES, Cooper WJ (eds) Biogenic sulfur in the environment, American Chemical Society, Washington DC, pp. 167–82

    Chapter  Google Scholar 

  • Keller MD, Kiene RP, Matrai PA, Bellows WK (1999) Production of glycine betaine and dimethy lsulfoniopropionate in marine phytoplankton. I. Batch cultures. Mar Biol 135:237–48

    Article  CAS  Google Scholar 

  • Keller MD, Korjeff-Bellows W (1996) Physiological aspects of the production of dimethylsulfoniopropionate (DMSP) by marine phytoplankton. In: Kiene RP, Visscher PT, Keller MD, Kirst GO (eds) Biological and environmental chemistry of DMSP and related sulfonium compounds, Plenum, New York, pp. 131–42

    Google Scholar 

  • Kiene RP, Linn LJ (2000) The fate of dissolved dimethylsulfoniopropionate (DMSP) in seawater: tracer studies using 35S-DMSP. Geochim Cosmochim Acta 64:2797–2810

    Article  CAS  Google Scholar 

  • Kiene RP, Taylor BF (1988) Demethylation of dimethylsulfonioproprionate and production of thiols in anoxic marine sediments. Appl Environ Microbiol 54:2208–12

    PubMed  CAS  Google Scholar 

  • Kirst GO (1990) Salinity tolerance in eukaryotic marine algae. Annu Rev Plant Physiol Mol Biol 41:21–53

    Article  CAS  Google Scholar 

  • Kirst GO (1996) Osmotic adjustment in phytoplankton and macroalgae. In: Kiene RP, Visscher PT, Keller MD, Kirst GO (eds) Biological and environmental chemistry of DMSP and related sulfonium compounds, Plenum, New York, pp. 121–9

    Google Scholar 

  • Kirst GO, Thiel C, Wolff H, Nothnagel J, Wanzek M, Ulmke R (1991) Dimethylsulfoniopropionate (DMSP) in ice-algae and its possible biological role. Mar Chem 35:381–8

    Article  CAS  Google Scholar 

  • Knoll AH (2003) Biomineralization and evolutionary history. Rev Mineral Geochem 54:329–56

    Article  CAS  Google Scholar 

  • Kocsis MG, Nolte KD, Rhodes D, Shen T, Gage DA, Hanson AD (1998) Dimethylsulfoniopropionate biosynthesis in Spartina alterniflora. Evidence that S-Methylmethionine and dimethylsulfoniopropylamine are intermediates. Plant Physiol 117:273–81

    Article  PubMed  CAS  Google Scholar 

  • Kwint RLJ, Kramer KJM (1995) DMS production by plankton communities. Mar Ecol Prog Ser 121:227–37

    Article  CAS  Google Scholar 

  • Lappartient AG, Touraine B (1997) Comparison between demand-driven regulation of ATP sulfuphurylase activity and responses to oxidation stress. In: Cram WJ, De Kok LJ, Stulen I, Brunold C, Rennenberg H (eds) Sulphur metabolism in higher plants, Backhuys Publisher, Leiden, The Netherlands, pp. 203–5

    Google Scholar 

  • Laroche D, Vezina AF, Levasseur M, Gosselin M, Stefels J, Keller MD, Matrai PA, Kwint RLJ (1999) DMSP synthesis and exudation in phytoplankton: a modelling approach. Mar Ecol Prog Ser 180:37–49

    Article  CAS  Google Scholar 

  • Leck C, Larsson U, Bagander LE, Johansson S, Hajdu S (1990) Dimethyl sulphide in the Baltic sea: annual variability in relation to biological activity. J Geophys Res 95:3353–63

    Article  Google Scholar 

  • Lee JH, Chae HS, Lee JH, Hwang B, Hahn KW, Kang BG, Kim WT (1997) Structure and expression of two cDNAs encoding S-adenosyl-L-methionine synthetase of rice (Oryza sativa L.) Biochim Biophys Acta 1354:13–18

    PubMed  CAS  Google Scholar 

  • Lee PA, de Mora SJ (1999) Intracellular dimethylsulfoxide (DMSO) in unicellular marine algae: Speculations on its origin and possible biological role. J Phycol 35:8–18

    Article  CAS  Google Scholar 

  • Leustek T, Saito K (1999) Sulfate transport and assimilation in plants. Plant Physiol 120:637–43

    Article  PubMed  CAS  Google Scholar 

  • Leustek T, Martin MN, Bick J-A and Davies JP (2000) Pathways and regulation of sulfur metabolism revealed through molecular and genetic studies. Annu Rev Plant Physiol 51:141–65

    Article  CAS  Google Scholar 

  • Levasseur M, Michaud S, Egge J, Cantin G, Nejstgaard JC, Sanders R, Fernadez E, Solberg PT, Heimdal B, Gosselin M (1996) Production of DMSP and DMS during a mesocosm study of an Emiliania huxleyi bloom: influence of bacteria and Calanus finmarchicus grazing. Mar Biol 126:609–18

    Article  CAS  Google Scholar 

  • Liss PS, Hatton AD, Malin G, Nightingale PD, Turner SM (1997) Marine sulphur emissions. Phil Trans R Soc Lond B 352:159–69

    Article  CAS  Google Scholar 

  • Logan BA, Demmig-Adams B, Rosenstiel TN, Adams III WW (1999) Effect of nitrogen limitation on foliar antioxidants in relationship to other metabolic characteristics. Planta 209:213–20

    Article  PubMed  CAS  Google Scholar 

  • Lovelock JE, Maggs RJ, Rasmussen RA (1972) Atmospheric dimethyl sulphide and the natural sulphur cycle Nature 237:452–3

    CAS  Google Scholar 

  • Malin G (1996) The role of DMSP and DMS in the global sulfur cycle and climate regulation. In: Kiene RP, Visscher PT, Keller MD, Kirst GO (eds) Biological and environmental chemistry of DMSP and related sulfonium compounds, Plenum, New York, pp. 177–89

    Google Scholar 

  • Matrai PA, Keller MD (1994) Total organic sulfur and dimethylsulfoniopropionate in marine phytoplankton: intracellular variation. Mar Biol 119:61–8

    Article  CAS  Google Scholar 

  • Maw GA (1981) The biochemistry of sulphonium salts. In: Stirling CJM (ed) The chemistry of the sulfonium group. Part 2, Wiley, New York, pp 703–70

    Google Scholar 

  • McNeil SD, Nuccio ML, Hanson AD (1999) Betaines and related osmoprotectants. Targets for metabolic engineering of stress resistance. Plant Physiol 120:945–9

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Meyerdierks D (1997) Ecophysiology of the dimethylsulfonioproprionate (DMSP) content of temperate and polar phytoplankton communities in comparison with cultures of the coccolithophore Emiliania huxleyi and the Antarctic diatom Nitszchia lecointei. Ber Polarforsch p. 233

    Google Scholar 

  • Michael, A (1887) Ueber die addition von natriumacetessig- und natriummalon- säureäthern zu den aethern ungesättigter säuren. J Prakt Chem35:349–56

    Article  Google Scholar 

  • Miller TR (2004) Swimming for sulfur: analysis of the Roseobacter- dinoflagellate interaction. PhD dissertation, University of Maryland

    Google Scholar 

  • Mudd SH, Datko AH (1990) The S-methylmethiomine cycle in Lemna paucicostata. Plant Physiol 93:623–30

    Article  PubMed  CAS  Google Scholar 

  • Nakamura H, Fujimaka K, Smapai O, Murai A (1993) Gonyol: Methionine-induced sulfonium accumulation in a dinoflagellate Gonyaulax polyedra. Tet Lett 34:8481–4

    Article  CAS  Google Scholar 

  • Nakamura H, Ohtoshi M, Sampei O, Akashi Y, Murai A (1992) Synthesis and absolute configuration of (+)-gonyauline: A modulating substance of bioluminescent circadian rhythm in the unicellular alga Gonyaulax polyedra. Tet Lett 33:2821–2

    Article  CAS  Google Scholar 

  • Nakamura H, Jin T, Funahashi M, Murai A (1996) Intergovernmental Oceanographic Commission of UNESCO. In: Yasumoto T, Oshima Y, Fukuyo Y (eds) Harmful and Toxic Algal Blooms, Intergovernmental Oceanographic Commission of UNESCO, Paris, pp. 515–18

    Google Scholar 

  • Nakamura H, Jin T, Funahashi M, Fujimaki K, Sampei O, Murai A, Roenneberg T, Hastings J W (1997) Biogenesis of sulfonium compounds in a dinoflagellate; methionine cascade. Tetrahedron 53:9067–74

    Article  CAS  Google Scholar 

  • Nakano Y, Koizumi N, Kusano T, Sano H (2000) Isolation and properties of an S-adenosyl-L-methionine binding protein from the green alga, Chlamydomonas reinhardtii. J Plant Physiol 157:707–11

    CAS  Google Scholar 

  • Nguyen BC, Belviso S, Mihalopoulos N, Gostan J, Nival P (1988) Dimethyl sulphide production during natural phytoplankton blooms. Mar Chem 24:133–41

    Article  Google Scholar 

  • Nguyen BC, Bonsang B, Gaudry A (1983) The role of the ocean in the global atmospheric sulphur cycle. J Geophys Resear 88:10903–14

    Article  CAS  Google Scholar 

  • Niki T, Kunugi M, Otsuki A (2000) DMSP-lyase activity in five marine phytoplankton species: its potential importance in DMS production. Mar Biol 136:759–64

    Article  CAS  Google Scholar 

  • Nishiguchi MK, Somero GN (1992) Temperature- and concentration- dependence of compatibility of the organic osmolyte β-dimethylsulfoniopropionate. Cryobiol 29:118–24

    Article  CAS  Google Scholar 

  • Norici A, Hell R, Giordano M (2005) Sulfur and primary production in aquatic environments: an ecological perspective. Photosynth Res 86:409–17

    Article  PubMed  CAS  Google Scholar 

  • Otte ML, Morris JT (1994) Dimethylsulphoniopropionate (DMSP) in Spartina alterniflora Loisel Aquat Bot 48:239–59

    Article  CAS  Google Scholar 

  • Otte ML, Wilson G, Morris JT, Moran BM (2004) Dimethylsulphoniopropionate (DMSP) and related compounds in higher plants. J Exp Bot 55:1919–25

    Article  PubMed  CAS  Google Scholar 

  • Painter TJ (1983) Algal polysaccharides. In: Aspinall GO (ed) The polysaccharides, Academic Press, New York, pp. 195–285:

    Google Scholar 

  • Perez-Castineira JR, Prieto JL, Vega JM (1992) Sulfate uptake in Chlamydomonas reinhardtii Phyton 32:91–3

    CAS  Google Scholar 

  • Pilson MEQ (1998) An introduction to the chemistry of the sea. Prentice Hall, Upper Saddle River, NJ, USA

    Google Scholar 

  • Pollock SV, Pootakham W, Shibagaki N, Moseley JL, Grossman AR (2005) Insights into the acclimation of Chlamydomonas reinhardtii to sulfur deprivation. Photosynth Res 86:475–89

    Article  PubMed  CAS  Google Scholar 

  • Ravanel S, Gakière B, Job D, Douce R (1998) The specific feature of methionine biosynthesis and metabolism in plants. Proc Natl Acad Sci USA 95:7805–12

    Article  PubMed  CAS  Google Scholar 

  • Ravina CG, Chang CI, Tsakraklides GP, McDermott JP, Vega JM, Leustek T, Gotor C, Davies JP (2002) The sac mutants of Chlamydomonas reinhardtii reveal transcriptional and posttranscriptional control of cysteine biosynthesis. Plant Physiol 130:2076–84

    Article  PubMed  CAS  Google Scholar 

  • Reed RH (1990) Solute accumulation and osmotic adjustment. In: Cole KM, Sheath RG (eds) Biology of the red algae, Cambridge University Press, pp. 147–70

    Google Scholar 

  • Rhodes D, Hanson AD (1993) Quaternary ammonium and tertiary sulfonium compounds in higher plants. Annu Rev Physiol Plant Mol Biol 44:357–84

    Article  CAS  Google Scholar 

  • Roenneberg T, Nakamura H, Cranmer LD, Ryan K, Kishi Y, Hastings JW (1991) Gonyauline: a novel endogenous substance shortening the period of the circadian clock of a unicellular algae. Experientia 47:103–6

    Article  PubMed  CAS  Google Scholar 

  • Saito K (2000) Regulation of sulfate transport and synthesis of sulfur-containing amino acids. Curr Opin Plant Biol 3:188–95

    PubMed  CAS  Google Scholar 

  • Scaduto RC (1995) Oxidation of DMSO and methane sulfinic acid by the hydroxyl radical. Free Radic Biol Med 18:271–7

    Article  PubMed  CAS  Google Scholar 

  • Schafer HJ, Greiner S, Rausch T, Haag-Derwer A (1997) In seedlings of the heavy metal accumulator Brassica juncea Cu2+ differentially affects transcript amounts for γ-glutamylcysteine synthetase (γ-ECS) and metallothionein (MT2) FEBS Lett 404:216–20

    Article  PubMed  CAS  Google Scholar 

  • Sheets EB, Rhodes D (1996) Determination of DMSP and other sulfonium compounds in Tetraselmis subcordiformis by plasma desorption mass spectrometry. In: Kiene RP, Visscher PT, Keller MD, Kirst GO (eds) Biological and environmental chemistry of DMSP and related sulfonium compounds, Plenum Press, New York, pp. 55–63

    Google Scholar 

  • Sieburth JM (1960) Acrylic acid, an “antibiotic” principle in Phaeocystis blooms in Antartic waters. Science 132:676–7

    Article  PubMed  CAS  Google Scholar 

  • Sieburth JM (1961) Antibiotic properties of acrylic acid, a factor in gastrointestinal antibiosis of polar marine animals. J Bact 82:72–9

    PubMed  CAS  Google Scholar 

  • Simó R, Pedrós-Allió C, Malin G, Grimalt JO (2000) Biological turnover of DMS, DMSP, and DMSO in contrasting open-sea waters. Mar Ecol Prog Ser 203:1–11

    Article  Google Scholar 

  • Sirko A, Hryniewicz MM, Hulanicka DM, Boeck A (1990) Sulfate and thiosulfate transport in Escherichia coli K-12: nucleotide sequence and expression of the cysTWAM gene cluster. J Bacteriol 172:3351–7

    PubMed  CAS  Google Scholar 

  • Stefels J (2000) Physiological aspects of the production and conversion of DMSP in marine algae and higher plants. J Sea Resear 43:183–97

    Article  CAS  Google Scholar 

  • Stefels J, Dijkhuizen L (1996) Characteristics of DMSP-lyase in Phaeocystis sp. (Primnesiophyceae) Mar Ecol Prog Ser 131:307–13

    Article  CAS  Google Scholar 

  • Stefels J, van Boekel WHM (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 

  • Steinke M, Kirst GO (1996) Enzymatic cleavage of dimethylsulfoniopropionate (DMSP) in cell-free extracts of the marine macroalga Enteromorpha clathrata (Roth) Grev. (Ulvales, Chlorophyta) J Exp Mar Biol Ecol 201:73–85

    Article  CAS  Google Scholar 

  • Steinke M, Wolfe GV, Kirst GO (1998) Partial characterisation of dimethylsulfoniopropionate (DMSP) lyase isozymes in 6 strains of Emiliania huxleyi. Mar Ecol Prog Ser 175:215–25

    Article  CAS  Google Scholar 

  • Storey R, Gorham J, Pitman MG, Hanson AD, Gage D (1993) Response of Melanthera biflora to salinity and water stress. J Exp Bot 44:1551–60

    Article  CAS  Google Scholar 

  • Strom S, Wolfe G, Holmes J, Stecher H, Shimeneck C, Lambert S, Moreno E (2003a) Chemical defense in the microplankton I: Feeding and growth rates of heterotrophic protists on the DMS-producing phytoplankter Emiliania huxleyi. Limnol Oceanogr 48:217–29

    Article  CAS  Google Scholar 

  • Strom S, Wolfe GV, Slajer A, Lambert S, Clough J (2003b) Chemical defence in the microplankton II: inhibition of protist feeding by β-dimethylsulfoniopropionate (DMSP) Limnol Oceanogr 48:230–7

    Article  CAS  Google Scholar 

  • Summers PS, Nolte KD, Cooper AJL, Leustek T, Rhodes D, Hanson AD (1998) Identification and stereospecificity of the first three enzymes of 3-dimethylsulfoniopropionate biosynthesis in a chlorophyte alga. Plant Physiol 116:369–78

    Article  CAS  Google Scholar 

  • Sunda W, Kieber DJ, Kiene RP, Huntsman S (2002) An antioxidant function for DMSP and DMS in marine algae. Nature 418:317–20

    Article  PubMed  CAS  Google Scholar 

  • Taylor BF, Gilchrist DC (1991) New routes of aerobic biodegradation of dimethylsulfonioproprionate. Appl Environ Microbiol 57:3581–4

    PubMed  CAS  Google Scholar 

  • Taylor BF, Visscher PT (1996) Metabolic pathways involved in DMSP degradation. In Kiene RP, Visscher PT, Keller MD, Kirst GO (eds) Biological and environmental chemistry of DMSP and related sulfonium compounds, Plenum, New York, pp. 265–76

    Google Scholar 

  • Turner SM, Maline G, Liss PS, Harbour DS, Holligan PM (1988) The seasonal variation of dimethyl sulphide and dimethylsulfonioproprionate concentrations in nearshore waters. Limnol Oceanogr 33:364–75

    Article  CAS  Google Scholar 

  • Uchida A, Ooguri T, Ishida T, Kitaguchi H, Ishida Y (1996) Biosynthesis of dimethylsulfonioproprionate in Crypthecodinium conhii (Dinophyceae). In Kiene RP, Visscher PT, Keller MD, Kirst GO (eds) Biological and environmental chemistry of DMSP and related sulfonium compounds, Plenum, New York, pp. 97–107

    Google Scholar 

  • Vairavamurthy A, Andreae MO, Iverson RL (1985) Biosynthesis of dimethylsulfide and dimethy lpropiothetin by Hymenomonas carterae in relation to sulfur source and salinity variations. Limnol Oceanogr 30:59–70

    Article  CAS  Google Scholar 

  • Van Alstyne KL, Houser LT (2003) Dimethylsulfide release during macroinvertebrate grazing and its role as an activated chemical defense. Mar Ecol Prog Ser 250:175–81

    Article  CAS  Google Scholar 

  • Van Alstyne KL, Wolfe GV, Freidenburg TL, Neill A, Hicken C (2001) Activated defence systems in marine macroalgae: evidence for an ecological role for DMSP cleavage. Mar Ecol Prog Ser 213:53–65

    Article  CAS  Google Scholar 

  • Van Bergeijk SA, Van der Zee C, Stal LJ (2003) Uptake and excretion of dimethylsulfoniopropionate is driven by salinity changes in marine benthic diatom Cylindrotheca closterium. Eur J Phycol 38:341–9

    Article  CAS  Google Scholar 

  • van Boekel WHM, Hansen FC, Riegman R, Bak RPM (1992) Lysis-induced decline of a Phaeocystis spring bloom and coupling with the microbial foodweb. Mar Ecol Prog Ser 81:269–76

    Article  Google Scholar 

  • Van Rijssel M, Gieskes WWC (2002) Temperature, light, and dimethylsulfonioproprionate (DMSP) content of Emiliania huxleyi (Prymnesiophyceae) J Sea Res 48:17–27

    Article  CAS  Google Scholar 

  • Welsh DT (2000) Ecological significance of compatible solute accumulation by micro-organisms: from single cells to global climate. FEMS Microbiol Rev 24:263–90

    Article  PubMed  CAS  Google Scholar 

  • Wilkinson F, Helman WP, Ross AB (1995) Rate constants for the decay and reactions of the lowest electronically excites singlet state of molecular oxygen in solution. An expanded and revised compilation J Phys Chem Ref Data 24:663–1021

    Article  CAS  Google Scholar 

  • Wolfe GV (2000) The chemical defence ecology of marine unicellular plankton: constraints, mechanisms, and impacts. Biol Bull 198:225–44

    Article  PubMed  CAS  Google Scholar 

  • Wolfe GV, Sherr EB, Sherr BF (1994) Release and consumption of DMSP from Emiliania huxleyi during grazing by Oxyrrhis marina. Mar Ecol Prog Ser 111:111–19

    Article  CAS  Google Scholar 

  • Wolfe GV, Steinke M (1996) Grazing-activated production of dimethyl sulphide (DMS) by two clones of Emiliania huxleyi. Limnol Oceanogr 41:1151–60

    Article  CAS  Google Scholar 

  • Wolfe GV, Steinke M, Kirst GO (1997) Grazing-activated chemical defence in a unicellular marine alga. Nature 387:894–7

    Article  CAS  Google Scholar 

  • Wolfe GV, Strom SL, Holmes JL, Radzio T, Olson MB (2002) Dimethylsulfoniopropionare cleavage by marine phytoplankton in response to mechanical, chemical, or dark stress. J Phycol 34:948–60

    Article  Google Scholar 

  • Yildiz FH, Davies JP, Grossman AR (1994) The regulation of photosynthetic electron transport in Chlamydomonas reinhardtii during sulfur-limited and sulfur-sufficient growth. Plant Physiol 104:981–7

    PubMed  CAS  Google Scholar 

  • Yoch DC (2002) Dimethylsulfoniopropionate: its sources, role in the marine food web, and biological degradation to dimethylsulfide. Appl Environm Microbiol 68:5804–15

    Article  CAS  Google Scholar 

  • Yoch DC, Ansede JH, Rabinowitz KS (1997) Evidence for intracellular and extracellular dimethy lsulfoniopropionate (DMSP) lyases and DMSP uptake sites in two species of marine bacteria. Appl Environ Microbiol 63:3182–8

    PubMed  CAS  Google Scholar 

  • Zarembinski TI, Theologis A (1994) Ethylene biosynthesis and action: a case of conservation. Plant Mol Biol 26:1579–97

    Article  PubMed  CAS  Google Scholar 

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  1. Dipartimento di Scienze del Mare, Università Politecnica delle Marche, Via Brecce Bianche, 60131, Ancona, Italy

    Simona Ratti & Mario Giordano

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  1. Simona Ratti
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  2. Mario Giordano
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  1. Aligarh Muslim University, 202002, Aligarh, India

    Nafees A. Khan  & Sarvajeet Singh  & 

  2. Jamia Hamdard, 110062, New Delhi, India

    Shahid Umar

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Ratti, S., Giordano, M. (2008). Allocation of Sulfur to Sulfonium Compounds in Microalgae. In: Khan, N.A., Singh, S., Umar, S. (eds) Sulfur Assimilation and Abiotic Stress in Plants. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-76326-0_15

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