Photosynthesis Research

, Volume 86, Issue 3, pp 409–417 | Cite as

Sulfur and primary production in aquatic environments: an ecological perspective

  • Alessandra Norici
  • Ruediger Hell
  • Mario Giordano


Sulfur is one of the critical elements in living matter, as it participates in several structural, metabolic and catalytic activities. Photosynthesis is an important process that entails the use of sulfur during both the light and carbon reactions. Nearly half of global photosynthetic carbon fixation is carried out by phytoplankton in the aquatic environment. Aquatic environments are very different from one another with respect to sulfur content: while in the oceans sulfate concentration is constantly high, freshwaters are characterized by daily and seasonal variations and by a wide range of sulfur concentration. The strategies that algal cells adopt for energy and resource allocation often reflect these differences. In the oceans, the amount and chemical form of sulfur has changed substantially during the course of the Earth's history; it is possible that sulfur availability played a role in the evolution of marine phytoplankton communities and it may continue to have appreciable effects on global biogeochemistry and ecology. Phytoplankton is also the main biogenic source of sulfur; sulfur can be released into the atmosphere by algal cells as dimethylsulfide, with possibly important repercussions on global climate. These and related matters are discussed in this review.

Key words

algal metabolism dimethylsulfide evolution nutrients photosynthesis phytoplankton sulfur 









Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. MO Andreae and PJ Crutzen, Atmospheric aerosols: biogeochemical sources and role in atmospheric chemistry. Science 276 (1997) 1052-1058CrossRefGoogle Scholar
  2. JH Ansede, PJ Pellechia and DC Yoch, Nuclear magnetic resonance analysis of [1-13C]dimethylsulfoniopropionate (DMSPP) and [1-13C]acrylate metabolism by a DMSP lyase-producing marine isolate of the α-subclass of Proteobacteria. Appl Environ Microb 67 (2001) 3134-3139CrossRefGoogle Scholar
  3. RK Bambach, AH Knoll and JJ Sepkoski Jr, Anatomical and ecological constraints on Phanerozoic animal diversity in the marine realm. Proc Natl Acad Sci USA 99 (2002) 6854-6859CrossRefPubMedGoogle Scholar
  4. D Bagchi and D Verma, Selenate-regulation of sulfur metabolism in a cyanobacterium, Phormidium uncinatum. J Plant Physiol 150 (1997) 762-764Google Scholar
  5. SB Baines and NS Fisher, Interspecific differences in the bioconcentration of selenite by phytoplankton and their ecological implications. Mar Ecol Prog Ser 213 (2001) 1-12Google Scholar
  6. TS Bates, RP Kiene, GV Wolfe, PA Matrai, FP Chavez, KR Buck, BW Blomquist and RL Cuhel, The cycling of sulfur in surface seawater of northeast Pacific. J Geophys Res 99 (1994) 7835-7843CrossRefGoogle Scholar
  7. J Beardall and M Giordano, Ecological implications of algal CO2 concentrating mechanisms and their regulation. Funct Plant Biol 29 (2002) 333-347CrossRefGoogle Scholar
  8. CM Benkovitz, MT Scholtz, J Pacyna, L Tarrasón, J Dignon, EC Voldner, PA Spiro, JA Logan and TE Graedel, global gridded inventories of anthropogenic emissions of sulfur and nitrogen. J Geophys Res 101 (1996) 29239-29253CrossRefGoogle Scholar
  9. P Brimbelcombe, C Hammer, H Rodhe, A Ryaboshapko and CF Boutron, Human influence on the sulfur cycle. In: P Brimblecombe and AY Lein (eds.) Evolution of the Global Biogeochemical Sulfur Cycle, SCOPE 39. Chichester, UK: Wiley (1989) pp. 77-121Google Scholar
  10. GL Cantoni and DG Anderson, Enzymatic cleavage of dimethylthetin by Polysiphonia lanosa. J Biol Chem 222 (1956) 171-177PubMedGoogle Scholar
  11. JN Cape, D Fowler and A Davison, Ecological effects of sulfur dioxide, fluorides, and minor air pollutants: recent trends and research needs. Environ Int 29 (2003) 201-211CrossRefPubMedGoogle Scholar
  12. RJ Charlson, JE Lovelock, MO Andreae and SG Warren, Oceanic phytoplankton atmospheric sulfur, cloud albedo and climate. Nature 326 (1987) 655-661CrossRefGoogle Scholar
  13. CS Cobbett, Phytochelatins and their roles in heavy metal detoxification. Plant Physiol 123 (2000) 825-832CrossRefPubMedGoogle Scholar
  14. JL Collier, SK Herbert, DC Fork and AR Grossman, Changes in the cyanobacterial photosynthetic apparatus in responses to macronutrient deprivation. Photosynth Res 42 (1994) 173-183CrossRefGoogle Scholar
  15. JWH Dacey and SG Wakeham, Oceanic dimethylsulfide: production during zooplankton grazing on phytoplankton. Science 233 (1986) 1314-1316PubMedGoogle Scholar
  16. JWH Dacey and NV Blough, Hydroxide decomposition of DMSP to form DMS. Geophys Res Lett 14 (1987) 1246-1249Google Scholar
  17. JP Davies, FH Yildiz and AR Grossman, Mutants of Chlamydomonas with aberrant responses to sulfur deprivation. Plant Cell 6 (1994) 53-63CrossRefPubMedGoogle Scholar
  18. JP Davies, FH Yildiz and AR Grossman, Sac1, a putative regulator that is critical for survival of Chlamydomonas reinhardtii during sulfur deprivation. EMBO J 15 (1996) 2150-2159PubMedGoogle Scholar
  19. JP Davies and AR Grossman, Responses to deficiences in macronutrients. In: JD Rochaix, M Goldschmidt-Clermont and S Merchant (eds.) The Molecular Biology of Chloroplasts and Mitochondria in Chlamydomonas. Dordrecht, The Netherlands: Kluwer Academic Publishers (1998) pp. 613-633Google Scholar
  20. JP Davies, FH Yildiz and AR Grossman, Sac3, an SFN1-like serine/threonine kinase that positively and negatively regulates the responses of Chlamydomonas reinhardtii to sulfur deprivation. Plant Cell 11 (1999) 1179-1190CrossRefPubMedGoogle Scholar
  21. JR Dominguez-Solis, MC Lopez-Martin, FJ Ager, M Dolores Ynsa, LC Romero and C Gotor, Increased cysteine availability is essential for cadmium tolerance and accumulation in Arabidopsis thaliana. Plant Biotechnol J 2 (2004) 469-476CrossRefPubMedGoogle Scholar
  22. PG Falkowski and JA Raven, Aquatic photosynthesis. Malden, MA: Blackwell Science (1997).Google Scholar
  23. PG Falkowski, ME Katz, AH Knoll, A Quigg, JA Raven, O Schofield and FJR Taylor, The evolution of modern eukaryotic phytoplankton. Science 305 (2004) 354-360CrossRefPubMedGoogle Scholar
  24. J Farquhar, H Bao and M Thiemens, Atmospheric influence of earth's earliest sulfur cycle. Science 289 (2000) 756-758CrossRefPubMedGoogle Scholar
  25. RMB Ferreira and ARN Teixeira, Sulfur starvation in Lemna leads to degradation of ribulose/bisphosphate carboxylase without plant death. J Biol Chem 267 (1992) 6253-6257Google Scholar
  26. C Field, M Behrenfeld, J Randerson and P Falkowski, Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281 (1998) 237-240CrossRefPubMedGoogle Scholar
  27. R Fleming, The composition of plankton and units for reporting populations and production. Pacific Sci Congr Calif Proc, 6th, 1939 3 (1940) 535-540Google Scholar
  28. Y Gao, OME Schofield and T Leustek, Characterization of sulfate assimilation in marine algae focusing on the enzyme 5'-adenylylsulfate reductase. Plant Physiol 123 (2000) 1087-1096CrossRefPubMedGoogle Scholar
  29. A Gabric, W Gregg, R Najjar, D Erickson and P Matrai, Modeling the biogeochemical cycle of dimethylsulfide in the upper ocean: a review. Glob Change Sci 3 (2001) 377-392CrossRefGoogle Scholar
  30. M Giordano, JS Davis and G Bowes, Organic carbon release by Dunaliella salina (Chlorophyta) under different growth conditions of CO2, nitrogen, and salinity. J Phycol 30 (1994) 249-257CrossRefGoogle Scholar
  31. M Giordano, Adaptation of Dunaliella salina (Volvocales, Chlorophyta) to growth on NH 4 + as the sole N source. Phycologia 36 (1997) 345-350CrossRefGoogle Scholar
  32. M Giordano and G Bowes, Gas exchanges, metabolism, and morphology of Dunaliella salina in response to the CO2 concentration and nitrogen source used for growth. Plant Physiol 115 (1997) 1049-1056PubMedGoogle Scholar
  33. M Giordano, V Pezzoni and R Hell, Strategies for the allocation of resources under sulfur limitation in the green alga Dunaliella salina. Plant Physiol 124 (2000) 857-864CrossRefPubMedGoogle Scholar
  34. M Giordano, Interactions between C and N metabolism in Dunaliella salina cells cultured at elevated CO2 and high N concentrations. J Plant Physiol 158 (2001) 577-581CrossRefGoogle Scholar
  35. M Giordano and R Hell, Mineral nutrition in photolithotrophs: cellular mechanisms and aquatic habitats. Recent Res Dev Plant Physiol 2 (2001) 95-123Google Scholar
  36. M Giordano, A Norici, M Forssen, M Eriksson and JA Raven, An anaplerotic role for the mitochondrial carbonic anhydrase in Chlamydomonas reinhardtii. Plant Physiol 132 (2003) 2126-2134CrossRefPubMedGoogle Scholar
  37. Giordano M, Norici A and Hell R (2005) Sulfur and phytoplankton: acquisition, metabolism and impact on the environment. New Phytol 166, in pressGoogle Scholar
  38. A Grossman and H Takahashi, Macronutrient utilization by photosynthetic eukaryotes and the fabric of interactions. Annu Rev Plant Phys Plant Mol Biol 52 (2001) 163-210CrossRefGoogle Scholar
  39. R Hell, Molecular physiology of plant sulfur metabolism. Planta 202 (1997) 138-148CrossRefPubMedGoogle Scholar
  40. RW Hill, BA White, MT Cottrell and JWH Dacey, Virus-mediated total release of dimethylsulfopropionate from marine phytoplankton: a potential climate process. Aquat Microb Ecol 14 (1998) 1-6Google Scholar
  41. TY Ho, A Quigg, ZV Finkel, AJ Milligan, K Wyman, PG Falkowski and FMM Morel, The elemental composition of some marine phytoplankton. J Phycol 39 (2003) 1145-1159CrossRefGoogle Scholar
  42. M Holmer and P Storkholm, Sulphate reduction and sulphur cycling in lake sediments: a review. Freshwater Biol 46 (2001) 431-451CrossRefGoogle Scholar
  43. GE Hutchinson, A Treatise on Limnology. New York, NY: Wiley (1971).Google Scholar
  44. SB Jonnalagadda and PVV Prasada Rao, Toxicity, bioavailability and metal speciation. Comparative Biochem Physiol Part C: Pharmacol Toxicol Endocrinol 106 (1993) 585-595CrossRefGoogle Scholar
  45. LC Kah, TW Lyons and TD Frank, Low marine sulphate and protracted oxygenation of the proterozoic biosphere. Nature 431 (2004) 834-838CrossRefPubMedGoogle Scholar
  46. N Kasamatsu, T Hirano, S Kudoh, T Odate and M Fukuchi, Dimethylsulfoniopropionate production by psychrophilic diatom isolates. J Phycol 40 (2004) 874-878CrossRefGoogle Scholar
  47. MD Keller, Dimethylsulfide production and marine phytoplankton. The importance of species composition and cell size. Biol Oceanogr 6 (1991) 375-382Google Scholar
  48. AJ Kettle and MO Andreae, Flux of dimethylsulfide from the oceans: a comparison of updates data sets and flux models. J Geophys Res 105 (2000) 26793-26808CrossRefGoogle Scholar
  49. RP Kiene and TS Bates, Biological removal of dimethylsulfide from seawater. Nature 345 (1990) 702-705CrossRefGoogle Scholar
  50. A Kleeberg, Interactions between bentic phosphorus release and sulfur cycling in Lake Scharmützelsee (Germany). Water Air Soil Poll 99 (1997) 391-399CrossRefGoogle Scholar
  51. A Kleeberg and GE Dudel, Changes in extent of phosphorus release in a shallow lake (Lake Grosser Müggelsee; Germany, Berlin) due to climatic factors and load. Mar Geol 139 (1997) 61-75CrossRefGoogle Scholar
  52. S Kopriva, M Suter, P Ballmoos von, H Hesse, U Krähenbühl, H Rennenberg and C Brunold, Interaction of sulfate assimilation with carbon and nitrogen metabolism in Lemna minor. Plant Physiol 130 (2002) 1406-1413CrossRefPubMedGoogle Scholar
  53. S Kristiansen and BA Lund, Nitrogen cycling in the Barents Sea-I. Uptake of nitrogen in the water column. Deep-Sea Res 36 (1989) 255-268CrossRefGoogle Scholar
  54. C Leck, U Larsson, LE Gander, S Johansson and S Hajdu, DMS in the Baltic Sea – annual variability in relation to biological society. J Geophys Res 95 (1990) 3353-3363Google Scholar
  55. T Leustek and K Saito, Sulfate transport and assimilation in plants. Plant Physiol 120 (1999) 637-643PubMedGoogle Scholar
  56. T Leustek, MN Martin, J-A Bick and JP Davies, Pathways and regulation of sulfur metabolism revealed through molecular and genetic studies. Annu Rev Plant Physiol Plant Mol Biol 51 (2000) 141-165CrossRefPubMedGoogle Scholar
  57. JW Lilly, JE Maul and DB Stern, The Chlamydomonas reinhardtii organellar genomes respond transcriptionally and post-transcriptionally to abiotic stimuli. Plant Cell 14 (2002) 2681-2706CrossRefPubMedGoogle Scholar
  58. JE Lovelock and L Margulis, Atmospheric homeostasis by and for the biosphere:the Gaia hypothesis. Tellus 26 (1974) 2-10CrossRefGoogle Scholar
  59. JE Lovelock, RJ Mags and RA Rasmussen, Atmospheric dimethylsulfide and the natural sulfur cycle. Nature 237 (1972) 452-453CrossRefGoogle Scholar
  60. SC Maberly, L King, CE Gibson, L May, RI Jones, MM Dent and C Jordan, Linking nutrient limitation and water chemistry in upland lakes to catchment characteristics. Hydrobiologia 506–509 (2003) 83-91CrossRefGoogle Scholar
  61. G Malin, Sulphur, climate and the microbial maze. Nature 387 (1998) 857-859CrossRefGoogle Scholar
  62. PA Matrai and MD Keller, Dimethylsulfide in a large-scale coccolitophore bloom in the Gulf of Maine. Cont Shelf Res 13 (1993) 831-843CrossRefGoogle Scholar
  63. S Mosulén, MJ Dominuez, J Vigara, C Vilchez, A Guiraum and JM Vega, Metal toxicity in Chlamydomonas reinhardtii. Effect on sulfate and nitrate assimilation. Biomol Eng 20 (2003) 199-203CrossRefPubMedGoogle Scholar
  64. TE Murray, The correlation between iron sulfide precipitation and hypolimnetic phosphorus accumulation during one summer in a softwater lake. Can J Fish Aquat Sci 52 (1995) 1190-1194CrossRefGoogle Scholar
  65. T Niki, M Kunugi and A Otsuki, DMSP-lyase activity in five marine phytoplankton species: its potential importance in DMS production. Mar Biol 136 (2000) 759-764CrossRefGoogle Scholar
  66. PM Neumann, MP Souza De, IJ Pickerung and N Terry, Rapid microalgal metabolism of selenate to volatile dimethylselenide. Plant Cell Environ 26 (2003) 897-905CrossRefPubMedGoogle Scholar
  67. G Noctor, L Gomez, H Vanacker and CH Foyer, Interactions between biosynthesis, compartmentation and transport in the control of glutathione homeostasis and signaling. J Exp Bot 53 (2002) 1283-1304CrossRefPubMedGoogle Scholar
  68. M Novàk, SH Bottrell and E Prechova, Sulfur isotope inventories of atmospheric deposition, spruce forest floor and living Sphagnum along a NW-SE transect across Europe. Biogeochemistry 53 (2001) 23-50CrossRefGoogle Scholar
  69. GK Nürnberg, Comment: Phosphorus budgets and stoichiometry during the open-water season in two unmanipulated lakes in the experimental lakes area, northwestern Ontario. Can J Fish Aquat Sci 53 (1996) 1469-1471CrossRefGoogle Scholar
  70. A Norici, A Dalsass and M Giordano, Role of phosphoenolpyruvate carboxylase in anaplerosis in the green microalga Dunaliella salina cultured under different nitrogen regimes. Physiol Plantarum 116 (2002) 186-191CrossRefPubMedGoogle Scholar
  71. T Obata, H Araic and Y Shiraiwa, Bioconcentration mechanism of selenium by coccolithophorid, Emiliania huxleyi. Plant Cell Physiol 45 (2004) 1434-1441CrossRefPubMedGoogle Scholar
  72. RS Ogle and AW Knight, Selenium bioaccumulation in aquatic ecosystems: 1. Effects of sulfate on the uptake and toxicity of selenate in Daphnia magna. Arch Environ Con Tox 30 (1996) 274-279CrossRefGoogle Scholar
  73. T Ohizumi, N Fukuzaki and M Kusakabe, Sulfur isotopic view on the sources of sulfur in atmospheric fallout along the coast of the Sea of Japan. Atmos Environ 31 (1997) 1339-1348CrossRefGoogle Scholar
  74. A Paytan, M Kastner, D Campbell and MH Thiemens, Sulfur isotopic composition of cenozoic seawater sulfate. Science 282 (1998) 1459-1462CrossRefPubMedGoogle Scholar
  75. C Petaloti, D Voutsa, C Samara, M Sofoniou, I Stratis and T Kouimtzis, Nutrient dynamics in shallow lakes of northern Greece. Environ Sci Pollut Res Int 11 (2004) 11-17PubMedCrossRefGoogle Scholar
  76. T Pfannschmidt, Chloroplast redox signals: how photosynthesis controls its own genes. Trends Plant Sci 8 (2003) 33-41CrossRefPubMedGoogle Scholar
  77. MEQ Pilson, An introduction to the chemistry of the sea. Upper Saddle River, USA: Prentice-Hall (1998).Google Scholar
  78. SW Poulton, PW Fralick and DE Canfield, The transition to a sulphidic ocean ˜1.84 billion years ago. Nature 431 (2004) 173-177CrossRefPubMedGoogle Scholar
  79. NM Price, WP Cochlan and PJ Harrison, Time course of uptake of inorganic and organic nitrogen by phytoplankton in the Strait of Georgia: comparison of frontal and stratified communities. Mar Ecol Prog Ser 27 (1985) 39-53Google Scholar
  80. A Ramaiah and ERB Shanmugasundaram, Effect of sulphur compounds on the uptake of molybdenum by Neurospora Crassa. Biochim Biophys Acta 60 (1962) 386-392CrossRefPubMedGoogle Scholar
  81. JA Raven, Carbon a phycocentric view. In: GT Evans and MJR Fasham (eds.) Towards a Model of Ocean Biogeochemical Processes. Berlin, Germany: Springer-Verlag (2004) pp. 123-132Google Scholar
  82. AC Redfield, BH Ketchum and FA Richards, The influence of organisms on the composition of seawater. In: MN Hill (ed.) The Sea. New York: Interscience (1963) pp. 26-77Google Scholar
  83. GF Riedel and JG Sanders, The influence of pH and media composition on the uptake of inorganic selenium by Chlamydomonas reinhardtii. Environ Toxic Chem 15 (1996) 1577-1583CrossRefGoogle Scholar
  84. GF Riedel, JG Sanders and CC Gilmour, Uptake, transformation, and impact of selenium in freshwater phytoplankton and bacterioplankton communities. Aquat Microb Ecol 11 (1996) 43-51Google Scholar
  85. WR Riekhof, ME Ruckle, TA Lydic, BB Sears and C Benning, The sulfolipids 2'-O-acyl-sulfoquinovosyldiacylglycerol and sulfoquinovosyldiacylglycerol are absent from a Chlamydomonas reinhardtii mutant deleted in SQD1. Plant Physiol 133 (2003) 864-874CrossRefPubMedGoogle Scholar
  86. GJ Roelofs, J Lelieveld and L Ganzeveld, Simulation of global sulfate distribution and the influence on effective cloud drop radii with a coupled phytochemistry-sulfur cycle model. Tellus 50B (1998) 224-242Google Scholar
  87. GJ Roelofs, P Kasibhatla, L Barrie, D Bergmann, C Bridgeman, M Chin, J Christensen, R Easter, J Feichter, A Jeuken, E Kjellström, D Koch, C Land, U Lohmann and P Rasch, Analysis of regional budgets of sulfur species modeled for the COSAM exercise. Tellus 53B (2001) 673-694Google Scholar
  88. K Saito, Regulation of sulfate transport and synthesis of sulfur containing amino acids. Curr Opin Plant Biol 3 (2000) 188-195PubMedGoogle Scholar
  89. K Saito, Sulfur assimilatory metabolism. The long and smelling road. Plant Physiol 136 (2004) 2443-2450CrossRefPubMedGoogle Scholar
  90. N Sato, Roles of the acidic lipids sulfoquinosovyl diacylglycerol and phosphatidylglycerol in photosynthesis: their specificity and evolution. J Plant Res 117 (2004) 495-505CrossRefPubMedGoogle Scholar
  91. CE Schlekat, B-G Lee and SN Luoma, Assimilation of selenium from phytoplankton by three benthic invertebrtes: effect of phytoplankton species. Mar Ecol Prog Ser 237 (2002) 79-85Google Scholar
  92. JM Seiburth, Acrylic acid, an 'antibiotic' principle in Phaeocystis blooms in Antarctic waters. Science 132 (1960) 676-677PubMedGoogle Scholar
  93. A Setya, M Murillo and T Leustek, Sulfate reduction in higher plants: molecular evidence for a novel 5'-adenylylsulfate reductase. Proc Natl Acad Sci USA 93 (1996) 13383-13388CrossRefPubMedGoogle Scholar
  94. EB Sheets and D Rhodes, Determination of DMSP and other onium compounds on Tetraselmis subcordiformis by plasma desorption mass spectrometry. In: RP Kiene, PT Visscher, MD Keller and GO Kirst (eds.) Biological and Environmental Chemistry of DMSP and Related Sulfonium Compounds. New York: Plenum Press (1996) pp. 317-324Google Scholar
  95. Y Shen, AH Knoll and MR Walter, Evidence for low sulphate and anoxia in a mid-Proterozoic marine basin. Nature 423 (2003) 632-635CrossRefPubMedGoogle Scholar
  96. M Søndergaard, J Windolf and E Jeppesen, Phosphorus fractions and profiles in the sediment of shallow Danish lakes as related to phosphorus load, sediment composition and lake chemistry. Water Res 30 (1996) 992-1002CrossRefGoogle Scholar
  97. J Stefels and L Dijkhuizen, Characteristics of DMSP-lyase in Phaeocystis sp. (Prymnesiophyceae). Mar Ecol Prog Ser 131 (1996) 307-313Google Scholar
  98. M Steinke and GO Kirst, Enzymatic cleavage of dimethylsulfonioproprionate (DMSP) in cell-free exctracts of the marine macroalgae Enteromorpha clathrata (Roth) Grev. (Ulvales, Chlorophyta). J Exp Mar Biol Ecol 210 (1996) 73-85CrossRefGoogle Scholar
  99. M Steinke, C Daniel and GO Kirst, DMSP lyase in marine macro- and microalgae. In: RP Kiene, PT Visscher, MD Keller and GO Kirst (eds.) Biological and Environmental Chemistry of DMSP and Related Sulfonium Compounds. New York: Plenum Press (1996) pp. 317-324Google Scholar
  100. M Steinke, GV Wolfe and GO Kirst, Partial characterization of dimethylsulfoniopropionate (DMSP) lyase in 6 strains of Emiliania huxleyi. Mar Ecol Prog Ser 175 (1998) 215-225Google Scholar
  101. M Steinke, G Malin and PS Liss, Trophic interactions in the sea: an ecological role for climate relevant volatiles?. J Phycol 38 (2002a) 630-638CrossRefGoogle Scholar
  102. M Steinke, G Malin, SD Archer, PH Burkill and PS Liss, DMS production in a coccolithophorid bloom: evidence for the importance of dinoflagellate DMSP lyases. Aquat Microb Ecol 26 (2002b) 259-270Google Scholar
  103. M Steinke, G Malin, WG Stuart and PH Burkill, Vertical and temporal variability of DMSP lyase activity in a coccolithophorid bloom in the northern North Sea. Deep-Sea Res Part II: Topical Studies in Oceanography 49 (2002c) 3001-3016CrossRefGoogle Scholar
  104. JL Stoddard, DS Jeffries, A Lukewille, TA Clair, PJ Dillon, CT Driscoll, M Forsius, M Johannessen, JS Kahl and JH Kellog, Regional trends in aquatic recovery from acidification in North America and Europe. Nature 401 (1999) 575-578CrossRefGoogle Scholar
  105. H Strauss, The isotopic composition of sedimentary sulfur through time. Paleogeogr Paleocl Paleoecol 132 (1997) 97-118CrossRefGoogle Scholar
  106. S Strom, G Wolfe, J Holmes, H Stecher, C Shimeneck, S Lambert and E Moreno, Chemical defense in the microplankton II: feeding and growth rates of heterotrophic protists on the DMS-producing phytoplankter Emilianai huxleyi. Limnol Oceanogr 48 (2003a) 217-229CrossRefGoogle Scholar
  107. S Strom, G Wolfe, A Slajer, S Lambert and J Clough, Chemical defense in the microplankton II: inhibition of protist feeding by β-dimethylsulfonioproprionate (DMSP). Limnol Oceanogr 48 (2003b) 230-237CrossRefGoogle Scholar
  108. W Sunda, DJ Kieber, RP Kiene and S Huntsman, An antioxidant function for DMSP and DMS in marine algae. Nature 418 (2002) 317-320CrossRefPubMedGoogle Scholar
  109. H Takahashi, CE Braby and AR Grossman, Sulfur economy and cell wall biosynthesis during sulfur limitation of Chlamydomonas reinhardtii. Plant Physiol 127 (2001) 665-673CrossRefPubMedGoogle Scholar
  110. KW Tang, Dynamics of dimethylsulfoproprionate (DMSP) in a migratory grazer: a laboratory simulation study. J Exp Mar Biol Ecol 243 (2000) 283-293CrossRefGoogle Scholar
  111. E Tipping, TR Carrick, MA Hurley, JB James, AJ Lawlor, S Lofts, E Rigg, DW Sutcliffe and C Woof, Reversal acidification in upland waters of the English lake district. Environ Poll 103 (1998) 143-151CrossRefGoogle Scholar
  112. C Trossat, B Rathinasabapathi, EA Weretilnyk, TL Shen, ZH Huang, DA Gage and AD Hanson, Salinity promotes accumulation of 3-dimethylsulfoniopropionate and its precursor S-methylmethionine in chloroplasts. Plant Physiol 116 (1998) 165-171CrossRefPubMedGoogle Scholar
  113. JW Tweedie and IH Segel, Specificity of transport processes for sulfur, selenium, and molybdenum anions by filamentous fungi. Biochim Biophys Acta 196 (1970) 95-106PubMedGoogle Scholar
  114. JH Vandermeulen and A Foda, Cycling of selenite and selenate in marine phytoplankton. Mar Biol 98 (1988) 115-123CrossRefGoogle Scholar
  115. PG Verità and V Smetacek, Organism life cycles, predation, and the structure of marine pelagic ecosystems. Mar Ecol Prog Ser 130 (1996) 277-293Google Scholar
  116. GJ Vermeij, The Mesozoic marine revolution: evidence from snails, predators and grazers. Paleobiology 3 (1977) 245-258Google Scholar
  117. Wakeham SG and Dacey JWH (1989) Biogeochemical cycling of dimethylsulfide in marine environments. In: Saltzman ES, Cooper WJ (eds) Biogenic sulfur in the environment. Am Chem Soc Symp Ser 89: 293–296Google Scholar
  118. RG Wetzel, Limnology. Philadelphia, PA: Saunders (1983).Google Scholar
  119. E Wheeler, RA Zingaro, ER Cox, KJ Irgolic and NR Bottino, The Effect of selenate, selenite and sulfate on the growth of six unicellular marine algae. J Exp Mar Biol Ecol 57 (1982) 181-194CrossRefGoogle Scholar
  120. GV Wolfe, M Steinke and GO Kirst, Grazing-activated chemical defence in a unicellular marine alga. Nature 387 (1997) 894-897CrossRefGoogle Scholar
  121. GV Wolfe, SL Strom, JL Holmes, T Radzio and MB Olson, Dimethylsulfoniopropionate cleavage by marine phytoplankton in response to mechanical, chemical, or dark stress. J Phycol 38 (2002) 948-960CrossRefGoogle Scholar
  122. DD Wykoff, JP Davies, A. Melis and AR Grossman, The regulation of photosynthetic electron transport during nutrient deprivation in Chlamydomonas reinhardtii. Plant Physiol 117 (1998) 129-139CrossRefPubMedGoogle Scholar
  123. DC Yoch, JH Ansede and KS Rabinowitz, Evidence for intracellular and extracellular dimethylsulfoniopropionate (DMSP) lyases and DMSP uptake sites in two species of marine bacteria. Appl Environ Microb 63 (1997) 3182-3188Google Scholar
  124. DC Yoch, Dimethyldulfoniopropionate: its source, role in the marine food web, and biological degradation to dimethylsulfide. Appl Environ Microb 68 (2002) 5804-5815CrossRefGoogle Scholar
  125. L Zhang, T Happe and A Melis, Biochemical and morphological characterization of sulfur-deprived and H2-producing Chlamydomonas reinhardtii (green alga). Planta 214 (2002) 552-561CrossRefPubMedGoogle Scholar
  126. Z Zhang, J Shrager, M Jain, CW Chang, O Vallon and A Grossman, Insights into the survival of Chlamydomonas reinhardtii during sulfur starvation based on microarray analysis of gene expression. Eukaryotic cell 3 (2004) 1331-1348CrossRefPubMedGoogle Scholar
  127. FJ Zhao, B Spiro, PR Poulton and SP McGrath, Use of sulfur isotope ratios to determine anthropogenic sulfur signals in a grassland ecosystem. Environ Science Technol 32 (1998) 2288-2291CrossRefGoogle Scholar

Copyright information

© Springer 2005

Authors and Affiliations

  • Alessandra Norici
    • 1
  • Ruediger Hell
    • 2
  • Mario Giordano
    • 1
  1. 1.Dipartimento di Scienze del Mare, Laboratorio di Fisiologia AlgaleUniversità Politecnica delle MarcheAnconaItaly
  2. 2.Department of Molecular Biology of Plants, Heidelberg Institute of Plant SciencesUniversity of HeidelbergHeidelbergGermany

Personalised recommendations