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Environmental problems - Chemical approaches
RESEARCH ARTICLE

Role of dimethylsulfoniopropionate as an osmoprotectant following gradual salinity shifts in the sea-ice diatom Fragilariopsis cylindrus

Barbara R. Lyon A B C E , Jennifer M. Bennett-Mintz A C , Peter A. Lee A C , Michael G. Janech B C D and Giacomo R. DiTullio A B C
+ Author Affiliations
- Author Affiliations

A Hollings Marine Lab, 331 Fort Johnson Road, Charleston, SC 29412, USA.

B Marine Biomedicine and Environmental Sciences Center, Medical University of South Carolina, 217 Fort Johnson Road, Charleston, SC 29412, USA.

C Grice Marine Laboratory, College of Charleston, 205 Fort Johnson Road, Charleston, SC 29412, USA.

D Division of Nephrology, Department of Medicine, Medical University of South Carolina, 96 Jonathan Lucas Street, Charleston, SC 29425, USA.

E Corresponding author. Present address: Coastal Studies Center, Biology Department, Bowdoin College, 6500 College Station, Brunswick, ME 04011, USA. Email: blyon@bowdoin.edu

Environmental Chemistry 13(2) 181-194 https://doi.org/10.1071/EN14269
Submitted: 16 December 2014  Accepted: 27 September 2015   Published: 7 January 2016

Environmental context. Dimethylsulfoniopropionate (DMSP), a small sulfur compound biosynthesised by algae, plays an important role in global climate, particularly in polar regions. We investigated salinity effects on DMSP levels, and provide the first experimental measurements of DMSP and associated physiological changes in a polar diatom across to a range of gradual salinity shifts representative of sea-ice conditions. Quantitative estimates of DMSP in polar diatoms following salinity changes will facilitate new mathematical models to predict seasonal responses and reactions to climate change.

Abstract. Although extreme environmental gradients within sea-ice have been proposed to stimulate dimethylsulfoniopropionate (DMSP) accumulation in diatoms, a taxa whose temperate counterparts show relatively low concentrations, this has yet to be experimentally validated across a range of salinities representative of sea-ice conditions. The present study examined changes in DMSP concentrations in the widespread polar diatom Fragilariopsis cylindrus in response to gradual salinity shifts representative of those encountered during sea-ice formation and melt. DMSP concentrations were elevated up to 127 % in 70-salinity cultures. Low-salinity shifts decreased intracellular DMSP concentrations in a gradient-dependent manner that suggests DMSP recycling rather than release under milder hyposalinity shifts. Permeable membranes were detected in ~45 % of 10-salinity cells; therefore, loss of membrane integrity may only partially explain DMSP release in the lowest-salinity group. Growth rates, photosynthetic efficiency of photosystem II and reactive oxygen species detection indicated only partial impairment by salinity stress in this organism. Thus, experimental evidence supports the role of DMSP as a compatible solute in the acclimation of a sea-ice diatom across large salinity gradients and measurements of associated physiological changes will improve interpretation of environmental measurements.

Additional keywords: DMSO, DMSP, FV/FM, membrane permeability, polar algae, reactive oxygen species, sulfur.


References

[1]  R. J. Charlson, J. E. Lovelock, M. O. Andreae, S. G. Warren, Oceanic phytoplankton, atmospheric sulphur, cloud albedo and climate. Nature 1987, 326, 655.
Oceanic phytoplankton, atmospheric sulphur, cloud albedo and climate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXitVWgsb8%3D&md5=8a4e47b6c58aead2ad82d0f3209a72f9CAS |

[2]  J. R. Gunson, S. A. Spall, T. R. Anderson, A. Jones, I. J. Totterdell, M. J. Woodage, Climate sensitivity to ocean dimethylsulphide emissions. Geophys. Res. Lett. 2006, 33, L07701.
Climate sensitivity to ocean dimethylsulphide emissions.Crossref | GoogleScholarGoogle Scholar |

[3]  P. K. Quinn, T. S. Bates, The case against climate regulation via oceanic phytoplankton sulphur emissions. Nature 2011, 480, 51.
The case against climate regulation via oceanic phytoplankton sulphur emissions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFGku73O&md5=a6a9f1e16b620d07e88e24248c16b778CAS | 22129724PubMed |

[4]  P. A. Matrai, M. C. Vernet, Dynamics of the vernal bloom in the marginal ice zone of the Barents Sea: dimethyl sulfide and dimethylsulfoniopropionate budgets. J. Geophys. Res. 1997, 102, 22 965.
Dynamics of the vernal bloom in the marginal ice zone of the Barents Sea: dimethyl sulfide and dimethylsulfoniopropionate budgets.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXntlGjsrg%3D&md5=94d3e60f6fd6da0cbc2d667873e4c170CAS |

[5]  G. R. DiTullio, W. O. Smith, Relationship between dimethylsulfide and phytoplankton pigment concentrations in the Ross Sea, Antarctica. Deep Sea Res. Part I Oceanogr. Res. Pap. 1995, 42, 873.
Relationship between dimethylsulfide and phytoplankton pigment concentrations in the Ross Sea, Antarctica.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXovFehsLo%3D&md5=73bc7edce602d17c8dfb207ef177ff36CAS |

[6]  Y. Inomata, M. Hayashi, K. Osada, Y. Iwasaka, Spatial distributions of volatile sulfur compounds in surface seawater and overlying atmosphere in the north-western Pacific Ocean, eastern Indian Ocean, and Southern Ocean. Global Biogeochem. Cycles 2006, 20, GB2022.
Spatial distributions of volatile sulfur compounds in surface seawater and overlying atmosphere in the north-western Pacific Ocean, eastern Indian Ocean, and Southern Ocean.Crossref | GoogleScholarGoogle Scholar |

[7]  M. A. J. Curran, G. B. Jones, Dimethyl sulfide in the Southern Ocean: seasonality and flux. J. Geophys. Res. – Oceans 2000, 105, 20 451.
Dimethyl sulfide in the Southern Ocean: seasonality and flux.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXmslShurg%3D&md5=153f76866f6837113a745989b40190a9CAS |

[8]  G. R. DiTullio, D. L. Garrison, S. Mathot, Dimethylsulfonioproprionate in sea ice algae from the Ross Sea polynya, in Antarctic Sea Ice: Biological Processes, Interactions and Variability (Eds K. R. Arrigo, M. P. Lizotte) 1998, pp. 139–146 (American Geophysical Union: Washington, DC).

[9]  A. J. Trevena, G. B. Jones, Dimethylsulphide and dimethylsulphoniopropionate in Antarctic sea ice and their release during sea ice melting. Mar. Chem. 2006, 98, 210.
Dimethylsulphide and dimethylsulphoniopropionate in Antarctic sea ice and their release during sea ice melting.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjsF2mug%3D%3D&md5=26ecd7ad536ec9432073b186c51ed1b6CAS |

[10]  A. J. Trevena, G. B. Jones, S. W. Wright, R. L. van den Enden, Profiles of DMSP, algal pigments, nutrients and salinity in pack ice from eastern Antarctica. J. Sea Res. 2000, 43, 265.
Profiles of DMSP, algal pigments, nutrients and salinity in pack ice from eastern Antarctica.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXms1Wrtbk%3D&md5=1b8491dca9cccf64a71698ac44888fc5CAS |

[11]  G. O. Kirst, C. Thiel, H. Wolff, J. Nothnagel, M. Wanzek, R. Ulmke, Dimethylsulfoniopropionate (DMSP) in ice-algae and its possible biological role. Mar. Chem. 1991, 35, 381.
Dimethylsulfoniopropionate (DMSP) in ice-algae and its possible biological role.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XotVSrsw%3D%3D&md5=673384fbb10fa549b92b395d81d5a1c7CAS |

[12]  P. A. Lee, S. J. De Mora, M. Gosselin, M. Levasseur, R. Bouillon, C. Nozais, C. Michel, Particulate dimethylsulfoxide in Arctic sea-ice algal communities: the cryoprotectant hypothesis revisited. J. Phycol. 2001, 37, 488.
Particulate dimethylsulfoxide in Arctic sea-ice algal communities: the cryoprotectant hypothesis revisited.Crossref | GoogleScholarGoogle Scholar |

[13]  M. Levasseur, A new source of dimethylsulfide (DMS) for the Arctic atmosphere: ice diatoms. Mar. Biol. 1994, 121, 381.
A new source of dimethylsulfide (DMS) for the Arctic atmosphere: ice diatoms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXktVakurs%3D&md5=8805963d1e368f86f4ac7e420634688dCAS |

[14]  A. J. Trevena, G. B. Jones, S. W. Wright, R. L. van den Enden, Profiles of dimethylsulphoniopropionate (DMSP), algal pigments, nutrients, and salinity in the fast ice of Prydz Bay, Antarctica. J. Geophys. Res. –Oceans 2003, 108, 3145.
Profiles of dimethylsulphoniopropionate (DMSP), algal pigments, nutrients, and salinity in the fast ice of Prydz Bay, Antarctica.Crossref | GoogleScholarGoogle Scholar |

[15]  F. Brabant, S. El Amri, J. L. Tison, A robust approach for the determination of dimethylsulfoxide in sea ice. Limnol. Oceanogr. Methods 2011, 9, 261.
A robust approach for the determination of dimethylsulfoxide in sea ice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFWrt7zO&md5=cfde17185e45b1fc2876e52c10d97447CAS |

[16]  R. Kiene, D. Kieber, D. Slezak, D. Toole, D. del Valle, J. Bisgrove, J. Brinkley, A. Rellinger, Distribution and cycling of dimethylsulfide, dimethylsulfoniopropionate, and dimethylsulfoxide during spring and early summer in the Southern Ocean south of New Zealand. Aquat. Sci. 2007, 69, 305.
Distribution and cycling of dimethylsulfide, dimethylsulfoniopropionate, and dimethylsulfoxide during spring and early summer in the Southern Ocean south of New Zealand.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1ajtrvK&md5=000967f46b0118c49f36626b3af31276CAS |

[17]  H. J. Zemmelink, L. Houghton, J. W. H. Dacey, A. P. Worby, P. S. Liss, Emission of dimethylsulfide from Weddell Sea leads. Geophys. Res. Lett. 2005, 32, L23610.
Emission of dimethylsulfide from Weddell Sea leads.Crossref | GoogleScholarGoogle Scholar |

[18]  H. J. Zemmelink, J. W. H. Dacey, L. Houghton, E. J. Hintsa, P. S. Liss, Dimethylsulfide emissions over the multi-year ice of the western Weddell Sea. Geophys. Res. Lett. 2008, 35, L06603.
Dimethylsulfide emissions over the multi-year ice of the western Weddell Sea.Crossref | GoogleScholarGoogle Scholar |

[19]  E. C. Asher, J. W. H. Dacey, M. M. Mills, K. R. Arrigo, P. D. Tortell, High concentrations and turnover rates of DMS, DMSP and DMSO in Antarctic sea ice. Geophys. Res. Lett. 2011, 38, L23609.
High concentrations and turnover rates of DMS, DMSP and DMSO in Antarctic sea ice.Crossref | GoogleScholarGoogle Scholar |

[20]  J. L. Tison, F. Brabant, I. Dumont, J. Stefels, High-resolution dimethyl sulfide and dimethylsulfoniopropionate time series profiles in decaying summer first-year sea ice at Ice Station Polarstern, western Weddell Sea, Antarctica. J. Geophys. Res. Biogeosci. 2010, 115, G04044.
High-resolution dimethyl sulfide and dimethylsulfoniopropionate time series profiles in decaying summer first-year sea ice at Ice Station Polarstern, western Weddell Sea, Antarctica.Crossref | GoogleScholarGoogle Scholar |

[21]  A. J. Gabric, J. M. Shephard, J. M. Knight, G. Jones, A. J. Trevena, Correlations between the satellite-derived seasonal cycles of phytoplankton biomass and aerosol optical depth in the Southern Ocean: evidence for the influence of sea ice. Global Biogeochem. Cy 2005, 19, 1.
Correlations between the satellite-derived seasonal cycles of phytoplankton biomass and aerosol optical depth in the Southern Ocean: evidence for the influence of sea ice.Crossref | GoogleScholarGoogle Scholar |

[22]  M. D. Keller, W. K. Bellows, R. R. L. Guillard, Dimethyl sulfide production in marine phytoplankton, in Biogenic Sulfur in the Environment (Eds E. S. Saltzman, W. J. Cooper) 1989, pp. 131–142 (American Chemical Society: Washington, DC).

[23]  G. O. Kirst, C. Wiencke, Ecophysiology of polar algae. J. Phycol. 1995, 31, 181.
Ecophysiology of polar algae.Crossref | GoogleScholarGoogle Scholar |

[24]  P. J. Ralph, K. G. Ryan, A. Martin, G. Fenton, Melting out of sea ice causes greater photosynthetic stress in algae than freezing in. J. Phycol. 2007, 43, 948.
Melting out of sea ice causes greater photosynthetic stress in algae than freezing in.Crossref | GoogleScholarGoogle Scholar |

[25]  P. Sudhir, S. D. S. Murthy, Effects of salt stress on basic processes of photosynthesis. Photosynthetica 2004, 42, 481.
Effects of salt stress on basic processes of photosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhsVOmtbw%3D&md5=e541dfbf91c2eb8fa08641d5b4562112CAS |

[26]  G. O. Kirst, Salinity tolerance of eukaryotic marine algae. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1989, 40, 21.

[27]  J. Stefels, Physiological aspects of the production and conversion of DMSP in marine algae and higher plants. J. Sea Res. 2000, 43, 183.
Physiological aspects of the production and conversion of DMSP in marine algae and higher plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXms1Wrtb4%3D&md5=469bb7bdecf693cb9625a3b2f0733d0eCAS |

[28]  A. Vairavamurthy, M. O. Andreae, R. L. Iverson, Biosynthesis of dimethylsulfide and dimethylpropiothetin by Hymenomonas carterae in relation to sulfur source and salinity variations. Limnol. Oceanogr. 1985, 30, 59.
Biosynthesis of dimethylsulfide and dimethylpropiothetin by Hymenomonas carterae in relation to sulfur source and salinity variations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXht1ymtb4%3D&md5=682315de129847b83cd81d6e0a4524d0CAS |

[29]  T. Gröne, G. O. Kirst, Aspects of dimethylsulfoniopropionate effects on enzymes isolated from the marine phytoplankter Tetraselmis subcordiformis (Stein). J. Plant Physiol. 1991, 138, 85.
Aspects of dimethylsulfoniopropionate effects on enzymes isolated from the marine phytoplankter Tetraselmis subcordiformis (Stein).Crossref | GoogleScholarGoogle Scholar |

[30]  W. Sunda, D. J. Kieber, R. P. Kiene, S. Huntsman, An antioxidant function for DMSP and DMS in marine algae. Nature 2002, 418, 317.
An antioxidant function for DMSP and DMS in marine algae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XltlGms7k%3D&md5=9739188bf4b6c7f9a6c07626d8632cb2CAS | 12124622PubMed |

[31]  D. J. Kieber, C. E. Spiese, R. P. Kiene, C. Liu, Direct DMS and DMSO production from DMSP reactions with reactive oxygen species, in ASLO 2011 : Aquatic Sciences Meeting, 13–18 February 2011, San Juan, Puerto Rico 2011 (American Society for Limnology and Oceanography). Available at https://www.sgmeet.com/aslo/sanjuan2011/viewabstract2.asp?AbstractID=8532 [Verified 9 November 2015].

[32]  R. Waditee, N. H. Bhuiyan, E. Hirata, T. Hibino, Y. Tanaka, M. Shikata, T. Takabe, Metabolic engineering for betaine accumulation in microbes and plants. J. Biol. Chem. 2007, 282, 34 185.
Metabolic engineering for betaine accumulation in microbes and plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlSltrvM&md5=b69f069255afce86dee5672e561c02f1CAS |

[33]  A. Cosquer, V. Pichereau, J. A. Pocard, J. Minet, M. Cormier, T. Bernard, Nanomolar levels of dimethylsulfoniopropionate, dimethylsulfonioacetate, and glycine betaine are sufficient to confer osmoprotection to Escherichia coli. Appl. Environ. Microbiol. 1999, 65, 3304.
| 1:CAS:528:DyaK1MXltVOlsro%3D&md5=2f570c338df649ead55b5204309d0ec5CAS | 10427011PubMed |

[34]  D. M. Dickson, R. G. Wyn Jones, J. Davenport, Steady state osmotic adaptation in Ulva lactuca. Planta 1980, 150, 158.
Steady state osmotic adaptation in Ulva lactuca.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXmtlGnsL4%3D&md5=76d37274e2ce83ea75e38787cd34c789CAS | 24306591PubMed |

[35]  D. M. J. Dickson, G. O. Kirst, Osmotic adjustment in marine eukaryotic algae: the role of inorganic ions, quaternary ammonium, tertiary sulphonium and carbohydrate solutes. 1. Diatoms and a rhodophyte. New Phytol. 1987, 106, 645.
Osmotic adjustment in marine eukaryotic algae: the role of inorganic ions, quaternary ammonium, tertiary sulphonium and carbohydrate solutes. 1. Diatoms and a rhodophyte.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXlslagt7k%3D&md5=4a3bac3815949774a99f9b7e07caece9CAS |

[36]  S. Van Bergeijk, C. Van der Zee, L. Stal, Uptake and excretion of dimethylsulphoniopropionate is driven by salinity changes in the marine benthic diatom Cylindrotheca closterium. Eur. J. Phycol. 2003, 38, 341.
Uptake and excretion of dimethylsulphoniopropionate is driven by salinity changes in the marine benthic diatom Cylindrotheca closterium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXltVagtr4%3D&md5=46de24987b695d5850ab25c26dd8de62CAS |

[37]  D. M. Dickson, G. O. Kirst, The role of β-dimethylsulphoniopropionate, glycine betaine and homarine in the osmoacclimation of Platymonas subcordiformis. Planta 1986, 167, 536.
The role of β-dimethylsulphoniopropionate, glycine betaine and homarine in the osmoacclimation of Platymonas subcordiformis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28Xkt1Wns7g%3D&md5=91daddc5739dbc52d501f7cd89dd4b4bCAS | 24240370PubMed |

[38]  U. Karsten, C. Wiencke, G. O. Kirst, The effect of salinity changes upon the physiology of eulittoral green macroalgae from Antartica and southern Chile. II. Intracellular inorganic ions and organic compounds. J. Exp. Bot. 1991, 42, 1533.
The effect of salinity changes upon the physiology of eulittoral green macroalgae from Antartica and southern Chile. II. Intracellular inorganic ions and organic compounds.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XhtVamurw%3D&md5=87b6ef9b1c5b763a98bdbda2251d9061CAS |

[39]  U. Karsten, C. Wiencke, G. O. Kirst, Dimethylsulphoniopropionate (DMSP) accumulation in green macroalgae from polar to temperate regions: interactive effects of light versus salinity and light versus temperature. Polar Biol. 1992, 12, 603.
Dimethylsulphoniopropionate (DMSP) accumulation in green macroalgae from polar to temperate regions: interactive effects of light versus salinity and light versus temperature.Crossref | GoogleScholarGoogle Scholar |

[40]  M. Gleitz, A. Bartsch, G. Dieckmann, H. Eicken, Composition and succession of sea ice diatom assemblages in the eastern and southern Weddell Sea, Antarctica, in Antarctic Sea Ice: Biological Processes, Interactions and Variability (Eds K. R. Arrigo, M. P. Lizotte) 1998, pp. 107–120 (American Geophysical Union:Washington, DC).

[41]  M. P. Lizotte, The contributions of sea ice algae to Antarctic marine primary production. Am. Zool. 2001, 41, 57.

[42]  C. Lovejoy, R. Massana, C. Pedros-Alio, Diversity and distribution of marine microbial eukaryotes in the Arctic Ocean and adjacent seas. Appl. Environ. Microbiol. 2006, 72, 3085.
Diversity and distribution of marine microbial eukaryotes in the Arctic Ocean and adjacent seas.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XkvFSqtbk%3D&md5=7871e0135689e9a4dc27c0bd5ad083eaCAS | 16672445PubMed |

[43]  S. Papadimitriou, D. N. Thomas, H. Kennedy, C. Haas, H. Kuosa, A. Krell, G. S. Dieckmann, Biogeochemical composition of natural sea ice brines from the Weddell Sea during early austral summer. Limnol. Oceanogr. 2007, 52, 1809.
Biogeochemical composition of natural sea ice brines from the Weddell Sea during early austral summer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1ahsL3O&md5=7b0d6ac14cc2d786fb87072b4d000db2CAS |

[44]  R. R. L. Guillard, P. E. Hargraves, Stichochrysis immobilis is a diatom, not a chrysophyte. Phycologia 1993, 32, 234.
Stichochrysis immobilis is a diatom, not a chrysophyte.Crossref | GoogleScholarGoogle Scholar |

[45]  R. A. Andersen (Ed.), Algal Culturing Techniques 2005, pp. 487–488 (Elsevier Academic Press: Burlington, MA).

[46]  T. R. Parsons, Y. Maita, C. M. Lalli, A Manual of Chemical and Biological Methods for Seawater Analysis 1984, pp. 142–148 (Pergamon Press: Oxford, UK).

[47]  G. Sarazin, G. Michard, F. Prevot, A rapid and accurate spectroscopic method for alkalinity measurements in sea water samples. Water Res. 1999, 33, 290.
A rapid and accurate spectroscopic method for alkalinity measurements in sea water samples.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXotVOqur0%3D&md5=b64678b85ac65fe4dff8ef3ffbf1691cCAS |

[48]  B. Sherr, E. Sherr, Pd. Giorgio, Enumeration of total and highly active bacteria, in Methods in Microbiology: Vol. 30 Marine Microbiology (Ed. J. H. Paul) 2001, p. 129–159 (Academic Press: New York).

[49]  R. P. Kiene, D. Slezak, Low dissolved DMSP concentrations in seawater revealed by small-volume gravity filtration and dialysis sampling. Limnol. Oceanogr. Methods 2006, 4, 80.
Low dissolved DMSP concentrations in seawater revealed by small-volume gravity filtration and dialysis sampling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XmtlWnt70%3D&md5=3be8a7772e588484be5f1fe6005e96f5CAS |

[50]  R. B. Dean, W. J. Dixon, Simplified statistics for small numbers of observations. Anal. Chem. 1951, 23, 636.
Simplified statistics for small numbers of observations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaG3MXjtFKnsw%3D%3D&md5=ab3625946acb3e0d3c4fb283d78bea15CAS |

[51]  S. F. Riseman, G. R. DiTullio, Particulate dimethylsulfoniopropionate and dimethylsulfoxide in relation to iron availability and algal community structure in the Peru Upwelling System. Can. J. Fish. Aquat. Sci. 2004, 61, 721.
Particulate dimethylsulfoniopropionate and dimethylsulfoxide in relation to iron availability and algal community structure in the Peru Upwelling System.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXns1Sjs74%3D&md5=3d979833454ccbbdd6108463a9adff36CAS |

[52]  C. Evans, G. Malin, G. P. Mills, W. H. Wilson, Viral infection of Emiliania huxleyi (Prymnesiophyceae) leads to elevated production of reactive oxygen species. J. Phycol. 2006, 42, 1040.
Viral infection of Emiliania huxleyi (Prymnesiophyceae) leads to elevated production of reactive oxygen species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFOrsb%2FP&md5=e72964ef6caf997813aa0b9a0f5e9838CAS |

[53]  M. K. Nishiguchi, G. N. Somero, Temperature- and concentration-dependence of compatibility of the organic osmolyte β-dimethylsulfoniopropionate. Cryobiology 1992, 29, 118.
Temperature- and concentration-dependence of compatibility of the organic osmolyte β-dimethylsulfoniopropionate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XitlWhtLs%3D&md5=b370abfae403148b7e90b0f1ea34e0efCAS | 1295491PubMed |

[54]  P. S. Low, Molecular basis of the biological compatibility of Nature’s osmolytes, in Transport Processes, Iono- and Osmoregulation (Eds R. Gilles, M. Gilles-Baillien M) 1985. p. 469–477 (Springer: Berlin, Germany).

[55]  I. Ahmad, J. A. Hellebust, The relationship between inorganic nitrogen metabolism and proline accumulation in osmoregulatory responses of two euryhaline microalgae. Plant Physiol. 1988, 88, 348.
The relationship between inorganic nitrogen metabolism and proline accumulation in osmoregulatory responses of two euryhaline microalgae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXmt1KntrY%3D&md5=572c61178b6465c1ebf01b1b792a0b35CAS | 16666306PubMed |

[56]  C. Trossat, B. Rathinasabapathi, E. A. Weretilnyk, T.-L. Shen, Z.-H. Huang, D. A. Gage, A. D. Hanson, Salinity promotes accumulation of 3-dimethylsulfoniopropionate and its precursor S-methylmethionine in chloroplasts. Plant Physiol. 1998, 116, 165.
Salinity promotes accumulation of 3-dimethylsulfoniopropionate and its precursor S-methylmethionine in chloroplasts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXkslCruw%3D%3D&md5=547b8143d181bfae9d740b78dc8a3b7cCAS | 9449841PubMed |

[57]  B. R. Lyon, P. A. Lee, J. M. Bennett, G. R. DiTullio, M. G. Janech, Proteomic analysis of a sea-ice diatom: salinity acclimation provides new insight into the dimethylsulfoniopropionate production pathway. Plant Physiol. 2011, 157, 1926.
Proteomic analysis of a sea-ice diatom: salinity acclimation provides new insight into the dimethylsulfoniopropionate production pathway.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs1ektL%2FF&md5=ced3b8a572f6d8f4fa75fbc595f43e98CAS | 22034629PubMed |

[58]  M. Janssen, L. Bathke, J. Marquardt, W. E. Krumbein, E. Rhiel, Changes in the photosynthetic apparatus of diatoms in response to low and high light intensities. Int. Microbiol. 2001, 4, 27.
| 1:CAS:528:DC%2BD38XmtFWmtbY%3D&md5=d4ffa3c784c9bdbfc9918ce98e4ef1c8CAS | 11770817PubMed |

[59]  R. H. Reed, P. J. Wright, Release of mannitol from Pilayella littoralis (Phaeophyta: Ectocarpales) in response to hypoosmotic stress. Mar. Ecol. Prog. Ser. 1986, 29, 205.
Release of mannitol from Pilayella littoralis (Phaeophyta: Ectocarpales) in response to hypoosmotic stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28XitVequ78%3D&md5=5183b62e0c4186d24b5fa7543d01767cCAS |

[60]  D. T. Welsh, Ecological significance of compatible solute accumulation by micro-organisms: from single cells to global climate. FEMS Microbiol. Rev. 2000, 24, 263.
Ecological significance of compatible solute accumulation by micro-organisms: from single cells to global climate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjslOru7Y%3D&md5=dd70f278a492fd333f7514d512f6e878CAS | 10841973PubMed |

[61]  S. Fulda, M. Hagemann, E. Libbert, Release of glucosylglycerol from the cyanobacterium Synechocystis spec. SAG 92.79 by hypoosmotic shock. Arch. Microbiol. 1990, 153, 405.
Release of glucosylglycerol from the cyanobacterium Synechocystis spec. SAG 92.79 by hypoosmotic shock.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXitFersL8%3D&md5=ba1a9ed4e04f266256a6d5c29249cb52CAS |

[62]  J. W. Rijstenbil, UV- and salinity-induced oxidative effects in the marine diatom Cylindrotheca closterium during simulated emersion. Mar. Biol. 2005, 147, 1063.
UV- and salinity-induced oxidative effects in the marine diatom Cylindrotheca closterium during simulated emersion.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVKqu7nK&md5=a4d1b5bb2e8e4c7810efd9576bb4706aCAS |

[63]  A. D. Hatton, S. T. Wilson, Particulate dimethylsulphoxide and dimethylsulphoniopropionate in phytoplankton cultures and Scottish coastal waters. Aquat. Sci. 2007, 69, 330.
Particulate dimethylsulphoxide and dimethylsulphoniopropionate in phytoplankton cultures and Scottish coastal waters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1ajtrjM&md5=227939c7c055c4d948b686ca5a579079CAS |

[64]  U. Karsten, C. Wiencke, G. O. Kirst, Growth pattern and β-dimethylsulphoniopropionate (DMSP) content of green macroalgae at different irradiances. Mar. Biol. 1991, 108, 151.
Growth pattern and β-dimethylsulphoniopropionate (DMSP) content of green macroalgae at different irradiances.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXks1ygurk%3D&md5=91f3890353a0e8294824f91722141467CAS |

[65]  G. F. Cota, C. W. Sullivan, Photoadaptation, growth and production of bottom ice algae in the Antarctic. J. Phycol. 1990, 26, 399.
Photoadaptation, growth and production of bottom ice algae in the Antarctic.Crossref | GoogleScholarGoogle Scholar |

[66]  A. Krell, D. Funck, I. Plettner, U. John, G. Dieckmann, Regulation of proline metabolism under salt stress in the psychrophilic diatom Fragilariopsis cylindrus (Bacillariophyceae). J. Phycol. 2007, 43, 753.
Regulation of proline metabolism under salt stress in the psychrophilic diatom Fragilariopsis cylindrus (Bacillariophyceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpvFSrt70%3D&md5=6d0ef96a246e4ebbd434af96e0738372CAS |

[67]  J. Stefels, J. Dacey, T. Elzenga, In vivo DMSP-biosynthesis measurements using stable-isotope incorporation and proton-transfer-reaction mass spectrometry (PTR-MS). Limnol. Oceanogr. Methods 2009, 7, 595.
In vivo DMSP-biosynthesis measurements using stable-isotope incorporation and proton-transfer-reaction mass spectrometry (PTR-MS).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht1WjtrfN&md5=fe3a11240c60e1f67928be9e834755fbCAS |