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Environmental problems - Chemical approaches
RESEARCH ARTICLE

A steady-state physiological model for intracellular dimethylsulfoxide in marine phytoplankton

Michel Lavoie A , Maurice Levasseur A C and William G. Sunda B
+ Author Affiliations
- Author Affiliations

A Québec-Océan and Unité Mixte Internationale Takuvik Ulaval–Centre national de recherche scientifique (CNRS), Département de Biologie, Université Laval, Québec, QC, G1K 7P4, Canada.

B Beaufort Laboratory, National Oceanic and Atmospheric Administration, Beaufort, NC 28516, USA.

C Corresponding author. Email: maurice.levasseur@bio.ulaval.ca

Environmental Chemistry 13(2) 212-219 https://doi.org/10.1071/EN14221
Submitted: 26 June 2014  Accepted: 3 April 2015   Published: 15 September 2015

Environmental context. Dimethylsulfoxide (DMSO) is important in the biogeochemical cycle of sulfur. Using a mathematical flux model of DMSO production and loss rates, we find that the high intracellular DMSO concentrations measured in phytoplankton cannot be produced without invoking unrealistically high intracellular concentrations of the precursor dimethylsulfoniopropionate, or much lower phytoplankton cellular efflux rates than currently reported. Our study emphasises the need for further investigations of DMSO fluxes across intracellular and outer cell membranes.

Abstract. Despite 20+ years of research, the mechanisms whereby marine phytoplankton accumulate high dimethylsulfoxide (DMSO) concentrations (up to 1–70 mmol per litre of cell volume) are still puzzling. In order to evaluate reported intracellular DMSO concentrations, we constructed a kinetic steady-state rate model of intracellular DMSO concentrations in microalgae based on reported DMSO production from the oxidation of dimethylsulfoniopropionate (DMSP) and loss by diffusion out of the cell. Based on measured rates of DMSO diffusion across the outer cell membrane of model algal species, the steady-state model indicates that sustaining intracellular DMSO concentrations in the millimolar range by the oxidation of intracellular DMSP would require steady-state intracellular DMSP concentrations that are 40 to 10 000 times higher than values measured in prymnesiophytes and diatoms, high- and low-DMSP algal groups. However, if DMSO is mainly produced within the chloroplast by the oxidation of DMSP by photosynthetically produced reactive oxygen species, it would have to diffuse through multiple chloroplast membranes before being lost from the cell across the outer membrane. Consequently, its loss rate might be considerably slower than our model predicts, allowing the build-up of higher intracellular DMSO concentrations. Possible biases in sample handling and DMSO analyses could also explain the discrepancy between modelled and measured intracellular DMSO.

Additional keywords: diatoms, dimethylsulfoniopropionate, dimethylsulfide, DMS, DMSO, DMSP, prymnesiophytes, reactive oxygen species.


References

[1]  T. K. Green, A. D. Hatton, The CLAW hypothesis: a new perspective on the role of biogenic sulphur in the regulation of global climate. Oceanogr. Mar. Biol. Annu. Rev. 2014, 52, 315.

[2]  R. P. Kiene, L. J. Linn, J. A. Bruton, New and important roles for DMSP in marine microbial communities. J. Sea Res. 2000, 43, 209.
New and important roles for DMSP in marine microbial communities.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXms1Wrtbw%3D&md5=789cb96d8406d5bbead908e442a540f1CAS |

[3]  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=24299dba1956a59c2726d9e91321070cCAS |

[4]  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=c9a82baa2292d53380b59fe3e33c367cCAS | 22129724PubMed |

[5]  R. Y. W. Chang, S. J. Sjostedt, J. R. Pierce, T. N. Papakyriakou, M. G. Scarratt, S. Michaud, M. Levasseur, W. R. Leatch, J. P. D. Abbatt, Relating atmospheric and oceanic DMS levels to particle nucleation events in the Canadian Arctic. J. Geophys. Res. 2011, 116, D00S03.
Relating atmospheric and oceanic DMS levels to particle nucleation events in the Canadian Arctic.Crossref | GoogleScholarGoogle Scholar |

[6]  W. R. Leaitch, S. Sharma, L. Huang, D. Toom-Sauntry, A. Chivulescu, A. M. Macdonald, K. von Salzen, J. R. Pierce, A. K. Bertram, J. C. Schroder, N. C. Shantz, R. Y.-W. Chang, A.-L. Norman, Dimethyl sulfide control of the clean summertime Arctic aerosol and cloud. Elem. Sci. Anth. 2013, 1, 000017.
Dimethyl sulfide control of the clean summertime Arctic aerosol and cloud.Crossref | GoogleScholarGoogle Scholar |

[7]  R. Simó, J. O. Grimalt, C. Pedrós-Alió, J. Albaiges, Occurrence and transformation of dissolved dimethyl sulfur species in stratified seawater (western Mediterranean Sea). Mar. Ecol. Prog. Ser. 1995, 127, 291.
Occurrence and transformation of dissolved dimethyl sulfur species in stratified seawater (western Mediterranean Sea).Crossref | GoogleScholarGoogle Scholar |

[8]  R. Simó, C. Pedrós-Alió, G. Malin, J. O. Grimalt, Biological turnover of DMS, DMSP and DMSO in contrasting open-sea waters. Mar. Ecol. Prog. Ser. 2000, 203, 1.
Biological turnover of DMS, DMSP and DMSO in contrasting open-sea waters.Crossref | GoogleScholarGoogle Scholar |

[9]  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=e0053968b8927b12cf82b4dc2332885cCAS |

[10]  C. Zindler, A. Bracher, C. A. Marandino, B. Taylor, E. Torricella, A. Kock, H. W. Bange, Sulphur compounds, methane, and phytoplankton: interactions along a north–south transit in the western Pacific Ocean. Biogeosciences 2013, 10, 3297.
Sulphur compounds, methane, and phytoplankton: interactions along a north–south transit in the western Pacific Ocean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXltlOrt70%3D&md5=c9534a201908d47faec31ae9fdcc6db4CAS |

[11]  C. E. Spiese, D. J. Kieber, C. T. Nomura, R. P. Kiene, Reduction of dimethylsulfoxide to dimethylsulfide by marine phytoplankton. Limnol. Oceanogr. 2009, 54, 560.
Reduction of dimethylsulfoxide to dimethylsulfide by marine phytoplankton.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsVCrtr3I&md5=9867c3b9da640ef30be69e713626065fCAS |

[12]  E. Bucciarelli, C. Ridame, W. G. Sunda, C. Dimier-Hugueney, M. Cheize, S. Belviso, Increased intracellular concentrations of DMSP and DMSO in iron-limited oceanic phytoplankton Thalassiosira oceanica and Trichodesmium erythraeum. Limnol. Oceanogr. 2013, 58, 1667.
Increased intracellular concentrations of DMSP and DMSO in iron-limited oceanic phytoplankton Thalassiosira oceanica and Trichodesmium erythraeum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhs1CmsLbP&md5=4df967e8e380c2c89368b6cd4020f193CAS |

[13]  A. D. Hatton, G. Malin, A. G. McEwan, P. S. Liss, Determination of dimethylsulfoxide in aqueous solution by an enzyme-linked method. Anal. Chem. 1994, 66, 4093.
Determination of dimethylsulfoxide in aqueous solution by an enzyme-linked method.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXmtlOqt74%3D&md5=7da15aee9e4ac1bb1e0e1cef4a70210cCAS |

[14]  R. Simó, J. O. Grimalt, J. Albaigés, Sequential method for the field determination of nanomolar concentrations of dimethyl sulfoxide in natural waters. Anal. Chem. 1996, 68, 1493.
Sequential method for the field determination of nanomolar concentrations of dimethyl sulfoxide in natural waters.Crossref | GoogleScholarGoogle Scholar | 21619113PubMed |

[15]  R. P. Kiene, G. Gerard, Determination of trace levels of dimethylsulfoxide (DMSO) in seawater and rainwater. Mar. Chem. 1994, 47, 1.
Determination of trace levels of dimethylsulfoxide (DMSO) in seawater and rainwater.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXmtFansbY%3D&md5=6e5583c0197f409bf1655332763d15e3CAS |

[16]  W. Sunda, D. Kieber, R. 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=1bcaa8d9ca44d13d4f343901c31cbed2CAS | 12124622PubMed |

[17]  G. V. Buxton, C. L. Greenstock, W. P. Helman, A. B. Ross, Critical review of rate constants for reactions of hydrated electrons, hydrogen atoms and hydroxyl radicals in aqueous solutions. J. Phys. Chem. Ref. Data 1988, 17, 513.
Critical review of rate constants for reactions of hydrated electrons, hydrogen atoms and hydroxyl radicals in aqueous solutions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXlvFyisLc%3D&md5=b62bd0e82814ec1ec169db382e3d48ffCAS |

[18]  J. Y. Tanaka, J. R. Walsh, K. R. Diller, J. J. Brand, S. J. Aggarwal, Algae permeability to Me2SO from –3 to 23 °C. Cryobiology 2001, 42, 286.
Algae permeability to Me2SO from –3 to 23 °C.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXptFOksLY%3D&md5=da873601ce573469e12691ce71688ffdCAS | 11748937PubMed |

[19]  C. E. Spiese, Cellular production and losses of dimethylsulfide in marine algae 2010, Ph.D. thesis, State University of New York, Syracuse, NY.

[20]  P. F. Bjørnsen, Phytoplankton exudation of organic matter: why do healthy cells do it? Limnol. Oceanogr. 1988, 33, 151.
Phytoplankton exudation of organic matter: why do healthy cells do it?Crossref | GoogleScholarGoogle Scholar |

[21]  M. N. Breckels, D. E. Boakes, E. A. Codling, G. Malin, S. D. Archer, M. Steinke, Modelling the concentration of exuded dimethylsulphoniopropionate (DMSP) in the boundary layer surrounding phytoplankton cells. J. Plankton Res. 2010, 32, 253.
Modelling the concentration of exuded dimethylsulphoniopropionate (DMSP) in the boundary layer surrounding phytoplankton cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtFKktQ%3D%3D&md5=672520e45044e2689b215543810a3ee6CAS |

[22]  P. Amels, H. Elias, K. J. Wannowius, Kinetics and mechanism of the oxidation of dimethyl sulfide by hydroperoxides in aqueous medium – study on the potential contribution of liquid-phase oxidation of dimethyl sulfide in the atmosphere. J. Chem. Soc., Faraday Trans. 1997, 93, 2537.
Kinetics and mechanism of the oxidation of dimethyl sulfide by hydroperoxides in aqueous medium – study on the potential contribution of liquid-phase oxidation of dimethyl sulfide in the atmosphere.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXlt1CntLg%3D&md5=692c3709c63e44378d51db6e1abcb671CAS |

[23]  R Development Core Team, R: a language and environment for statistical computing 2013 (R Foundation for Statistical Computing: Vienna, Austria). Available at http://www.R-project.org [Verified 4 June 2015].

[24]  K. Soetaert, T. Petzoldt, R. W. Setzer, Solving differential equations in R: package deSolve. J. Stat. Softw. 2010, 33, 1.

[25]  J. Marchetti, G. Bourgarana, L. L. Deana, C. Mégriera, E. Lukomska, R. Kaasa, E. Olivo, R. Baron, R. Robert, J. P. Cadoret, Optimizing conditions for the continuous culture of Isochrysis affinis galbana relevant to commercial hatcheries. Aquaculture 2012, 336–329, 106.
Optimizing conditions for the continuous culture of Isochrysis affinis galbana relevant to commercial hatcheries.Crossref | GoogleScholarGoogle Scholar |

[26]  J. Farrant, Permeability of guinea-pig smooth muscle to non-electrolytes. J. Physiol. 1965, 178, 1.
Permeability of guinea-pig smooth muscle to non-electrolytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF2MXosV2gsQ%3D%3D&md5=fe0eafea5b04edac4f5c3c6c67ca3e0bCAS | 14298109PubMed |

[27]  W. G. Sunda, S. A. Huntsman, Processes regulating cellular metal accumulation and physiological effects: phytoplankton as model systems. Sci. Total Environ. 1998, 219, 165.
Processes regulating cellular metal accumulation and physiological effects: phytoplankton as model systems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXlslWltrg%3D&md5=4484faa7dba4ff4d575f92cec5dc66b4CAS |

[28]  R. Notman, W. K. den Otter, M. G. Noro, W. J. Briels, J. Anwa, The permeability-enhancing mechanism of DMSO in ceramide bilayers simulated by molecular dynamics. Biophys. J. 2007, 93, 2056.
The permeability-enhancing mechanism of DMSO in ceramide bilayers simulated by molecular dynamics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVSqur%2FO&md5=f1bfeb4e5471bd15a5caa4c533d19042CAS | 17513383PubMed |

[29]  C. Trossat, K. D. Nolte, A. D. Hanson, Evidence that the pathway of dimethylsulfoniopropionate biosynthesis begins in the cytosol and ends in the chloroplast. Plant Physiol. 1996, 111, 965.
| 1:CAS:528:DyaK28XltVGgtrw%3D&md5=2a1c6204e03c6bfb56bcea002f92fb13CAS | 12226341PubMed |

[30]  B. Jakob, U. Heber, Photoproduction and detoxification of hydroxyl radicals in chloroplasts and leaves and relation to photoinactivation of photosystems I and II. Plant Cell Physiol. 1996, 37, 629.
Photoproduction and detoxification of hydroxyl radicals in chloroplasts and leaves and relation to photoinactivation of photosystems I and II.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xks1OnsL8%3D&md5=3158e1c711407e5417ab9500d44a96b0CAS |

[31]  K. K. Niyogi, Photoprotection revisited: genetic and molecular approaches. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1999, 50, 333.
Photoprotection revisited: genetic and molecular approaches.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXkt1yksbo%3D&md5=8b3f58f026b611756bcf0a59c8df7fb4CAS | 15012213PubMed |

[32]  P. G. Falkowski, J. A. Raven, Aquatic Photosynthesis 2007 (Princeton University Press).

[33]  R. Simó, A. D. Hatton, G. Malin, P. S. Liss, Particulate dimethyl sulphoxide in seawater: production by microplankton. Mar. Ecol. Prog. Ser. 1998, 167, 291.
Particulate dimethyl sulphoxide in seawater: production by microplankton.Crossref | GoogleScholarGoogle Scholar |

[34]  D. A. del Valle, D. J. Kieber, D. A. Toole, J. Bisgrove, R. P. Kiene, Dissolved DMSO production via biological and photochemical oxidation of dissolved DMS in the Ross Sea, Antarctica. Deep Sea Res. Part I Oceanogr. Res. Pap. 2009, 56, 166.
Dissolved DMSO production via biological and photochemical oxidation of dissolved DMS in the Ross Sea, Antarctica.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmtFOgtQ%3D%3D&md5=2caafda6ff86e2c7169192d2873e1ba2CAS |

[35]  D. A. del Valle, D. J. Kieber, J. Bisgrove, R. P. Kiene, Light-stimulated production of dissolved DMSO by a particle-associated process in the Ross Sea, Antarctica. Limnol. Oceanogr. 2007, 52, 2456.
Light-stimulated production of dissolved DMSO by a particle-associated process in the Ross Sea, Antarctica.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhsVCnsLzJ&md5=8fa23fc219b99a8778a55478a106267eCAS |

[36]  C. Junot, C. Fenaille, B. Colsch, F. Bécher, High resolution mass spectrometry based techniques at the crossroads of metabolic pathways. Mass Spectrom. Rev. 2014, 33, 471.
High resolution mass spectrometry based techniques at the crossroads of metabolic pathways.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhs1yit7rM&md5=1581ae1e0b4080f88fee7bcb4b080c5fCAS | 24288070PubMed |

[37]  M. S. Savoca, G. A. Nevitt, Evidence that dimethyl sulfide facilitates a tritrophic mutualism between marine primary producers and top predators. Proc. Natl. Acad. Sci. USA 2014, 111, 4157.
Evidence that dimethyl sulfide facilitates a tritrophic mutualism between marine primary producers and top predators.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXjtl2kt7w%3D&md5=935ded43fa889e5e490eb3ddb55b477eCAS | 24591607PubMed |

[38]  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=893747ce9353bc7a9b6600a67fae72bdCAS | 22034629PubMed |