Salinity and growth effects on dimethylsulfoniopropionate (DMSP) and dimethylsulfoxide (DMSO) cell quotas of Skeletonema costatum, Phaeocystis globosa and Heterocapsa triquetra
Speeckaert, G; Borges, Alberto; Gypens, N
2019 • In Estuarine Coastal and Shelf Science, 226 (106275), p. 1-10
[en] The effects of growth stage and salinity on dimethylsulfoniopropionate (DMSP) and dimethylsulfoxide (DMSO) cellular content were investigated in laboratory batch cultures of three phytoplankton species (Skeletonema costatum, Phaeocystis globosa and Heterocapsa triquetra). DMSP and DMSO cell quotas of the three microalgae were measured at three salinities (20, 27, 35) and in three growth phases at salinity 35. DMSP and DMSO cell quotas varied along the growth for all species with an increase of DMSP for S. costatum and a decrease of the DMSP to DMSO ratio (DMSP/DMSO) for P. globosa and H. triquetra in late exponential-stationary phase. We hypothesized that the oxidative stress caused by light and/or nutrients limitation induced the oxidation of DMS or DMSP to DMSO. DMSP cell quotas increased with salinity, mostly in S. costatum and H. triquetra, for which DMSP is supposed to be an osmoregulator. In H. triquetra, DMSO cell quotas stayed constant with increasing salinity. DMSO was near detection limits in S. costatum experiments. In P. globosa, DMSP and DMSO concentrations increased at low and high salinity. DMSO showed higher increase at low salinity presumably as the result of a salinity-induced oxidative stress which caused DMSP oxidation into DMSO in hyposaline conditions. We concluded that DMSP acts as an osmoregulator for the three studied species and DMSO acts as an antioxidant for P. globosa at low salinity. In P. globosa and H. triquetra, DMSP/DMSO increase with salinity in response to salinity stress.
Disciplines :
Aquatic sciences & oceanology
Author, co-author :
Speeckaert, G
Borges, Alberto ; Université de Liège - ULiège > Département d'astrophys., géophysique et océanographie (AGO) > Chemical Oceanography Unit (AGO)
Gypens, N
Language :
English
Title :
Salinity and growth effects on dimethylsulfoniopropionate (DMSP) and dimethylsulfoxide (DMSO) cell quotas of Skeletonema costatum, Phaeocystis globosa and Heterocapsa triquetra
del Valle, D.A, Slezak, D., Smith, C.M., Rellinger, A.N., Kieber, D.J., Kiene, R.P., Effect of acidification on preservation of DMSP in seawater and phytoplankton cultures: evidence for rapid loss and cleavage of DMSP in samples containing Phaeocystis sp. Mar. Chem. 124:1–4 (2011), 57–67 3682.
Ahmad, P., Plant productivity and environment. Science 218 (2014), 443–448 Oxidative damage to plants. Academic Press, Elsevier USA Boyer JS (1982).
Amels, P., Elias, H., Wannowius, K.-J., 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. 93:15 (1997), 2537–2544.
Apel, K., Hirt, H., REACTIVE OXYGEN SPECIES: metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 55:1 (2004), 373–399 https://doi.org/10.1146/annurev.arplant.55.031903.141701.
Baek, S.H., Ki, J.S., Katano, T., You, K., Park, B.S., Shin, H.H., et al. Dense winter bloom of the dinoflagellate Heterocapsa triquetra below the thick surface ice of brackish Lake Shihwa, Korea. Phycol. Res. 59:4 (2011), 273–285.
Balzano, S., Sarno, D., Kooistra, W.H., Effects of salinity on the growth rate and morphology of ten Skeletonema strains. J. Plankton Res. 33:6 (2011), 937–945.
Berman-Frank, I., Bidle, K.D., Haramaty, L., Falkowski, P.G., The demise of the marine cyanobacterium, Trichodesmium spp., via an autocatalyzed cell death pathway. Limnol. Oceanogr. 49:4 (2004), 997–1005.
Brand, L.E., The salinity tolerance of forty-six marine phytoplankton isolates. Estuar. Coast Shelf Sci. 18:5 (1984), 543–556.
Bucciarelli, E., Sunda, W.G., Influence of CO2, nitrate, phosphate, and silicate limitation on intracellular dimethylsulfoniopropionate in batch cultures of the coastal diatom Thalassiosira pseudonana. Limnol. Oceanogr. 48:6 (2003), 2256–2265.
Caruana, A.M.N., Malin, G., The variability in DMSP content and DMSP lyase activity in marine dinoflagellates. Prog. Oceanogr. 120 (2014), 410–424 https://doi.org/10.1016/j.pocean.2013.10.014.
Caruana, A.M.N., Steinke, M., Turner, S.M., Malin, G., Concentrations of dimethylsulphoniopropionate and activities of dimethylsulphide-producing enzymes in batch cultures of nine dinoflagellate species. Biogeochemistry 110:1–3 (2012), 87–107 https://doi.org/10.1007/s10533-012-9705-4.
Cavalcanti, F.R., Lima, J.P.M.S., Ferreira-Silva, S.L., Viégas, R.A., Silveira, J.A.G., Roots and leaves display contrasting oxidative response during salt stress and recovery in cowpea. J. Plant Physiol. 164:5 (2007), 591–600.
Deschaseaux, E.S., Jones, G.B., Deseo, M.A., Shepherd, K.M., Kiene, R.P., Swan, H.B., et al. Effects of environmental factors on dimethylated sulfur compounds and their potential role in the antioxidant system of the coral holobiont. Limnol. Oceanogr. 59:3 (2014), 758–768.
Dickson, D.M.J., Kirst, G.O., The role of β-dimethylsulphoniopropionate, Glycine betaine and homarine in the osmoacclimation of platymonas subcordiformis. Planta 167:4 (1986), 536–543.
Dring, M.J., Stress resistance and disease resistance in seaweeds: the role of reactive oxygen metabolism. Adv. Bot. Res. 43 (2005), 175–207.
Foote, C.S., Peters, J.W., Chemistry of singlet oxygen. XIV. Reactive intermediate in sulfide photooxidation. J. Am. Chem. Soc. 93:15 (1971), 3795–3796 https://doi.org/10.1021/ja00744a055.
García, N., López-Elías, J.A., Miranda, A., Huerta, M.M.-P.N., García, A., Effect of salinity on growth and chemical composition of the diatom Thalassiosira weissflogii at three culture phases/Efecto de la salinidad en el crecimiento y composición química de la diatomea Thalassiosira weissflogii en tres fases de cultivo. Latin Am. J. Aquat. Res., 40(2), 2012, 435.
Grasshoff, K., Determination of nitrate. Grasshoff, K., Ehrhardt, M., Kremling, K., (eds.) Methods of Seawater Analysis, 1983, Verlag Chemie, Basel, 143–150.
Gröne, T., Kirst, G.O., Aspects of dimethylsulfoniopropionate effects on enzymes isolated from the marine phytoplankter Tetraselmis subcordiformis (Stein). J. Plant Physiol. 138:1 (1991), 85–91.
Guillard, R.R., Division Rates. Handbook of Phycological Methods: Culture Methods and Growth Measurements. 1973.
Harada, H., Kiene, R.P., Assessment and Characteristics of DMSP Lyase Activity in Seawater and Phytoplankton Cultures, vol 41, 2011, Publications of the Seto Marine Biological Laboratory, 1–16.
Hoppenrath, M., A revised checklist of planktonic diatoms and dinoflagellates from Helgoland (North Sea, German Bight). Helgol. Mar. Res., 58(4), 2004, 243.
Iverson, R.L., Nearhooj, F.L., Andreae, M.O., Production of dimethylsulfonium 3849 propionate and dimethylsulfide by phytoplankton in estuarine and coastal waters. 3850 Limnol. Oceanogr. 34:1 (1989), 53–67.
Jahnke, L.S., White, A.L., Long-term hyposaline and hypersaline stresses produce distinct antioxidant responses in the marine alga Dunaliella tertiolecta. J. Plant Physiol. 160 (2003), 1193–1202.
Karsten, Ulf, Kirst, G.O., Wiencke, C., Dimethylsulphoniopropionate (DMSP) accumulation in green macioalgae from polar to temperate regions: interactive effects of light versus salinity and light versus temperature. Polar Biol. 12:6–7 (1992), 603–607.
Keller, M.D., Dimethyl sulfide production and marine phytoplankton: the importance of species composition and cell size. Biol. Oceanogr. 6:5–6 (1989), 375–382.
Keller, M.D., Bellows, W.K., Guillard, R.R., Dimethyl sulfide production in marine phytoplankton. Biog. Sulfur Environ.(393), 1989, 167–182.
Keller, M.D., Kiene, R.P., Matrai, P.A., Bellows, W.K., Production of glycine betaine and dimethylsulfoniopropionate in marine phytoplankton. II. N-limited chemostat cultures. Mar. Biol. 135:2 (1999), 249–257.
Kettles, Nicola Louise, Kopriva, Stanislav, Gill, Malin, Insights into the regulation of DMSP synthesis in the diatom thalassiosira pseudonana through APR activity, proteomics and gene expression analyses on cells acclimating to changes in salinity, light and nitrogen. PLoS One, 9(4), 2014, e94795.
Kiene, R.P., Gerard, G., Determination of trace levels of dimethylsulfoxide (DMSO) in seawater and rainwater. Mar. Chem. 47:1 (1994), 1–12.
Kiene, R.P., Slezak, D., Low dissolved DMSP concentrations in seawater revealed by small-volume gravity filtration and dialysis sampling. Limnol Oceanogr. Methods 4 (2006), 80–95.
Kiene, R.P., Linn, L.J., Bruton, J.A., New and important roles for DMSP in marine microbial communities. J. Sea Res. 43:3 (2000), 209–224.
Kinsey, J.D., Kieber, D.J., Microwave preservation method for DMSP, DMSO, and acrylate in unfiltered seawater and phytoplankton culture samples. Limnol Oceanogr. Methods 14:3 (2016), 196–209.
Kinsey, J.D., Kieber, D.J., Neale, P.J., Effects of iron limitation and UV radiation on Phaeocystis Antarctica growth and dimethylsulfoniopropionate, dimethylsulfoxide and acrylate concentrations. Environ. Chem. 13:2 (2016), 195–211.
Kirst, G.O., Osmotic adjustment in phytoplankton and MacroAlgae. Kiene, Ronald P., Visscher, Pieter T., Keller, Maureen D., Kirst, Gunter O., (eds.) Biological and Environmental Chemistry of DMSP and Related Sulfonium Compounds, vols. 121–29, 1996, Springer US, Boston, MA http://link.springer.com/10.1007/978-1-4613-0377-0_11.
Kirst, G.O., Thiel, C., Wolff, H., Nothnagel, J., Wanzek, M., Ulmke, R., Dimethylsulfoniopropionate (DMSP) in ice-algae and its possible biological role. Mar. Chem. 35 (1991), 381–388.
Koroleff, F., Grasshoff, K., Ehrhardt, M., Kremling, K., (eds.) Determination of Total Silicon. Methods of Seawater Analysis, 1983, Verlag Chemie, Basel, 174–183.
Koroleff, F., Grasshoff, K., Ehrhardt, M., Kremling, K., (eds.) Determination of Total Silicon. Methods of Seawater Analysis, 1983, Verlag Chemie, Basel, 125–139.
Kreslavski, V.D., Carpentier, R., Klimov, V.V., Murata, N., Allakhverdiev, S.I., Molecular mechanisms of stress resistance of the photosynthetic apparatus. Membr. Cell Biol. 1 (2007), 185–205.
Kumar, M., Gupta, V., Trivedi, N., Kumari, P., Bijo, A.J., Reddy, C.R.K., Jha, B., Dessication induced oxidative stress and its biochemical responses in intertidal red alga Gracilaria corticata (Gracilariales, Rhodophyta). Environ. Exp. Bot. 72 (2011), 194–201.
Lavoie, M., Levasseur, M., Babin, M., Testing the potential ballast role for dimethylsulfoniopropionate in marine phytoplankton: a modeling study. J. Plankton Res. 37:4 (2015), 699–711.
Lavoie, M., Raven, J.A., Levasseur, M., Energy cost and putative benefits of cellular mechanisms modulating buoyancy in aflagellate marine phytoplankton. J. Phycol. 52:2 (2016), 239–251.
Lee, P.A., Haase, R., De Mora, S.J., Chanut, J.-P., Gosselin, M., Dimethylsulfoxide (DMSO) and related sulfur compounds in the saguenay fjord, Quebec. Can. J. Fish. Aquat. Sci. 56:9 (1999), 1631–1638.
Leshem, Y., Seri, L., Levine, A., Induction of phosphatidylinositol 3-kinase-mediated endocytosis by salt stress leads to intracellular production of reactive oxygen species and salt tolerance. Plant J. 51:2 (2007), 185–197.
Liss, P.S., Malin, G., Turner, S.M., Holligan, P.M., Dimethyl sulphide and Phaeocystis: a review. J. Mar. Syst. 5:1 (1994), 41–53.
Litaker, R.W., Tester, P.A., Duke, C.S., Kenney, B.E., Pinckney, J.L., Ramus, J., Seasonal niche strategy of the bloom-forming dinoflagellate Heterocapsa triquetra. Mar. Ecol. Prog. Ser. 232 (2002), 45–62.
Liu, F., Pang, S.J., Stress tolerance and antioxidant enzymatic activities in the metabolisms of the reactive oxygen species in two intertidal red algae Grateloupia turuturu and Palmaria palmata. J. Exp. Mar. Biol. Ecol. 382:2 (2010), 82–87.
Liu, W., Au, D.W., Anderson, D.M., Lam, P.K., Wu, R.S., Effects of nutrients, salinity, pH and light: dark cycle on the production of reactive oxygen species in the alga Chattonella marina. J. Exp. Mar. Biol. Ecol. 346:1 2 (2007), 76–86.
Liu, C., Gao, C., Zhang, H., Chen, S., Deng, P., Yue, X., Guo, X., Production of dimethylsulfide and acrylic acid from dimethylsulfoniopropionate during growth of three marine microalgae. Chin. J. Oceanol. Limnol. 32 (2014), 1270–1279.
Lund, J.W.G., Kipling, C., Le Cren, E.D., The inverted microscope method of estimating algal numbers and the statistical basis of estimations by counting. Hydrobiologia 11:2 (1958), 143–170.
Luo, M.B., Liu, F., Salinity-induced oxidative stress and regulation of antioxidant defense system in the marine macroalga Ulva prolifera. J. Exp. Mar. Biol. Ecol. 409:1–2 (2011), 223–228.
Lyon, Barbara R., Bennett-Mintz, Jennifer M., Lee, Peter A., Janech, Michael G., DiTullio, Giacomo R., Role of dimethylsulfoniopropionate as an osmoprotectant following gradual salinity shifts in the sea-ice diatom fragilariopsis cylindrus. Environ. Chem. 13:2 (2016), 181–194.
Muylaert, K., Sabbe, K., Spring phytoplankton assemblages in and around the maximum turbidity zone of the estuaries of the Elbe (Germany), the Schelde (Belgium/The Netherlands) and the Gironde (France). J. Mar. Syst. 22:2–3 (1999), 133–149.
Niki, Takushi, Shimizu, Miwa, Fujishiro, Ayako, Kinoshita, Junji, Effects of salinity downshock on dimethylsulfide production. J. Oceanogr. 63:5 (2007), 873–877 https://doi.org/10.1007/s10872-007-0074-x.
Pancha, I., Chokshi, K., Maurya, R., Trivedi, K., Patidar, S.K., Ghosh, A., Mishra, S., Salinity induced oxidative stress enhanced biofuel production potential of microalgae Scenedesmus sp. CCNM 1077. Bioresour. Technol. 189 (2015), 341–348.
Parida, A.K., Das, A.B., Salt tolerance and salinity effects on plants: a review. Ecotoxicol. Environ. Saf. 60:3 (2005), 324–349.
Peperzak, L., The wax and Wane of Phaeocystis globosa Blooms (PhD Thesis)., 2002, University Library Groningen.
Rijstenbil, J.W., UV-and salinity-induced oxidative effects in the marine diatom cylindrotheca closterium during simulated emersion. Mar. Biol. 147:5 (2005), 1063–1073.
Rousseau, V., Mathot, S., Lancelot, C., Calculating carbon biomass of Phaeocystis sp. from microscopic observations. Mar. Biol. 107:2 (1990), 305–314.
Schoemann, V., Becquevort, S., Stefels, J., Rousseau, V., Lancelot, C., Phaeocystis blooms in the global ocean and their controlling mechanisms: a review. J. Sea Res. 53:1–2 (2005), 43–66 https://doi.org/10.1016/j.seares.2004.01.008.
Sciare, J., Mihalopoulos, N., Nguyen, B.C., Spatial and temporal variability of dissolved sulfur compounds in european estuaries. Biogeochemistry 59:1–2 (2002), 121–141 https://doi.org/10.1023/A:1015539725017.
Sekmen, A.H., Türkan, İ., Takio, S., Differential responses of antioxidative enzymes and lipid peroxidation to salt stress in salt-tolerant Plantago maritima and salt-sensitive Plantago media. Physiol. Plantarum 131:3 (2007), 399–411.
Shen, P., Qi, Y., Wang, Y., Huang, L., Phaeocystis globosa Scherffel, a harmful microalga, and its production of dimethylsulfoniopropionate. Chin. J. Oceanol. Limnol. 29:4 (2011), 869–873.
Sigaud-Kutner, T.C.S., Pinto, E., Okamoto, O.K., Latorre, L.R., Colepicolo, P., Changes in superoxide dismutase activity and photosynthetic pigment content during growth of marine phytoplankters in batch-cultures. Physiol. Plantarum 114:4 (2002), 566–571.
Simó, R., Vila-Costa, M., Ubiquity of algal dimethylsulfoxide in the surface ocean: geographic and temporal distribution patterns. Mar. Chem. 100:1–2 (2006), 136–146 https://doi.org/10.1016/j.marchem.2005.11.006.
Simó, R., Hatton, A.D., Malin, G., Liss, P.S., Particulate dimethyl sulphoxide in seawater: production by microplankton. Mar. Ecol. Prog. Ser. 167 (1998), 291–296.
Spielmeyer, A., Gebser, B., Pohnert, G., Dimethylsulfide sources from microalgae: improvement and application of a derivatization-based method for the determination of dimethylsulfoniopropionate and other zwitterionic osmolytes in phytoplankton. Mar. Chem. 124:1–4 (2011), 48–56 https://doi.org/10.1016/j.marchem.2010.12.001.
Spiese, C.E., Cellular Production and Losses of Dimethylsulfide in Marine Phytoplankton (PhD Thesis)., 2010, State University of New York College of Environmental Science and Forestry.
Stefels, J., Physiological aspects of the production and conversion of DMSP in marine algae and higher plants. J. Sea Res. 43:3 (2000), 183–197.
Stefels, J., Determination of DMS, DMSP, and DMSO in seawater. Practical Guidelines for the Analysis of Seawater, 2009, 223.
Stefels, J., Dijkhuizen, L., Characteristics of DMSP-lyase in Phaeocystis sp.(prymnesiophyceae). Mar. Ecol. Prog. Ser. 131 (1996), 307–313.
Stefels, J., van Leeuwe, M.A., Effects of iron and light stress on the biochemical composition of Antarctic Phaeocystis sp. (Prymnesiophyceae). I. Intracellular DMSP concentrations. J. Phycol., 34(3), 1998 486–49.
Steinke, M., Wolfe, G.V., Kirst, G.O., Partial characterisation of dimethylsulfoniopropionate (DMSP) lyase isozymes in 6 strains of Emiliania huxleyi. Mar. Ecol. Prog. Ser. 175 (1998), 215–225.
Sudhir, P., Murthy, S.D.S., Effects of salt stress on basic processes of photosynthesis. Photosynthetica 42:2 (2004), 481–486.
Sunda, W., Kieber, D.J., Kiene, R.P., Huntsman, S., An antioxidant function for DMSP and DMS in marine algae. Nature 418:6895 (2002), 317–320.
Sunda, W., Hardison, R., Kiene, R.P., Bucciarelli, E., Harada, H., The effect of nitrogen limitation on cellular DMSP and DMS release in marine phytoplankton: climate feedback implications. Aquat. Sci., 69(2007), 2007 341–35.
Tammam, A.A., Fakhry, E.M., El-Sheekh, M., Effect of salt stress on antioxidant system and the metabolism of the reactive oxygen species in Dunaliella salina and Dunaliella tertiolecta. Afr. J. Biotechnol. 10:19 (2011), 3795–3808.
Vairavamurthy, A., Andreae, M.O., Iverson, R.L., Biosynthesis of dimethylsulfide and dimethylpropiothetin by hymenomonas carterae in relation to sulfur source and salinity variations. Limnol. Oceanogr. 30 (1985), 1 59–70 https://doi.org/10.4319/lo.1985.30.1.0059.
Van Bergeijk, Stef, A., Van der Zee, Claar, Stal, Lucas J., Uptake and excretion of dimethylsulphoniopropionate is driven by salinity changes in the marine benthic diatom cylindrotheca closterium. Eur. J. Phycol. 38:4 (2003), 341–349.
Welsh, D.T., Ecological significance of compatible solute accumulation by micro-organisms: from single cells to global climate. FEMS Microbiol. Rev. 24:3 (2000), 263–290.
Wolfe, G.V., Steinke, M., Grazing-activated production of dimethyl sulfide (DMS) by two clones of Emiliania huxleyi. Oceanography, 41(6), 1996.
Yang, Guipeng, Li, Chengxuan, Sun, Juan, Influence of salinity and nitrogen content on production of dimethylsulfoniopropionate (DMSP) and dimethylsulfide (DMS) by Skeletonema costatum. Chin. J. Oceanol. Limnol. 29 (2011), 378–386.
Zhang, M.P., Zhen, C., Wei, C., Fang, W., Hui-zhen, Z., Ping, S., Study on the dimethylsulfide and dimethylsulfoni-opropionate in algae by laboratory batch cultures. Chin. J. Oceanol. Limnol. 17:4 (1999), 366–370 https://doi.org/10.1007/BF02842831.
Zhuang, Guangchao, Yang, Guipeng, Yu, Juan, Gao, Yuan, Production of DMS and DMSP in different physiological stages and salinity conditions in two marine algae. Chin. J. Oceanol. Limnol. 29 (2011), 369–377.