Abstract
Dimethylsulphoniopropionate (DMSP) is one of the most abundant and widespread organic sulfur molecules in the marine environment and has substantial physiological and ecological importance, from subcellular to global scales. Despite its diverse range of implications in the environment, little understanding of the physiological role of DMSP in the cell exists. Here, we report the physiological response of a non-DMSP-producing diatom Thalassiosira weissflogii grown at different salinities (15, 35 and 55 ppt) in the presence and absence of DMSP. Hypersaline conditions (55 ppt) negatively affected growth rate and hyposaline conditions (15 ppt) caused an increase in cell volume, yet no effect was observed on the photophysiological state of the algae, demonstrating a broad salinity tolerance in T. weissflogii. Addition of DMSP and subsequent uptake by T. weissflogii had no effect on the salinity-induced symptoms. Importantly, using a non-DMSP-producing diatom, we observed some of the first direct evidence of the intracellular role of DMSP as an antioxidant through the quenching of damaging reactive oxygen species (ROS), which based on its pattern, was likely due to the growth phase of the culture. This study confirms the utility of T. weissflogii as a model organism for DMSP-related physiological studies, with results revealing that DMSP accumulation reduces growth-related reactive oxygen in T. weissflogii.


Data Availability
The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.
References
Curson ARJ, Todd JD, Sullivan MJ, Johnston AWB (2011) Catabolism of dimethylsulphoniopropionate: microorganisms, enzymes and genes. Nat Rev Microbiol 9:849–859. https://doi.org/10.1038/nrmicro2653
Curson ARJ, Liu J, Bermejo Martínez A, Green RT, Chan Y, Carrión O, Williams BT, Zhang S-H, Yang G-P, Bulman Page PC, Zhang X-H, Todd JD (2017) Dimethylsulfoniopropionate biosynthesis in marine bacteria and identification of the key gene in this process. Nat Microbiol 2:17009. https://doi.org/10.1038/nmicrobiol.2017.9
Darroch LJ, Lavoie M, Levasseur M, Laurion I, Sunda WG, Michaud S, Scarratt M, Gosselin M, Caron G (2015) Effect of short-term light- and UV-stress on DMSP, DMS, and DMSP lyase activity in Emiliania huxleyi. Aquat Microb Ecol 74:173–185
Deschaseaux ESM, Jones GB, Deseo MA, Shepherd KM, Kiene RP, Swan HB, Harrison PL, Eyre BD (2014) Effects of environmental factors on dimethylated sulfur compounds and their potential role in the antioxidant system of the coral holobiont. Limnol Oceanogr 59:758–768. https://doi.org/10.4319/lo.2014.59.3.0758
Deschaseaux E, O'Brien J, Siboni N, Petrou K, Seymour JR (2019) Shifts in dimethylated sulfur concentrations and microbiome composition in the red-tide causing dinoflagellate Alexandrium minutum during a simulated marine heatwave. Biogeosciences 16:4377–4391
R Development Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing. Retrieved from https://www.R-project.org/. Vienna, Austria
Dickson DMJ, Kirst GO (1986) The role of β-dimethylsulphoniopropionate, glycine betaine and homarine in the osmoacclimation of Platymonas subcordiformis. Planta 167:536–543. https://doi.org/10.1007/BF00391230
García N, López-Elías JA, Miranda A, Martínez-Porchas M, Huerta N, García A (2012) Effect of salinity on growth and chemical composition of the diatom Thalassiosira weissflogii at three culture phases. Latin Am J Aqua Res 40:435–440
Gardner SG, Nielsen DA, Laczka O, Shimmon R, Beltran VH, Ralph PJ, Petrou K (2016) Dimethylsulfoniopropionate, superoxide dismutase and glutathione as stress response indicators in three corals under short-term hyposalinity stress. Proc R Soc B Biol Sci 283:20152418. https://doi.org/10.1098/rspb.2015.2418
Gardner SG, Raina J-B, Nitschke MR, Nielsen DA, Stat M, Motti CA, Ralph PJ, Petrou K (2017a) A multi-trait systems approach reveals a response cascade to bleaching in corals. BMC Biol 15:117. https://doi.org/10.1186/s12915-017-0459-2
Gardner SG, Raina J-B, Ralph PJ, Petrou K (2017b) Reactive oxygen species (ROS) and dimethylated sulphur compounds in coral explants under acute thermal stress. J Exp Biol 220:1787–1791. https://doi.org/10.1242/jeb.153049
Guillard RR, Ryther JH (1962) Studies of marine planktonic diatoms I. Cyclotella nana Hudstedt and Detonula confervacea Cleve. Can J Microbiol 8:229–239
Hillebrand H, Durselen C, Kirschtel D, Pollinger U, Zohary T (1999) Biovolume calculation for pelagic and benthic microalgae. J Phycol 35:403–424
Johnston AW, Green RT, Todd JD (2016) Enzymatic breakage of dimethylsulfoniopropionate—a signature molecule for life at sea. Curr Opin Chem Biol 31:58–65
Keller MD (1989) Dimethyl sulfide production and marine phytoplankton: the importance of species composition and cell size. Biol Oceanogr 6:375–382
Kettles NL, Kopriva S, Malin G (2014) 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 Nitrogen PLOS One 9:e94795. https://doi.org/10.1371/journal.pone.0094795
Kiene RP, Slezak D (2006) Low dissolved DMSP concentrations in seawater revealed by small-volume gravity filtration and dialysis sampling. Limnol Oceanogr Methods 4:80–95
Kiene R, Linn L, Bruten J (2000) New and important roles for DMSP in marine microbial communities. J Sea Res 43:209–224
Kirst GO (1989) Salinity tolerance of eukaryotic marine algae. Annu Rev Plant Physiol Plant Mol Biol 40:21–53
Lavoie M, Waller JC, Kiene RP, Levasseur M (2018) Polar marine diatoms likely take up a small fraction of dissolved dimethylsulfoniopropionate relative to bacteria in oligotrophic environments. Aquat Microb Ecol 81:213–218
Lyon BR, Lee PA, Bennett JM, DiTullio GR, Janech MG (2011) Proteomic analysis of a sea-ice diatom: salinity acclimation provides new insight into the dimethylsulfoniopropionate production pathway. Plant Physiol 157:1926–1941. https://doi.org/10.1104/pp.111.185025
Matrai PA, Keller MD (1994) Total organic sulfur and dimethylsulfoniopropionate in marine phytoplankton: intracellular variations. Mar Biol 119:61–68. https://doi.org/10.1007/BF00350107
Matrai PA, Vernet M, Hood R, Jennings A, Brody E, Saemundsdóttir S (1995) Light-dependence of carbon and sulfur production by polar clones of the genus Phaeocystis. Mar Biol 124:157–167. https://doi.org/10.1007/BF00349157
McParland EL, Wright A, Art K, He M, Levine NM (2020) Evidence for contrasting roles of dimethylsulfoniopropionate production in Emiliania huxleyi and Thalassiosira oceanica. New Phytol 226(2):396–409. https://doi.org/10.1111/nph.16374
Petrou K, Nielsen DA (2018) Uptake of dimethylsulphoniopropionate (DMSP) by the diatom Thalassiosira weissflogii: a model to investigate the cellular function of DMSP. Biogeochemistry 141:265–271. https://doi.org/10.1007/s10533-018-0507-1
Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods 9:676–682
Schreiber U (2004) Pulse-amplitude-modulated (PAM) fluorometry and saturation pulse method. In: Papagiorgiou GG (ed) Advances in photosynthesis and respiration. Springer, Dordrecht, pp 279–319
Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot
Sheehan CE, Petrou K (2020) Dimethylated sulfur production in batch cultures of Southern Ocean phytoplankton. Biogeochemistry 147:53–69. https://doi.org/10.1007/s10533-019-00628-8
Spielmeyer A, Gebser B, Pohnert G (2011) Investigations of the uptake of dimethylsulfoniopropionate by phytoplankton. Chem Bio Chem 12:2276–2279
Stefels J (2000) Physiological aspects of the production and conversion of DMSP in marine algae and higher plants. J Sea Res 43:183–197
Sunda W, Kieber D, Kiene R, Huntsman S (2002) An antioxidant function for DMSP and DMS in marine algae. Nature 418:317–320
Vila-Costa M, Simo R, Harada H, Gasol JM, Slezak D, Kiene RP (2006) Dimethylsulfoniopropionate uptake by marine phytoplankton. Science 314:652–654
Welsh DT (2000) Ecological significance of compatible solute accumulation by micro-organisms: from single cells to global climate. FEMS Microbiol Rev 24:263–290
Yoch DC (2002) Dimethylsulfoniopropionate: its sources, role in the marine food web, and biological degradation to dimethylsulfide. Appl Environ Microbiol 68:5804–5815. https://doi.org/10.1128/aem.68.12.5804-5815.2002
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Funding for this research was provided by the School of Life Sciences, University of Technology Sydney.
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DAN, KP designed the experiments, AMT performed experiments, AMT, DAN and KP analysed data, AMT, DAN and KP wrote the manuscript.
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Theseira, A.M., Nielsen, D.A. & Petrou, K. Uptake of dimethylsulphoniopropionate (DMSP) reduces free reactive oxygen species (ROS) during late exponential growth in the diatom Thalassiosira weissflogii grown under three salinities. Mar Biol 167, 127 (2020). https://doi.org/10.1007/s00227-020-03744-4
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DOI: https://doi.org/10.1007/s00227-020-03744-4