Published September 30, 2022 | Version v1
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Metabolic adaptation of diatoms to hypersalinity

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Nikitashina, Vera, Stettin, Daniel, Pohnert, Georg (2022): Metabolic adaptation of diatoms to hypersalinity. Phytochemistry 201: 113267, DOI: 10.1016/j.phytochem.2022.113267, URL: http://dx.doi.org/10.1016/j.phytochem.2022.113267

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urn:lsid:plazi.org:pub:C271FF992D44B2716077FFA8FFFE9F08

References

  • Adams, P., Thomas, J.C., Vernon, D.M., Bohnert, H.J., Jensen, R.G., 1992. Distinct cellular and organismic responses to salt stress. Plant Cell Physiol. 33, 1215-1223. https://doi.org/10.1093/oxfordjournals.pcp.a078376.
  • Armbrust, E.V., Berges, J.A., Bowler, C., Green, B.R., Martinez, D., Putnam, N.H., Zhou, S., Allen, A.E., Apt, K.E., Bechner, M., Brzezinski, M.A., Chaal, B.K., Chiovitti, A., Davis, A.K., Demarest, M.S., Detter, J.C., Glavina, T., Goodstein, D., Hadi, M.Z., Hellsten, U., Hildebrand, M., Jenkins, B.D., Lau, W.W.Y., Lane, T.W., Larimer, F.W., Lippmeier, J.C., Lucas, S., Montsant, A., Obornik, M., Parker, M.S., Palenik, B., Pazour, G.J., Richardson, P.M., Rynearson, T.A., Saito, M.A., Schwartz, D.C., Thamatrakoln, K., Valentin, K., Vardi, A., Wilkerson, F.P., Rokhsar, D.S., 2004. The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science 306, 79-87. https://doi.org/10.1126/ science.1101156.
  • Bergeijk, S.A. Van, Zee, C. Van Der, Stal, L.J., 2003. Uptake and excretion of dimethylsulphoniopropionate is driven by salinity changes in the marine benthic diatom Cylindrotheca closterium. Eur. J. Phycol. 38, 341-349. https://doi.org/ 10.1080/09670260310001612600.
  • Blunden, G., Smith, B.E., Irons, M.W., Yang, M.-H., Roch, O.G., Patel, A.V., 1992. Betaines and tertiary sulphonium compounds from 62 species of marine algae. Biochem. Systemat. Ecol. 20, 373-388. https://doi.org/10.1016/0305-1978(92) 90050-N.
  • B¨ocker, S., Duhrkop, K., 2016. Fragmentation trees reloaded. J. Cheminf. 8, 1-26. https://doi.org/10.1186/s13321-016-0116-8.
  • Bowler, C., Allen, A.E., Badger, J.H., Grimwood, J., Jabbari, K., Kuo, A., Maheswari, U., Martens, C., Maumus, F., Otillar, R.P., Rayko, E., Salamov, A., Vandepoele, K., Beszteri, B., Gruber, A., Heijde, M., Katinka, M., Mock, T., Berges, J.A., Brownlee, C., Cadoret, J., Chiovitti, A., Valentin, K., Choi, C.J., Coesel, S., Martino, A. De, Detter, J. C., Durkin, C., Falciatore, A., Lopez, P.J., Lucas, S., Lindquist, E., Lommer, M., Napoli, C., Obornik, M., Parker, M.S., Petit, J., Porcel, B.M., 2008. The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature 456, 239-244. https://doi.org/10.1038/nature07410.
  • Branda, L.E., 1984. The salinity tolerance of forty-six marine phytoplankton isolates. Estuar. Coast Shelf Sci. 18, 543-556. https://doi.org/10.1016/0272-7714(84) 90089-1.
  • Chong, J., Soufan, O., Li, C., Caraus, I., Li, S., Bourque, G., Wishart, D.S., Xia, J., 2018. MetaboAnalyst 4.0: towards more transparent and integrative metabolomics analysis. Nucleic Acids Res. 46, 486-494. https://doi.org/10.1093/nar/gky310.
  • Czech, L., Hermann, L., St¨oveken, N., Richter, A.A., Id, A.H., Smits, S.H.J., Heider, J., Bremer, E., 2018. Role of the extremolytes ectoine and hydroxyectoine as stress protectants and nutrients: genetics, phylogenomics, biochemistry, and structural analysis. Genes 9, 1-58. https://doi.org/10.3390/genes9040177.
  • Dawson, H.M., Heal, K.R., Boysen, A.K., Carlson, L.T., Ingalls, A.E., Young, J.N., 2020. Potential of temperature- and salinity-driven shifts in diatom compatible solute concentrations to impact biogeochemical cycling within sea ice. Elem. Sci. Anthr. 8, 25. https://doi.org/10.1525/elementa.421.
  • Dickson, D.M., Kirst, G.O., 1987. Osmotic adjustment in marine eukaryotic algae: the role of inorganic ions, quaternary ammonium, tertiary sulphonium and carbohydrate solutes. New Phytol. 106, 645-655. https://doi.org/10.1111/j.1469-8137.1987. tb00165.x.
  • Downing, A.B., Wallace, G.T., Yancey, P.H., 2018. Organic osmolytes of amphipods from littoral to hadal zones: increases with depth in trimethylamine N-oxide , scylloinositol and other potential pressure counteractants. Deep. Res. Part I 138, 1-10. https://doi.org/10.1016/j.dsr.2018.05.008.
  • Durack, P.J., Wijffels, S.E., 2010. Fifty-year trends in global ocean salinities and their relationship to broad-scale warming. J. Clim. 23, 4342-4362. https://doi.org/ 10.1175/2010JCLI3377.1.
  • Duhrkop, K., Fleischauer, M., Ludwig, M., Aksenov, A.A., Melnik, A.V., Meusel, M., Dorrestein, P.C., Rousu, J., B¨ocker, S., 2019. Sirius 4: a rapid tool for turning tandem mass spectra into metabolite structure information. Nat. Methods 16, 299-302. https://doi.org/10.1038/s41592-019-0344-8.
  • Duhrkop, K., Shen, H., Meusel, M., Rousu, J., Bocker ¨, S., 2015. Searching molecular structure databases with tandem mass spectra using CSI:FingerID. Proc. Natl. Acad. Sci. Unit. States Am. 112, 12580-12585. https://doi.org/10.1073/ pnas.1509788112.
  • Fenizia, S., Thume, K., Wirgenings, M., Pohnert, G., 2020. Ectoine from bacterial and algal origin is a compatible solute in microalgae. Mar. Drugs 18, 1-13. https://doi. org/10.3390/md18010042.
  • Field, C.B., Behrenfeld, M.J., Randerson, J.T., Falkowski, P., 1998. Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281, 237-240. https://doi.org/10.1126/science.281.5374.237.
  • Fukutoku, Y., Yamada, Y., 1981. Sources of proline-nitrogen in water-stressed soybean (Glycine max L.) I. protein metabolism and proline accumulation. Plant Cell Physiol. 22, 1397-1404. https://doi.org/10.1093/oxfordjournals.pcp.a076292.
  • Garcia, N., L´opez-elias, J.A., Miranda, A., Martinez-Porchas, M., Huerta, N., Garcia, A., 2012. Effect of salinity on growth and chemical composition of the diatom Thalassiosira weissflogii at three culture phases. Lat. Am. J. Aquat. Res. 40, 435-440. https://doi.org/10.3856/vol40-issue2-fulltext-18.
  • Gebser, B., Pohnert, G., 2013. Synchronized regulation of different zwitterionic metabolites in the osmoadaption of phytoplankton. Mar. Drugs 11, 2168-2182. https://doi.org/10.3390/md11062168.
  • Gilmour, D.J., Hipkins, M.F., Boney, A.D., 1982. The effect of salt stress on the primary processes of photosynthesis in Dunaliella tertiolecta. Plant Sci. Lett. 26, 325-330. https://doi.org/10.1016/0304-4211(82)90107-9.
  • Gilmour, D.J., Hipkins, M.F., Webber, A.N., Baker, N.R., Boney, A.D., 1985. The effect of ionic stress on photosynthesis in Dunaliella tertiolecta. Chlorophyll fluorescence kinetics and spectral characteristics. Planta 163, 250-256. https://doi.org/10.1007/ BF00393515.
  • Glaser, K., Karsten, U., 2020. Salinity tolerance in biogeographically different strains of the marine benthic diatom Cylindrotheca closterium (Bacillariophyceae). J. Appl. Phycol. 32, 3809-3816. https://doi.org/10.1007/s10811-020-02238-6.
  • Hellebust, J.A., 1976. Osmoregulation. Annu. Rev. Plant Physiol. 27, 485-505. https:// doi.org/10.1146/annurev. .27.060176.002413.
  • Hulsen, T., Vlieg, J. De, Alkema, W., 2008. BioVenn - a web application for the comparison and visualization of biological lists using area-proportional Venn diagrams. BMC Genom. 9, 1-6. https://doi.org/10.1186/1471-2164-9-488.
  • Jaramillo-Madrid, A.C., Ashworth, J., Ralph, P.J., 2020. Levels of diatom minor sterols respond to changes in temperature and salinity. J. Mar. Sci. Eng. 8, 1-14. https:// doi.org/10.3390/jmse8020085.
  • Johansson, O.N., T¨opel, M., Pinder, M.I.M., Kourtchenko, O., Blomberg, A., Godhe, A., Clarke, A.K., 2019. Skeletonema marinoi as a new genetic model for marine chainforming diatoms. Nat. Sci. Reports 9, 1-10. https://doi.org/10.1038/s41598-019- 41085-5.
  • Joshi, V., Fei, Z., Joung, J., Jander, G., 2010. Interdependence of threonine, methionine and isoleucine metabolism in plants accumulation and transcriptional regulation under abiotic stress. Amino Acids 39, 933-947. https://doi.org/10.1007/s00726- 010-0505-7.
  • Kanehisa, M., Goto, S., 2000. KEGG : kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 28, 27-30. https://doi.org/10.1093/nar/28.1.27.
  • Keller, M.D., Kiene, R.P., Matrai, P.A., Bellows, W.K., 1999. Production of glycine betaine and dimethylsulfoniopropionate in marine phytoplankton. I. Batch cultures. Mar. Biol. 135, 237-248. https://doi.org/10.1007/s002270050621.
  • Kets, E.P.W., Bont, J.A.M. De, 1997. Effect of carnitines on Lactobacillus plantarum subjected to osmotic stress. FEMS Microbiol. Lett. 146, 205-209. https://doi.org/ 10.1111/j.1574-6968.1997.tb10194.x.
  • Kim, K.H., Jia, B., Jeon, C.O., 2017. Identification of trans-4-hydroxy-l-proline as a compatible solute and its biosynthesis and molecular characterization in Halobacillus halophilus. Front. Microbiol. 8, 1-11. https://doi.org/10.3389/fmicb.2017.02054.
  • Kirst, G.O., 1989. Salinity tolerance of eukaryotic marine algae. Annu. Rev. Plant Physiol. Plant Mol. Biol. 40, 21-53. https://doi.org/10.1146/annurev, 41.060190.000321.
  • Kissoudis, C., Kalloniati, C., Flemetakis, E., Madesis, P., Labrou, N.E., Tsaftaris, A., Nianiou-Obeidat, I., 2015. Stress-inducible GmGSTU4 shapes transgenic tobacco plants metabolome towards increased salinity tolerance. Acta Physiol. Plant. 37, 102. https://doi.org/10.1007/s11738-015-1852-5.
  • Klages, K., Boldings, H., Smith, G.S., 1999. Accumulation of myo-inositol in Actinidia seedlings subjected to salt stress. Ann. Bot. 84, 521-527. https://doi.org/10.1006/ anbo.1999.0946.
  • Kuhl, C., Tautenhahn, R., Bo, C., Larson, T.R., Neumann, S., 2012. CAMERA: an integrated strategy for compound spectra extraction and annotation of liquid chromatography/mass spectrometry data sets. Anal. Chem. 84, 283-289. https:// doi.org/10.1021/ac202450g.
  • Landa, M., Burns, A.S., Roth, S.J., Moran, M.A., 2017. Bacterial transcriptome remodeling during sequential co-culture with a marine dinoflagellate and diatom. ISME J. 11, 2677-2690. https://doi.org/10.1038/ismej.2017.117.
  • Laws, E.A., 2013. Evaluation of in situ phytoplankton growth rates: a synthesis of data from varied approaches. Ann. Rev. Mar. Sci 5, 247-268. https://doi.org/10.1146/ annurev-marine-121211-172258.
  • Leimer, K.R., Rice, R.H., Gehrke, C.W., 1977. Complete mass spectra of the pertrimethylsilylated amino acids. J. Chromatogr. A 141, 355-375. https://doi.org/ 10.1016/S0021-9673(00)93539-8.
  • Liu, M.S., Hellebust, J.A., 1976. Regulation of proline metabolism in the marine centric diatom Cyclotella cryptica. Can. J. Bot. 54, 949-959. https://doi.org/10.1139/b76- 099.
  • Luan, H., Ji, F., Chen, Y., Cai, Z., 2018. statTarget: a streamlined tool for signal drift correction and interpretations of quantitative mass spectrometry-based omics data. Anal. Chim. Acta 1036, 66-72. https://doi.org/10.1016/j.aca.2018.08.002.
  • Maier, I., Calenberg, M., 1994. Effect of extracellular Ca2+ and Ca2+ -antagonists on the movement and chemoorientation of male gametes of Ectocarpus siliculosus (Phaeophyceae). Bot. Acta 107, 451-460. https://doi.org/10.1111/j.1438- 8677.1994.tb00820.x.
  • Martino, A. De, Meichenin, A., Shi, J., Pan, K., Bowler, C., 2007. Genetic and phenotypic characterization of Phaeodactylum tricornutum (Bacillariophyceae) accessions. J. Phycol. 43, 992-1009. https://doi.org/10.1111/j.1529-8817.2007.00384.x.
  • Medlin, L.K., Kaczmarska, I., 2004. Evolution of the diatoms: V. Morphological and cytological support for the major clades and a taxonomic revision. Phycologia 43, 245-270. https://doi.org/10.2216/i0031-8884-43-3-245.1.
  • Mentzen, W.I., Peng, J., Ransom, N., Nikolau, B.J., Wurtele, E.S., 2008. Articulation of three core metabolic processes in Arabidopsis: fatty acid biosynthesis, leucine catabolism and starch metabolism. BMC Plant Biol. 8, 1-15. https://doi.org/ 10.1186/1471-2229-8-76.
  • Mimura, H., Nagata, S., Matsumoto, T., 1994. Concentrations and compositions of internal free amino acids in a halotolerant Brevibacterium sp. in response to salt stress. Biosci. Biotechnol. Biochem. 58, 1873-1874. https://doi.org/10.1271/ bbb.58.1873.
  • Moulin, M., Deleu, C., Larher, F., 2000. L-Lysine catabolism is osmo-regulated at the level of lysine-ketoglutarate reductase and saccharopine dehydrogenase in rapeseed leaf discs. Plant Physiol. Biochem. 38, 577-585. https://doi.org/10.1016/S0981-9428 (00)00777-4.
  • Neshich, I.A.P., Kiyota, E., Arruda, P., 2013. Genome-wide analysis of lysine catabolism in bacteria reveals new connections with osmotic stress resistance. ISME J. 7, 2400-2410. https://doi.org/10.1038/ismej.2013.123.
  • Ochsenkuhn, M.A., R¨othig, T., D' Angelo, C., Wiedenmann, J., Voolstra, C.R., 2017. The role of floridoside in osmoadaptation of coral-associated algal endosymbionts to high-salinity conditions. Sci. Adv. 3, e1602047 https://doi.org/10.1126/ sciadv.1602047.
  • Peters, P., Galinski, E.A., Truper, H.G., 1990. The biosynthesis of ectoine. FEMS Microbiol. Lett. 71, 157-162. https://doi.org/10.1111/j.1574-6968.1990.tb03815. x.
  • Rijstenbil, J.W., 2003. Effects of UVB radiation and salt stress on growth, pigments and antioxidative defence of the marine diatom Cylindrotheca closterium. Mar. Ecol. Prog. Ser. 254, 37-47.
  • Ruttkies, C., Schymanski, E.L., Wolf, S., Hollender, J., Neumann, S., 2016. MetFrag relaunched: incorporating strategies beyond in silico fragmentation. J. Cheminf. 8, 1-16. https://doi.org/10.1186/s13321-016-0115-9.
  • Scholz, B., Liebezeit, G., 2012. Compatible solutes in three marine intertidal microphytobenthic Wadden Sea diatoms exposed to different salinities. Eur. J. Phycol. 47, 393-407. https://doi.org/10.1080/09670262.2012.720714.
  • Smith, C.A., Want, E.J., O' Maille, G., Abagyan, R., Siuzdak, G., 2006. XCMS: processing mass spectrometry data for metabolite profiling using nonlinear peak alignment, matching, and identification. Anal. Chem. 78, 779-787. https://doi.org/10.1021/ ac051437y.
  • Stettin, D., Poulin, R.X., Pohnert, G., 2020. Metabolomics benefits from GC Orbitrap - comparison of low- and high-resolution GC-MS. Metabolites 10, 143. https://doi. org/10.3390/metabo10040143.
  • Sugie, K., Fujiwara, A., Nishino, S., Kameyama, S., Harada, N., 2020. Impacts of temperature, CO2, and salinity on phytoplankton community composition in the western Arctic Ocean. Front. Mar. Sci. 6, 821. https://doi.org/10.3389/ fmars.2019.00821.
  • Thomas, M.K., Kremer, C.T., Klausmeier, C.A., Litchman, E., 2012. A global pattern of thermal adaptation in marine phytoplankton. Science 338, 1085-1088. https://doi. org/10.1126/science.1224836.
  • Thume, K., Gebser, B., Chen, L., Meyer, N., Kieber, D.J., Pohnert, G., 2018. The metabolite dimethylsulfoxonium propionate extends the marine organosulfur cycle. Nature 563, 412-415. https://doi.org/10.1038/s41586-018-0675-0.
  • Trinchant, J., Boscari, A., Spennato, G., Sype, G. Van De, Rudulier, D. Le, 2004. Proline betaine accumulation and metabolism in alfalfa plants under sodium chloride stress. Exploring its compartmentalization in nodules. Plant Physiol. 135, 1583-1594. https://doi.org/10.1104/pp.103.037556.1.
  • Tsugawa, H., Kind, T., Nakabayashi, R., Yukihira, D., Tanaka, W., Cajka, T., Saito, K., Fiehn, O., Arita, M., 2016. Hydrogen rearrangement rules: computational ms/ms fragmentation and structure elucidation using MS-FINDER software. Anal. Chem. 88, 7946-7958. https://doi.org/10.1021/acs.analchem.6b00770.
  • Vidal, T., Calado, A.J., Moita, M.T., Cunha, M.R., 2017. Phytoplankton dynamics in relation to seasonal variability and upwelling and relaxation patterns at the mouth of Ria de Aveiro (West Iberian Margin) over a four-year period. PLoS One 12, 1-25. https://doi.org/10.1371/journal.pone.0177237.
  • Vidoudez, C., Pohnert, G., 2012. Comparative metabolomics of the diatom Skeletonema marinoi in different growth phases. Metabolomics 8, 654-669. https://doi.org/ 10.1007/s11306-011-0356-6.
  • Wehrens, R., Weingart, G., Mattivi, F., 2014. metaMS : an open-source pipeline for GC - MS-based untargeted metabolomics. J. Chromatogr. B 966, 109-116. https://doi.
  • Weinisch, L., Ku, S., Roth, R., Grimm, M., Roth, T., Daili, J., Netz, A., Pierik, A.J., Filker, S., 2018. Identification of osmoadaptive strategies in the halophile, heterotrophic ciliate Schmidingerothrix salinarum. PLoS Biol. 16, 1-29. https://doi.
  • Yamamoto, M., Chiba, T., Tuji, A., 2017. Salinity responses of benthic diatoms inhabiting tidal flats. Diatom Res. 32, 243-250. https://doi.org/10.1080/ 0269249X.2017.1366951.
  • Yancey, P.H., 2005. Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses. J. Exp. Biol. 208, 2819-2830. https://doi.org/10.1242/jeb.01730.
  • Zhang, J., Chen, G., Zhao, P., Zhou, Q., Zhao, X., 2017. The abundance of certain metabolites responds to drought stress in the highly drought tolerant plant Caragana korshinskii. Acta Physiol. Plant. 39, 116. https://doi.org/10.1007/s11738-017-2412- y.
  • Zhang, J., Yang, D., Li, M., Shi, L., 2016. Metabolic profiles reveal changes in wild and cultivated soybean seedling leaves under salt stress. PLoS One 11, 1-17. https://doi. org/10.1371/journal.pone.0159622.
  • Zika, J.D., Skliris, N., Blaker, A.T., Marsh, R., Nurser, A.J.G., Josey, S.A., 2018. Improved estimates of water cycle change from ocean salinity: the key role of ocean warming. Environ. Res. Lett. 13, 074036 https://doi.org/10.1088/1748-9326/aace42.