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Signals or resources? : biosynthesis and accumulation of zwitterionic compatible solutes in marine phytoplankton and their role in environmental stress responses

Marine phytoplankton are among the main sources of the zwitterionic sulfur compound dimethylsulfoniopropionate (DMSP). Although the several functions of this metabolite in marine algae have largely been demonstrated, knowledge related to the environmental drivers of DMSP catabolism was still missing. In this work, the application of analytical and physiological methods enabled the exploration of conditions involved in DMSP degradation and its conversion into dimethylsulfide (DMS). Salinity and temperature affect biotic interactions and living organisms, which synthesize and accumulate organic metabolites with osmoregulatory and cryoprotectant properties, including DMSP, to mitigate adverse environmental conditions. Through analytical methods based on ultra-high-performance-liquid chromatography (UHPLC) and high-resolution-mass spectrometry (HRMS), we investigated further and expanded the group of phytoplankton osmolytes by adding cysteinolic acid and ectoine: their identities were confirmed through MS/MS experiments and co-elution with the corresponding synthetic standards, while their osmoregulatory properties were verified by investigating the algal cells at physiological and high salinity conditions. We also expanded our investigation on ectoine and cysteinolic acid distribution to the class of marine macroalgae by including in our screening the green seaweed Ulva sp. We investigated the cryoprotectant properties of ectoine and cysteinolic acid in these species. Interestingly, our results showed that both these metabolites were upregulated in U. mutabilis after a warm to cold temperature shift, thus demonstrating their role in thermotolerance. With our work, we therefore added ectoine and cysteinolic acid to the family of key compatible solutes produced by marine phytoplankton and provided new insights into the molecular responses of marine algae to environmental stressors.

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