Cysteinolic Acid Is a Widely Distributed Compatible Solute of Marine Microalgae.

Simona Fenizia,Jerrit Weissflog,Georg Pohnert

doi:10.3390/md19120683

Simona Fenizia, Jerrit Weissflog + Show 1 more

Open Access

https://doi.org/10.3390/md19120683

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Abstract

Phytoplankton rely on bioactive zwitterionic and highly polar small metabolites with osmoregulatory properties to compensate changes in the salinity of the surrounding seawater. Dimethylsulfoniopropionate (DMSP) is a main representative of this class of metabolites. Salinity-dependent DMSP biosynthesis and turnover contribute significantly to the global sulfur cycle. Using advanced chromatographic and mass spectrometric techniques that enable the detection of highly polar metabolites, we identified cysteinolic acid as an additional widely distributed polar metabolite in phytoplankton. Cysteinolic acid belongs to the class of marine sulfonates, metabolites that are commonly produced by algae and consumed by bacteria. It was detected in all dinoflagellates, haptophytes, diatoms and prymnesiophytes that were surveyed. We quantified the metabolite in different phytoplankton taxa and revealed that the cellular content can reach even higher concentrations than the ubiquitous DMSP. The cysteinolic acid concentration in the cells of the diatom Thalassiosira weissflogii increases significantly when grown in a medium with elevated salinity. In contrast to the compatible solute ectoine, cysteinolic acid is also found in high concentrations in axenic algae, indicating biosynthesis by the algae and not the associated bacteria. Therefore, we add this metabolite to the family of highly polar metabolites with osmoregulatory characteristics produced by phytoplankton.

Highlights

Free-floating phytoplankton in the open ocean contribute substantially to primary production
Besides DMSP, many other highly polar metabolites that can serve as compatible solutes have been discovered in phytoplankton
Xenic and axenic cultures of the diatom Thalassiosira weissflogii were grown under standard culture conditions of 35 Practical Salinity Units (PSU, g NaCl kg−1 seawater) and under increased salinity of 50 PSU to cover the effect of a substantial salinity increase according to previous studies [7,26,27]

Summary

Introduction

Free-floating phytoplankton in the open ocean contribute substantially to primary production. Cells respond by production/uptake or degradation/exudation of compatible solutes These polar organic compounds adjust the osmolality of the cells to that of the environment [4,5,6,7]. Dimethylsulfoniopropionate (DMSP) is a major compatible solute in many phytoplankton species The amount of this sulfur-containing zwitterionic metabolite produced globally by marine organisms is estimated to be around two petagrams per year [8,9]. The enzymatic cleavage of this osmolyte results in the release of the volatile dimethylsulfide (DMS) This metabolite contributes significantly (30 teragram per year) to the global sulfur flux from the hydrosphere to the atmosphere [10,11,12,13]. Besides DMSP, many other highly polar metabolites that can serve as compatible solutes have been discovered in phytoplankton. DMSOP is produced by phytoplankton and is readily taken up by marine bacteria, confirming that this class of molecules supports bacterial heterotrophy in the ocean [11,18,19]

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