No abstract

Osmoregulation in phytoplankton is attributed to several highly polar low-molecular-weight metabolites. A widely accepted model considers dimethylsulfoniopropionate (DMSP) as the most important and abundant osmotically active metabolite. Using an optimized procedure for the extraction and detection of highly polar metabolites, we expand the group of phytoplankton osmolytes by identifying ectoine in several microalgae. Ectoine is known as a bacterial compatible solute, but, to the best of our knowledge, was never considered as a phytoplankton-derived product. Given the ability of microalgae to take up zwitterions, such as DMSP, we tested the hypothesis that the algal ectoine is derived from associated bacteria. We therefore analyzed methanol extracts of xenic and axenic cultures of two different species of microalgae and could detect elevated concentrations of ectoine in those that harbor associated bacteria. However, also microalgae without an associated microbiome contain ectoine in smaller amounts, pointing towards a dual origin of this metabolite in the algae from their own biosynthesis as well as from uptake. We also tested the role of ectoine in the osmoadaptation of microalgae. In the model diatoms Thalassiosira weissflogii and Phaeodactylum tricornutum, elevated amounts of ectoine were found when cultivated in seawater with salinities of 50 PSU compared to the standard culture conditions of 35 PSU. Therefore, we add ectoine to the family of osmoadaptive metabolites in phytoplankton and prove a new, potentially synergistic metabolic interplay of bacteria and algae.

The marine sulfur cycle is substantially fueled by the phytoplankton osmolyte dimethylsulfoniopropionate (DMSP). This metabolite can be metabolized by bacteria, which results in the emission of the volatile sulfur species methanethiol (MeSH) and the climate‐cooling dimethylsulfide (DMS). It is generally accepted that bacteria contribute significantly to DMSP turnover. We show that the other low molecular weight zwitterionic dimethylsulfonio compounds dimethylsulfonioacetate (DMSA) and gonyol are also widely distributed in phytoplankton and can serve as alternative substrates for volatile production. DMSA was found in 11 of the 16 surveyed phytoplankton species, and gonyol was detected in all haptophytes and dinoflagellates. These prevalent zwitterions are also metabolized by marine bacteria. The patterns of bacterial MeSH and DMS release were dependent on the zwitterions present. Certain bacteria metabolize DMSA and gonyol and release MeSH, in others gonyol inhibited DMS‐producing enzymes. If added in addition to DMSP, gonyol entirely inhibited the formation of volatiles in Ruegeria pomeroyi. In contrast, no substantial effect of this compound was observed in the DMSP metabolism of Halomonas sp. We argue that the production of DMSA and gonyol and their inhibitory properties on the release of volatiles from DMSP has the potential to modulate planktonic sulfur cycling between species.

Dimethylsulfide (DMS) is produced by phytoplankton in the ocean and plays an important role in biogeochemical cycles and climate system of the Earth. Previous field studies reported a possible relationship between DMS enhancement and anoxic condition, although the governing processes are still to be identified. Here we show the first direct evidence for the enhancement of DMS production by natural planktonic assemblages caused by anoxic stress. Under the anoxic condition, DMS production was considerably enhanced and DMS bacterial consumption was inhibited, resulting in an eightfold higher rate of gross DMS production than that under the oxic condition. Our results demonstrated that anoxic stress is one of important “environmental factors” in the marine DMS dynamics, suggesting the possible global importance due to ubiquity of anoxic conditions in the coastal oceans. This process would become more important in the future due to expansion of coastal hypoxic and anoxic zones by global warming.

Chemically modified diatom cell walls represent a powerful tool to support ionization in LDI MS. The lack of background signals in the low molecular weight region of the mass spectra allows also the investigations of small analytes.