Phytoplankton‐derived zwitterionic gonyol and dimethylsulfonioacetate interfere with microbial dimethylsulfoniopropionate sulfur cycling

Abstract

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.

Glycine betaine uptake and metabolism in marine microbial communities

“…Though DMSP can be made by heterotrophic bacteria that expressed bhmt in this region (Fig. 4), gonyol synthesis seems to be restricted to eukaryotic plankton (Nakamura et al ., 1993; Gebser et al ., 2020; Heal et al ., 2021, Durham et al ., submitted). The appearance of labelled gonyol therefore suggests that either there is a bacterial gonyol source or that some of the unverified eukaryotic bhmt homologues we excluded from our gene expression searches are functional and may include dinoflagellates, as they are considered the main gonyol producers (Gebser et al ., 2020; Heal et al ., 2021).…”

Marine Community Metabolomes Carry Fingerprints of Phytoplankton Community Composition

“…S3 ). Both of these compounds share structural similarity with DMSP and disrupt bacterial DMSP degradation pathways ( 51 ). Thus, predicting marine dimethyl sulfide (DMS) production from DMSP may be complicated by these highly abundant compounds.…”

Highly flexible metabolism of the marine euglenozoan protist Diplonema papillatum

“…Unusual metabolites identified by MS may shed further light on the role of diplonemids in the marine ecosystem. To our surprise, we have identified gonyol, which affects the marine sulfur cycle by modulating the release of methanethiol and dimethyl sulfide into the atmosphere [ 65 ]. The synthesis of gonyol was so far known only from photosynthesizing diatoms, dinoflagellates, and haptophytes [ 65 ] and, consequently, higher levels of the climate-influencing dimethyl sulfide occur in areas where an increased activity of phytoplankton was recorded [ 66 ].…”

“…To our surprise, we have identified gonyol, which affects the marine sulfur cycle by modulating the release of methanethiol and dimethyl sulfide into the atmosphere [ 65 ]. The synthesis of gonyol was so far known only from photosynthesizing diatoms, dinoflagellates, and haptophytes [ 65 ] and, consequently, higher levels of the climate-influencing dimethyl sulfide occur in areas where an increased activity of phytoplankton was recorded [ 66 ]. Hence, diplonemids are the first heterotrophs known to produce not only gonyol but also trigonelline, so far considered to be plant-specific [ 67 ].…”