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...

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Main Authors: Björn Gebser, Kathleen Thume, Michael Steinke, Georg Pohnert
Format: Article
Language:English
Published: Wiley 2020-05-01
Series:MicrobiologyOpen
Subjects:
Online Access:https://doi.org/10.1002/mbo3.1014
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author Björn Gebser
Kathleen Thume
Michael Steinke
Georg Pohnert
author_facet Björn Gebser
Kathleen Thume
Michael Steinke
Georg Pohnert
author_sort Björn Gebser
collection DOAJ
description 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.
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spelling doaj.art-b3c052c1677240d3880d3c112fcb6e3d2022-12-22T01:59:44ZengWileyMicrobiologyOpen2045-88272020-05-0195n/an/a10.1002/mbo3.1014Phytoplankton‐derived zwitterionic gonyol and dimethylsulfonioacetate interfere with microbial dimethylsulfoniopropionate sulfur cyclingBjörn Gebser0Kathleen Thume1Michael Steinke2Georg Pohnert3Institute for Inorganic and Analytical Chemistry Friedrich Schiller University Jena Jena GermanyInstitute for Inorganic and Analytical Chemistry Friedrich Schiller University Jena Jena GermanySchool of Life Sciences University of Essex Colchester UKInstitute for Inorganic and Analytical Chemistry Friedrich Schiller University Jena Jena GermanyAbstract 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.https://doi.org/10.1002/mbo3.1014dimethylsulfoniopropionategonyolinhibitionmetabolismvolatile sulfur species
spellingShingle Björn Gebser
Kathleen Thume
Michael Steinke
Georg Pohnert
Phytoplankton‐derived zwitterionic gonyol and dimethylsulfonioacetate interfere with microbial dimethylsulfoniopropionate sulfur cycling
MicrobiologyOpen
dimethylsulfoniopropionate
gonyol
inhibition
metabolism
volatile sulfur species
title Phytoplankton‐derived zwitterionic gonyol and dimethylsulfonioacetate interfere with microbial dimethylsulfoniopropionate sulfur cycling
title_full Phytoplankton‐derived zwitterionic gonyol and dimethylsulfonioacetate interfere with microbial dimethylsulfoniopropionate sulfur cycling
title_fullStr Phytoplankton‐derived zwitterionic gonyol and dimethylsulfonioacetate interfere with microbial dimethylsulfoniopropionate sulfur cycling
title_full_unstemmed Phytoplankton‐derived zwitterionic gonyol and dimethylsulfonioacetate interfere with microbial dimethylsulfoniopropionate sulfur cycling
title_short Phytoplankton‐derived zwitterionic gonyol and dimethylsulfonioacetate interfere with microbial dimethylsulfoniopropionate sulfur cycling
title_sort phytoplankton derived zwitterionic gonyol and dimethylsulfonioacetate interfere with microbial dimethylsulfoniopropionate sulfur cycling
topic dimethylsulfoniopropionate
gonyol
inhibition
metabolism
volatile sulfur species
url https://doi.org/10.1002/mbo3.1014
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