Algae produce massive amounts of dimethylsulfoniopropionate (DMSP), which fuel the organosulfur cycle1,2. On a global scale, several petagrams of this sulfur species are produced annually, thereby driving fundamental processes and the marine food web1. An important DMSP transformation product is dimethylsulfide, which can be either emitted to the atmosphere3,4 or oxidized to dimethylsulfoxide (DMSO) and other products5. Here we report the discovery of a structurally unusual metabolite, dimethylsulfoxonium propionate (DMSOP), that is synthesized by several DMSP-producing microalgae and marine bacteria. As with DMSP, DMSOP is a low-molecular-weight zwitterionic metabolite that carries both a positively and a negatively charged functional group. Isotope labelling studies demonstrate that DMSOP is produced from DMSP, and is readily metabolized to DMSO by marine bacteria. DMSOP was found in near nanomolar amounts in field samples and in algal culture media, and thus represents—to our knowledge—a previously undescribed biogenic source for DMSO in the marine environment. The estimated annual oceanic production of oxidized sulfur from this pathway is in the teragram range, similar to the calculated dimethylsulfide flux to the atmosphere3. This sulfoxonium metabolite is therefore a key metabolite of a previously undescribed pathway in the marine sulfur cycle. These findings highlight the importance of DMSOP in the marine organosulfur cycle.
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The datasets generated and analysed during the current study are available from the corresponding authors upon reasonable request.
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We thank A. Curson for the provision of the A. faecalis mutant; R. Kiene and A. Rellinger, M. Galí, M. Vila, L. Viure and E. Berdalet for collection of field samples and chlorophyll a analyses during field campaigns in the northeast Pacific, Arctic and Mediterranean Sea. We acknowledge the funding by the German Research Foundation (CRC1127 ChemBioSys to G.P. and N.M.), the Max Planck Society (IMPRS BGC) and the National Science Foundation (OCE-1756907 to D.J.K.). This study was co-financed by the State of Thuringia/Thüringer Aufbaubank (2015 FGI 0021) with means of the EU in the framework of the EFRE programme.
Nature thanks G. Siuzdak and the other anonymous reviewer(s) for their contribution to the peer review of this work.
G.P., K.T., B.G. and D.J.K. designed the research. B.G. identified DMSOP signals, performed the synthesis and the initial screening of the metabolite. K.T. performed DMSOP quantification, experiments on the biosynthesis and transformation in algae and bacteria. N.M. carried out experiments on DMSOP production and transformation in algae and performed several analytical measurements. The I. galbana growth experiment and DMSO quantification was performed by L.C. D.J.K. was responsible for field sampling and sample work-up. K.T. and N.M. performed the statistical evaluation of the data. G.P. and D.K. were the principal investigators for their respective research teams. K.T. and G.P. wrote the main drafts of the manuscript. All authors discussed the results and provided feedback and revisions to the manuscript.