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The metabolite dimethylsulfoxonium propionate extends the marine organosulfur cycle

Abstract

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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Fig. 1: Simplified, revised marine sulfur cycle.
Fig. 2: Detection and structural elucidation of DMSOP.
Fig. 3: Biosynthesis and catabolism of DMSOP.

Data availability

The datasets generated and analysed during the current study are available from the corresponding authors upon reasonable request.

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Acknowledgements

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.

Reviewer information

Nature thanks G. Siuzdak and the other anonymous reviewer(s) for their contribution to the peer review of this work.

Author contributions

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.

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Correspondence to David J. Kieber or Georg Pohnert.

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Extended data figures and tables

Extended Data Fig. 1 DMSOP mass spectra.

The HRMS/MS spectra of natural occurring DMSOP and the authentic standard (normalized collision energy of 35) are shown. a, DMSOP standard, molecular ion m/z 151.0421, fragments [C2H7O2S]+ m/z 79.0210 and [C3H5O2]+ m/z 73.0283. b, Isotopic pattern of the molecular ion m/z 151.0421 with the calculated formula C5H11O3S and isotopic fine structure of [M + 1] and [M + 2]. c, DMSOP from a P. parvum extract with added 13C2-DMSOP. d, 13C2-DMSOP, molecular ion m/z 153.0485, fragments [13C2H7O2S]+ m/z 81.0277 and [C3H5O2]+ m/z 73.0282.

Extended Data Fig. 2 Structure of DMSOP.

Arrows show the heteronuclear multiple-bond coherence correlations. Numbers indicate carbon atom positions.

Extended Data Fig. 3 I. galbana growth and cellular DMSOP.

a, b, Growth (a) and photosynthetic efficiency (b) of I. galbana cultures. c, Cellular DMSP and DMSOP content. Data are mean ± s.d. of n = 3 independent cultures. P values are from a one-way repeated-measures ANOVA with Tukey post hoc test. A significant difference in cellular DMSOP concentration compared to day 3 was detected from day 7 onward.

Extended Data Fig. 4 DMSOP stablity in seawater and base.

a, DMSOP is stable over a period of 72 days in seawater (left). It degraded at room temperature under basic pH (pH = 11, monitored over 23 h; right). b, DMSO was released during this base treatment (integration of m/z = 79 in GC/MS). Data are mean ± s.d. of n = 3 independent samples. P values are from one-way repeated-measures ANOVA with Tukey post hoc test compared to t = 0 h.

Extended Data Fig. 5 DMSO release from DMSOP by bacteria.

a, b, DMSOP (1 µM) is degraded by A. faecalis, a dddY knockout mutant of A. faecalis (a) and by Halomonas sp. (b). Data are mean ± s.d. of n = 4 independent cultures. P values result from unpaired two-tailed Student’s t-tests. c, In separate experiments, it was demonstrated that DMSOP is the exclusive source for DMSO production in A. faecalis. Release of labelled DMSO from 13C2-DMSOP was monitored by GC/HRMS. The mass spectrum shows an average over the DMSO peak extracted from an A. faecalis culture that was incubated for 23 h with DMSOP. Integration of the ion traces 80.0200 (13C2-DMSO) and 78.0134 (DMSO) in three independent replicates revealed a degree of labelling of 99.3 ± 0.25%.

Extended Data Fig. 6 Map of sampling sites.

Sampling sites are indicated in red.

Extended Data Table 1 Occurrence of DMSOP in different algal species
Extended Data Table 2 DMSPtotal and DMSOPtotal concentrations in seawater
Extended Data Table 3 Incorporation of 13C2-DMSP into DMSOP in P. bermudensis

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Thume, K., Gebser, B., Chen, L. et al. The metabolite dimethylsulfoxonium propionate extends the marine organosulfur cycle. Nature 563, 412–415 (2018). https://doi.org/10.1038/s41586-018-0675-0

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Keywords

  • Dimethylsulfoniopropionate (DMSP)
  • Marine Sulfur Cycle
  • DMSP Lyase
  • Sargasso Seawater
  • Bermudensis

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