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A new route for synthesis of dimethylsulphoniopropionate in marine algae

Abstract

The 3-dimethylsulphoniopropionate (DMSP) produced by marine algae is the main biogenic precursor of atmospheric dimethylsulphide (DMS)1,2,3. This biogenic DMS, formed by bacterial and algal degradation of DMSP4,5, contributes about 1.5 × 1013 g of sulphur to the atmosphere annually3, and plays a major part in the global sulphur cycle, in cloud formation and potentially in climate regulation1,3. Although DMSP biosynthesis has been partially elucidated in a higher plant6,7, nothing is known about how algae make DMSP except that the whole molecule is derived from methionine8,9,10,11,12. Here we use in vivo isotope labelling to demonstrate that DMSP synthesis in the green macroalga Enteromorpha intestinalis proceeds by a route entirely distinct from that in higher plants. From methionine, the steps are transamination, reduction and S -methylation to give the novel sulphonium compound 4-dimethylsulphonio-2-hydroxybutyrate (DMSHB), which is oxidatively decarboxylated to DMSP. The key intermediate DMSHB was also identified in three diverse phytoplankton species, indicating that the same pathway operates in other algal classes that are important sources of DMS. The fact that a transamination initiates this pathway could help explain how algal DMSP (and thereby DMS) production is enhanced by nitrogen deficiency12.

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Figure 1: Labelling kinetics of selected small molecules and protein following administration of a tracer [35S]Met dose to E. intestinalis.
Figure 2: Evidence for conversion of DMSHB to DMSP by an oxygenase reaction in E.intestinalis.
Figure 3: Proposed pathway of DMSP synthesis in E.intestinalis and other algae.
Figure 4: Evidence that DMSHB participates in DMSP synthesis in Emiliania huxleyi (EH), Melosira nummuloides (MN) and Tetraselmis sp. (TS).

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Acknowledgements

We thank J. Hellebust, O. Schofield and J. S. Davis for algal material. This work was supported by grants from the NSF and ONR to A.D.H. and D.A.G., from the ONR to D.R. and T.L., from the NIH to the MSU-NIH Mass Spectrometry Facility and by the C.V. Griffin Sr Foundation. (Florida Agricultural Experiment Station journal series no. R-05740.)

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Correspondence to Douglas A. Gage or Andrew D. Hanson.

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Gage, D., Rhodes, D., Nolte, K. et al. A new route for synthesis of dimethylsulphoniopropionate in marine algae. Nature 387, 891–894 (1997). https://doi.org/10.1038/43160

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