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Novel pathway for assimilation of dimethylsulphoniopropionate widespread in marine bacteria

Abstract

Dimethylsulphoniopropionate (DMSP) accounts for up to 10% of carbon fixed by marine phytoplankton in ocean surface waters1,2, producing an estimated 11.7–103 Tmol S per year3, most of which is processed by marine bacteria through the demethylation/demethiolation pathway4. This pathway releases methanethiol (MeSH) instead of the climatically active gas dimethylsulphide (DMS) and enables marine microorganisms to assimilate the reduced sulphur5,6,7. Despite recognition of this critical microbial transformation for over two decades, the biochemical pathway and enzymes responsible have remained unidentified. Here we show that three new enzymes related to fatty acid β-oxidation constitute the pathway that assimilates methylmercaptopropionate (MMPA), the first product of DMSP demethylation/demethiolation, and that two previously unknown coenzyme A (CoA) derivatives, 3-methylmercaptopropionyl-CoA (MMPA-CoA) and methylthioacryloyl-CoA (MTA-CoA), are formed as novel intermediates. A member of the marine roseobacters, Ruegeria pomeroyi DSS-3, requires the MMPA-CoA pathway for MMPA assimilation and MeSH production. This pathway and the ability to produce MeSH from MMPA are present in diverse bacteria, and the ubiquitous SAR11 clade bacterium Pelagibacter ubique possesses enzymes for at least the first two steps. Analysis of marine metagenomic data indicates that the pathway is widespread among bacterioplankton in the ocean surface waters, making it one of the most important known routes for acquisition of reduced carbon and sulphur by surface ocean heterotrophs.

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Figure 1: Pathway of DMSP demethylation as identified in R. pomeroyi DSS-3.
Figure 2: Phylogenetic tree of DmdC from representative bacteria.

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Acknowledgements

We thank G. Wylie for assistance with NMR spectroscopy, S. Sharma, S. Sun and H. Luo for bioinformatics assistance, S. Gifford for technical advice, C. Smith and W. Crabb for technical assistance, and C. English for assistance with graphics. Funding for this research was provided by the National Science Foundation (MCB-0702125 and OCE-0724017) and the Gordon and Betty Moore Foundation.

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Contributions

C.R.R. performed growth experiments, enzyme assays, protein purifications, substrate synthesis, phylogenetic analysis, and all reaction analysis except MALDI-FT-ICR. M.J.S. and I.J.A. performed MALDI-FT-ICR analysis. C.R.R. and V.A.V. performed genetic modifications of R. pomeroyi DSS-3. V.A.V. performed RT-qPCR. C.R.R. and M.A.M. conducted bioinformatic analyses. C.R.R., M.A.M. and W.B.W. designed the experiments and wrote the paper. All authors reviewed the manuscript before submission.

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Correspondence to William B. Whitman.

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The authors declare no competing financial interests.

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Reisch, C., Stoudemayer, M., Varaljay, V. et al. Novel pathway for assimilation of dimethylsulphoniopropionate widespread in marine bacteria. Nature 473, 208–211 (2011). https://doi.org/10.1038/nature10078

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