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Dimethylsulfoniopropionate biosynthesis in marine bacteria and identification of the key gene in this process

Nature Microbiology volume 2, Article number: 17009 (2017) Cite this article

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Abstract

Dimethylsulfoniopropionate (DMSP) is one of the Earth's most abundant organosulfur molecules, a signalling molecule1, a key nutrient for marine microorganisms2,3 and the major precursor for gaseous dimethyl sulfide (DMS). DMS, another infochemical in signalling pathways4, is important in global sulfur cycling2 and affects the Earth's albedo, and potentially climate, via sulfate aerosol and cloud condensation nuclei production5,6. It was thought that only eukaryotes produce significant amounts of DMSP7–9, but here we demonstrate that many marine heterotrophic bacteria also produce DMSP, probably using the same methionine (Met) transamination pathway as macroalgae and phytoplankton10. We identify the first DMSP synthesis gene in any organism, dsyB, which encodes the key methyltransferase enzyme of this pathway and is a reliable reporter for bacterial DMSP synthesis in marine Alphaproteobacteria. DMSP production and dsyB transcription are upregulated by increased salinity, nitrogen limitation and lower temperatures in our model DMSP-producing bacterium Labrenzia aggregata LZB033. With significant numbers of dsyB homologues in marine metagenomes, we propose that bacteria probably make a significant contribution to oceanic DMSP production. Furthermore, because DMSP production is not solely associated with obligate phototrophs, the process need not be confined to the photic zones of marine environments and, as such, may have been underestimated.

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Figure 1: DMSP biosynthesis pathways and bacterial DMSP production.
Figure 2: Maximum-likelihood phylogenetic tree of DsyB proteins.
Figure 3: DMSP production, dsyB transcription and dddL transcription in L. aggregata LZB033 under different conditions.

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Acknowledgements

Funding from the Natural Environmental Research Council (NE/J01138X, NE/M004449 and NE/N002385) supported work in J.D.T.'s laboratory, and funding from the National Natural Science Foundation of China (41521064, 41476112 and 41276141) supported the research in X.-H.Z.'s laboratory. The authors thank L. Hill of the John Innes Centre Metabolite Services for technical support with LC–MS experiments and P. Wells for general technical support. The authors thank C. Brearley, E. Mercadé, C. Murrell and L. Sims for advice and discussion of results. The authors also acknowledge the Tara Oceans Consortium for providing metagenomic sequence data.

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Authors and Affiliations

  1. School of Biological Sciences, University of East Anglia, Norwich Research Park, Norwich, NR4 7TJ, UK

    Andrew R. J. Curson, Ji Liu, Ana Bermejo Martínez, Robert T. Green, Ornella Carrión, Beth T. Williams & Jonathan D. Todd

  2. College of Marine Life Sciences, Ocean University of China, 5 Yushan Road, Qingdao, 266003, China

    Ji Liu & Xiao-Hua Zhang

  3. School of Chemistry, University of East Anglia, Norwich Research Park, Norwich, NR4 7TJ, UK

    Yohan Chan & Philip C. Bulman Page

  4. Key Laboratory of Marine Chemistry Theory and Technology, Ministry of Education,

    Sheng-Hui Zhang & Gui-Peng Yang

  5. College of Chemistry and Chemical Engineering, Ocean University of China, Qingdao, 266100, China

    Sheng-Hui Zhang & Gui-Peng Yang

  6. Laboratory for Marine Ecology and Environmental Science, Qingdao National Laboratory for Marine Science and Technology, Qingdao, 266071, China

    Gui-Peng Yang & Xiao-Hua Zhang

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Contributions

J.D.T. wrote the paper, designed all the experiments and performed experiments (genomic library screening, gene cloning and enzyme assays) and analysed data. A.R.J.C. wrote the paper, performed experiments (genomic library construction, gene cloning, enzyme assays, mutant construction, GC experiments to quantify DMSP and DMS production, growth experiments to measure DMSP production under different environmental conditions, mutant phenotyping, bioinformatics analysis to identify homologues in bacterial genomes, and phylogenetic trees), analysed data and prepared figures/tables. A.B.M. performed experiments (sample preparation, method development and operation of LC–MS, RNA isolation, and RT–qPCR experiments) and analysed data. X.-H.Z. and J.L. performed experiments (isolation of LZB033 and generation of a draft genome sequence, identification of DMS production in LZB033, mutant phenotyping) and analysed data. R.T.G. performed bioinformatic analysis of metagenomes and prepared figures/tables. Y.C. and P.C.B.P. performed chemical syntheses. O.C. and B.T.W. performed GC experiments and discussed results. S.-H.Z. and G.-P.Y. performed preliminary GC experiments on DMS production in LZB033. All authors reviewed the manuscript before submission.

Corresponding authors

Correspondence to Xiao-Hua Zhang or Jonathan D. Todd.

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Supplementary Figures 1 and 2; Supplementary Tables 1–5; Supplementary References. (PDF 538 kb)

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Curson, A., Liu, J., Bermejo Martínez, A. et al. Dimethylsulfoniopropionate biosynthesis in marine bacteria and identification of the key gene in this process. Nat Microbiol 2, 17009 (2017). https://doi.org/10.1038/nmicrobiol.2017.9

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