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Bacteria are important dimethylsulfoniopropionate producers in coastal sediments

Nature Microbiology volume 4, pages 1815–1825 (2019)Cite this article

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Abstract

Dimethylsulfoniopropionate (DMSP) and its catabolite dimethyl sulfide (DMS) are key marine nutrients1,2 that have roles in global sulfur cycling2, atmospheric chemistry3, signalling4,5 and, potentially, climate regulation6,7. The production of DMSP was previously thought to be an oxic and photic process that is mainly confined to the surface oceans. However, here we show that DMSP concentrations and/or rates of DMSP and DMS synthesis are higher in surface sediment from, for example, saltmarsh ponds, estuaries and the deep ocean than in the overlying seawater. A quarter of bacterial strains isolated from saltmarsh sediment produced DMSP (up to 73 mM), and we identified several previously unknown producers of DMSP. Most DMSP-producing isolates contained dsyB8, but some alphaproteobacteria, gammaproteobacteria and actinobacteria used a methionine methylation pathway independent of DsyB that was previously only associated with higher plants. These bacteria contained a methionine methyltransferase gene (mmtN)—a marker for bacterial synthesis of DMSP through this pathway. DMSP-producing bacteria and their dsyB and/or mmtN transcripts were present in all of the tested seawater samples and Tara Oceans bacterioplankton datasets, but were much more abundant in marine surface sediment. Approximately 1 × 108 bacteria g−1 of surface marine sediment are predicted to produce DMSP, and their contribution to this process should be included in future models of global DMSP production. We propose that coastal and marine sediments, which cover a large part of the Earth’s surface, are environments with high levels of DMSP and DMS productivity, and that bacteria are important producers of DMSP and DMS within these environments.

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Fig. 1: DMSP synthesis in tested marine sediments.
Fig. 2: DMSP-biosynthesis pathways and bacterial production of DMSP.
Fig. 3: Maximum-likelihood phylogenetic tree of MmtN proteins.

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Data availability

The 16S rRNA gene amplicon sequencing, metagenomic data and whole-genome sequences generated in this study are publicly available from the NCBI Sequence Read Archive (BioProject: PRJNA522699).

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Acknowledgements

Funding from the Natural Environmental Research Council (NE/N002385, NE/P012671 and NE/S001352) supported work in J.D.T.’s laboratory. Funding from the National Natural Science Foundation of China (grant numbers 91751202 and 41730530) supported the research in X.-H.Z.’s laboratory. B.T.W. was supported by a NERC EnvEast grant (NE/L002582/1). A.B.M. and K.C. were supported by the BBSRC Norwich Research Park Biosciences Doctoral Training Partnership grant number BB/M011216/1. J.P. was supported by a NERC Independent Research Fellowship (NE/L010771/2). We thank P. Wells for general technical support, and P. Nelson and R. Whiting at the CEFAS, Lowestoft for sediment nutrient analysis. We acknowledge the Tara Oceans Consortium for providing metagenomic sequence data. We also thank the late R. Kiene, whose work on DMSP was an inspiration for this study.

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Authors and Affiliations

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

    Beth T. Williams, Kasha Cowles, Ana Bermejo Martínez, Andrew R. J. Curson, Yanfen Zheng, Jingli Liu, Simone Newton-Payne, Peter Paolo L. Rivera, Ji Liu, Lewis G. Spurgin, Charles A. Brearley, Benjamin J. Pinchbeck & Jonathan D. Todd

  2. College of Marine Life Sciences, Ocean University of China, Qingdao, China

    Yanfen Zheng, Jingli Liu, Chun-Yang Li, Ji Liu & Xiao-Hua Zhang

  3. School of Environmental Sciences, University of East Anglia, Norwich Research Park, Norwich, UK

    Andrew J. Hind, Ornella Carrión & J. Colin Murrell

  4. Department of Surgery, University of Auckland, Auckland, New Zealand

    Brett Wagner Mackenzie

  5. State Key Laboratory of Microbial Technology, Shandong University, Qingdao, China

    Ming Peng & Yu-Zhong Zhang

  6. The Lyell Centre, Heriot-Watt University, Edinburgh, UK

    Jennifer Pratscher

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Contributions

J.D.T. wrote the paper, designed all of the experiments and performed experiments. B.T.W. wrote the paper, designed all of the experiments and performed or contributed to all of the experiments and prepared figures and tables. K.C. performed experiments (genomic library screening, mutant complementation and characterization of MMT+ bacteria). A.B.M. performed experiments (LC–MS work). A.R.J.C. performed experiments (genomic library construction, MMT assays, mutant construction and rate experiments). Y.Z. performed experiments (qPCR, degenerate primer design, sampling and DMSP quantification in the Mariana Trench). Jingli Liu and Ji Liu performed experiments (seawater incubations, qPCR, sediment sampling, purge-trap analysis, DNA/RNA purification from water). S.N.-P., M.P. and C.-Y.L. designed and performed experiments (MmtN protein characterization). P.P.L.R. performed experiments (DMSP quantification in sediment, isolation and characterization of eukaryotic species). L.G.S. wrote the paper and performed experiments (evolutionary analysis of MmtN sequences and phylogenetic tree construction). C.A.B. devised experiments for measuring DMSP pathway intermediates in sediment and cell lysate by HPLC, carried out LC–MS experiments and discussed results. B.W.M. performed experiments (16S rRNA amplicon sequencing analysis) and prepared figures. B.J.P. performed experiments (cell lysate assays); J.P. performed experiments (degenerate primer design, sediment sampling and bioinformatics analysis of metagenomic sequencing). O.C., X.-H.Z., Y.-Z.Z. and J.C.M. designed experiments and discussed results.

Corresponding author

Correspondence to Jonathan D. Todd.

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Supplementary information

Supplementary Information

Supplementary Figs. 1–18, Supplementary Tables 1–3, Supplementary Tables 5 and 6, Supplementary Tables 9–11, Supplementary Tables 13–17, Supplementary references.

Reporting Summary

Supplementary Table 4

Species shown to produce DMSP, including those containing dsyB, mmtN or unknown DMSP-synthesis genes, as of June 2018.

Supplementary Table 7

Metagenome information and results of mmtN/dsyB metagenomic searches in OM-RGC and Stiffkey metagenomes.

Supplementary Table 8

DMSP production in selected strains of bacteria and activity of the corresponding cloned mmtN genes.

Supplementary Table 12

Tara Oceans metatranscriptome mmtN transcript abundance, alongside dsyB, DSYB and DMSP lyases calculated in ref. 1.

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Williams, B.T., Cowles, K., Bermejo Martínez, A. et al. Bacteria are important dimethylsulfoniopropionate producers in coastal sediments. Nat Microbiol 4, 1815–1825 (2019). https://doi.org/10.1038/s41564-019-0527-1

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