DSYB catalyses the key step of dimethylsulfoniopropionate biosynthesis in many phytoplankton

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Dimethylsulfoniopropionate (DMSP) is a globally important organosulfur molecule and the major precursor for dimethyl sulfide. These compounds are important info-chemicals, key nutrients for marine microorganisms, and are involved in global sulfur cycling, atmospheric chemistry and cloud formation1,2,3. DMSP production was thought to be confined to eukaryotes, but heterotrophic bacteria can also produce DMSP through the pathway used by most phytoplankton4, and the DsyB enzyme catalysing the key step of this pathway in bacteria was recently identified5. However, eukaryotic phytoplankton probably produce most of Earth’s DMSP, yet no DMSP biosynthesis genes have been identified in any such organisms. Here we identify functional dsyB homologues, termed DSYB, in many phytoplankton and corals. DSYB is a methylthiohydroxybutryate methyltransferase enzyme localized in the chloroplasts and mitochondria of the haptophyte Prymnesium parvum, and stable isotope tracking experiments support these organelles as sites of DMSP synthesis. DSYB transcription levels increased with DMSP concentrations in different phytoplankton and were indicative of intracellular DMSP. Identification of the eukaryotic DSYB sequences, along with bacterial dsyB, provides the first molecular tools to predict the relative contributions of eukaryotes and prokaryotes to global DMSP production. Furthermore, evolutionary analysis suggests that eukaryotic DSYB originated in bacteria and was passed to eukaryotes early in their evolution.

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Fig. 1: Transamination pathway for DMSP biosynthesis pathway in bacteria and marine algae and phylogenetic tree of DsyB/DSYB proteins.
Fig. 2: Immunogold localization of DSYB in P. parvum CCAP946/6.
Fig. 3: Subcellular distribution of 34S in P. parvum CCAP946/6 following sulfur uptake for 48 h.

Change history

  • 30 January 2019

    In the version of this Letter originally published, the Methods incorrectly stated that all phytoplankton cultures were sampled in mid-exponential phase. The low-nitrogen cultures were sampled in early stationary phase and at the point at which Fv/Fm values decreased, to indicate that cultures were experiencing low-nitrogen conditions. All other phytoplankton cultures were sampled in exponential phase. Growth and Fv/Fm data are provided here on high- and low-nitrogen cultures (Figs 1, 2 and 3) to clarify and support this correction. The Methods also stated that cell counting was done using a Beckman Multisizer 3 Coulter Counter, but a CASY Model TT Cell Counter was used.


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Funding from the Natural Environment Research Council (NE/J01138X/1, NE/M004449/1, NE/N002385/1 and NE/P012671/1) supported work in J.D.T.’s laboratory. B.T.W. was supported by an NERC EnvEast grant (NE/L002582/1) and A.B.M. was supported by a BBSRC Norwich Research Park Biosciences Doctoral Training Partnership grant (BB/M011216/1). The NanoSIMS work was supported by an Australian Research Council Grant (DE160100636) to J.-B.R. We thank P. Wells and M. Giardina for general technical support, T. Mock for supplying Fragilariopsis cylindrus, and R. Green, J. Liu and C. Murrell for advice and discussion of results. We also acknowledge the Tara Oceans Consortium for providing metagenomic sequence data, and the facilities at the Australian Microscopy & Microanalysis Research Facility at the Centre for Microscopy, Characterisation & Analysis, University of Western Australia, a facility funded by the University, State and Commonwealth Governments.

Author information

J.D.T. wrote the paper, designed experiments, performed experiments (gene cloning, enzyme assays, bioinformatics) and analysed data; A.R.J.C. wrote the paper, designed experiments, performed experiments (gene cloning, enzyme assays, GC to quantify DMSP/DMSHB, phytoplankton growth experiments), analysed data and prepared figures/tables; B.T.W. performed experiments (bioinformatics analysis of DsyB/DSYB in transcriptomes, metagenomes and metatranscriptomes, phylogenetic tree construction), analysed data and prepared figures/tables; B.J.P. performed experiments (gene cloning, RNA isolation, RT–qPCR experiments, protein purification, in vitro enzyme assays and western blots) and analysed data; L.P.S. performed experiments (gene cloning) and analysed data; A.B.M. performed experiments (LC-MS detection of DMSP and glycine betaine) and analysed data; P.P.L.R. performed experiments (phytoplankton growth experiments); D.K. performed experiments (bioinformatic analysis and phylogenetic tree construction); E.M. performed experiments (immunogold labelling, microscopy) and prepared figures; L.G.S. wrote the paper, performed experiments (evolutionary analysis of DsyB and DSYB sequences and phylogenetic tree construction) and prepared figures/tables; J.-B.R. wrote the paper, performed experiments (NanoSIMS, LC-MRM-MS) and prepared figures; U.K. performed experiments (LC-MRM-MS); P.L.C. and P.G. performed experiments (NanoSIMS); O.C. designed antibodies and prepared materials for microscopy; S.M. performed experiments (bioinformatic analysis); and R.A.C. supplied C. tobin CCMP291 strain. All authors reviewed the manuscript before submission.

Correspondence to Jonathan D. Todd.

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Supplementary information

Supplementary Information

Supplementary Figures 1–5, 7; Supplementary Tables 1,2,4,5,7,8,10 and 11; and Supplementary References

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Supplementary Figure 6

Phylogenetic tree of environmental DsyB/DSYB protein sequences

Supplementary Table 3

DSYB proteins identified from genomes and transcriptomes

Supplementary Table 6

Metagenome information and results of DsyB and DSYB metagenomic searches

Supplementary Table 9.

GeoMICS metatranscriptome dsyB, DSYB and DMSP lyase gene transcript abundance

Supplementary Data 1

DSYB amino acid sequences identified from genomes or transcriptomes. Presented in FASTA format

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