Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

DSYB catalyses the key step of dimethylsulfoniopropionate biosynthesis in many phytoplankton

An Author Correction to this article was published on 30 January 2019

This article has been updated

Abstract

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.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

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.

Similar content being viewed by others

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.

References

  1. Nevitt, G. A. The neuroecology of dimethyl sulfide: a global-climate regulator turned marine infochemical. Integr. Comp. Biol. 51, 819–825 (2011).

    Article  CAS  Google Scholar 

  2. Sievert, S. M., Kiene, R. P. & Schulz-Vogt, H. N. The sulfur cycle. Oceanography 20, 117–123 (2007).

    Article  Google Scholar 

  3. Curson, A. R., Todd, J. D., Sullivan, M. J. & Johnston, A. W. Catabolism of dimethylsulphoniopropionate: microorganisms, enzymes and genes. Nat. Rev. Microbiol. 9, 849–859 (2011).

    Article  CAS  Google Scholar 

  4. Summers, P. S. et al. Identification and stereospecificity of the first three enzymes of 3-dimethylsulfoniopropionate biosynthesis in a chlorophyte alga. Plant Physiol. 116, 369–378 (1998).

    Article  CAS  Google Scholar 

  5. Curson, A. R. et al. Dimethylsulfoniopropionate biosynthesis in marine bacteria and identification of the key gene in this process. Nat. Microbiol. 2, 17009 (2017).

    Article  CAS  Google Scholar 

  6. Caruana, A. M. N. & Malin, G. The variability in DMSP content and DMSP lyase activity in marine dinoflagellates. Prog. Oceanogr. 120, 410–424 (2014).

    Article  Google Scholar 

  7. Lyon, B. R., Lee, P. A., Bennett, J. M., DiTullio, G. R. & Janech, M. G. Proteomic analysis of a sea-ice diatom: salinity acclimation provides new insight into the dimethylsulfoniopropionate production pathway. Plant Physiol. 157, 1926–1941 (2011).

    Article  CAS  Google Scholar 

  8. Raina, J. B. et al. DMSP biosynthesis by an animal and its role in coral thermal stress response. Nature 502, 677–680 (2013).

    Article  CAS  Google Scholar 

  9. Keller, M. D., Bellows, W. K. & Guillard, R. R. L. in Biogenic Sulfur in the Environment (eds Saltzman, E. S. & Cooper, W. J.) Ch. 11 (American Chemical Society, Washington DC, 1989).

  10. Nei, M. & Rooney, A. P. Concerted and birth-and-death evolution of multigene families. Annu. Rev. Genet. 39, 121–152 (2005).

    Article  CAS  Google Scholar 

  11. Ku, C. et al. Endosymbiotic origin and differential loss of eukaryotic genes. Nature 524, 427–432 (2015).

    Article  CAS  Google Scholar 

  12. Baumgarten, S. et al. The genome of Aiptasia, a sea anemone model for coral symbiosis. Proc. Natl Acad. Sci. USA 112, 11893–11898 (2015).

    Article  CAS  Google Scholar 

  13. Van Alstyne, K. L. & Puglisi, M. P. DMSP in marine macroalgae and macroinvertebrates: distribution, function, and ecological impacts. Aquat. Sci. 69, 394–402 (2007).

    Article  CAS  Google Scholar 

  14. Spielmeyer, A. & Pohnert, G. Influence of temperature and elevated carbon dioxide on the production of dimethylsulfoniopropionate and glycine betaine by marine phytoplankton. Mar. Environ. Res. 73, 62–69 (2012).

    CAS  PubMed  Google Scholar 

  15. Dickschat, J. S., Rabe, P. & Citron, C. A. The chemical biology of dimethylsulfoniopropionate. Org. Biomol. Chem. 13, 1954–1968 (2015).

    Article  CAS  Google Scholar 

  16. Hovde, B. T. et al. Genome sequence and transcriptome analyses of Chrysochromulina tobin: metabolic tools for enhanced algal fitness in the prominent order Prymnesiales (Haptophyceae). PLoS Genet. 11, e1005469 (2015).

    Article  Google Scholar 

  17. Jones, H. L. J., Leadbeater, B. S. C. & Green, J. C. Mixotrophy in marine species of Chrysochromulina (Prymnesiophyceae) – ingestion and digestion of a small green flagellate. J. Mar. Biol. Assoc. UK 73, 283–296 (1993).

    Article  Google Scholar 

  18. Kettles, N. L., Kopriva, S. & Malin, G. Insights into the regulation of DMSP synthesis in the diatom Thalassiosira pseudonana through APR activity, proteomics and gene expression analyses on cells acclimating to changes in salinity, light and nitrogen. PLoS ONE 9, e94795 (2014).

    Article  Google Scholar 

  19. Dickson, D. M. J. & Kirst, G. O. Osmotic adjustment in marine eukaryotic algae: the role of inorganic-ions, quaternary ammonium, tertiary sulfonium and carbohydrate solutes. II Prasinophytes and Haptophytes. New Phytol. 106, 657–666 (1987).

    Article  CAS  Google Scholar 

  20. Trossat, C. et al. Salinity promotes accumulation of 3-dimethylsulfoniopropionate and its precursor S-methylmethionine in chloroplasts. Plant Physiol. 116, 165–171 (1998).

    Article  CAS  Google Scholar 

  21. Gruber, A. et al. Protein targeting into complex diatom plastids: functional characterisation of a specific targeting motif. Plant Mol. Biol. 64, 519–530 (2007).

    Article  CAS  Google Scholar 

  22. Raina, J. B. et al. Subcellular tracking reveals the location of dimethylsulfoniopropionate in microalgae and visualises its uptake by marine bacteria. eLife 6, e23008 (2017).

    Article  Google Scholar 

  23. Matrai, P. A. & Keller, M. D. Total organic sulfur and dimethylsulfoniopropionate in marine phytoplankton: intracellular variations. Mar. Biol. 119, 61–68 (1994).

    Article  CAS  Google Scholar 

  24. Stefels, J. Physiological aspects of the production and conversion of DMSP in marine algae and higher plants. J. Sea Res. 43, 183–197 (2000).

    Article  CAS  Google Scholar 

  25. Sunda, W., Kieber, D. J., Kiene, R. P. & Huntsman, S. An antioxidant function for DMSP and DMS in marine algae. Nature 418, 317–320 (2002).

    Article  CAS  Google Scholar 

  26. Sunagawa, S. et al. Structure and function of the global ocean microbiome. Science 348, 1261359 (2015).

    Article  Google Scholar 

  27. Johnston, A. W. B., Green, R. T. & Todd, J. D. Enzymatic breakage of dimethylsulfoniopropionate – a signature molecule for life at sea. Curr. Opin. Chem. Biol. 31, 58–65 (2016).

    Article  CAS  Google Scholar 

  28. Belviso, S. et al. Size distribution of dimethylsulfoniopropionate (DMSP) in areas of the tropical northeastern Atlantic Ocean and the Mediterranean Sea. Mar. Chem. 44, 55–71 (1993).

    Article  CAS  Google Scholar 

  29. Amin, S. A. et al. Interaction and signalling between a cosmopolitan phytoplankton and associated bacteria. Nature 522, 98–101 (2015).

    Article  CAS  Google Scholar 

  30. Guillard, R. R. L. in Culture of Marine Invertebrate Animals (eds Smith, W. L. & Chanley, M. H.) 29–60 (Plenum Press, New York, 1975).

  31. Berges, J. A., Franklin, D. J. & Harrison, P.J. Evolution of an artificial seawater medium: improvements in enriched seawater, artificial water over the last two decades. J. Phycol. 37, 1138–1145 (2001).

    Article  Google Scholar 

  32. Mock, T. et al. Evolutionary genomics of the cold-adapted diatom Fragilariopsis cylindrus. Nature 541, 536–540 (2017).

    Article  CAS  Google Scholar 

  33. Fixen, K. R. et al. Genome sequences of eight bacterial species found in coculture with the haptophyte Chrysochromulina tobin. Genome Announc. 4, e01162-16 (2016).

    Article  Google Scholar 

  34. Sambrook, J., Fritsch, E. F., Maniatis, T. & Nolan, C. Molecular Cloning: A Laboratory Manual 2nd edn, Vol. 3 (Cold Spring Harbor Laboratory Press, New York, 1989).

  35. Beringer, J. E. R factor transfer in Rhizobium leguminosarum. J. Gen. Microbiol. 84, 188–198 (1974).

    CAS  PubMed  Google Scholar 

  36. Gonzalez, J. M., Whitman, W. B., Hodson, R. E. & Moran, M. A. Identifying numerically abundant culturable bacteria from complex communities: an example from a lignin enrichment culture. Appl. Environ. Microbiol. 62, 4433–4440 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Baumann, P. & Baumann, L. in The Prokaryotes: A Handbook on Habitats, Isolation and Identification of Bacteria 1st edn (eds Starr, M. P., Stolp, H., Truper, H. G., Balows, A. & Schlegel, H. G.) 1302–1331 (Springer-Verlag, Berlin, 1981).

  38. Porter, K. G. & Feig, Y. S. The use of DAPI for identifying and counting aquatic microflora. Limnol. Oceanogr. 25, 943–948 (1980).

    Article  Google Scholar 

  39. Figurski, D. H. & Helinski, D. R. Replication of an origin-containing derivative of plasmid Rk2 dependent on a plasmid function provided in trans. Proc. Natl Acad. Sci. USA 76, 1648–1652 (1979).

    Article  CAS  Google Scholar 

  40. Downie, J. A. et al. Cloned nodulation genes of Rhizobium leguminosarum determine host range specificity. Mol. Gen. Genet. 190, 359–365 (1983).

    Article  CAS  Google Scholar 

  41. Keen, N. T., Tamaki, S., Kobayashi, D. & Trollinger, D. Improved broad-host-range plasmids for DNA cloning in Gram-negative bacteria. Gene 70, 191–197 (1988).

    Article  CAS  Google Scholar 

  42. Tett, A. J., Rudder, S. J., Bourdes, A., Karunakaran, R. & Poole, P. S. Regulatable vectors for environmental gene expression in Alphaproteobacteria. Appl. Environ. Microbiol. 78, 7137–7140 (2012).

    Article  CAS  Google Scholar 

  43. Untergasser, A. et al. Primer3 – new capabilities and interfaces. Nucleic Acids Res. 40, e115 (2012).

    Article  CAS  Google Scholar 

  44. Heid, C. A., Stevens, J., Livak, K. J. & Williams, P. M. Real time quantitative PCR. Genome Res. 6, 986–994 (1996).

    Article  CAS  Google Scholar 

  45. Livak, K. J. & Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the method. Methods 25, 402–408 (2001).

    Article  CAS  Google Scholar 

  46. Mahmood, T. & Yang, P. C. Western blot: technique, theory, and trouble shooting. N. Am. J. Med. Sci. 4, 429–434 (2012).

    Article  Google Scholar 

  47. Perez-Cruz, C. et al. New type of outer membrane vesicle produced by the Gram-negative bacterium Shewanella vesiculosa M7T: implications for DNA content. Appl. Environ. Microbiol. 79, 1874–1881 (2013).

    Article  CAS  Google Scholar 

  48. Kilburn, M. R. & Clode, P. L. in Electron Microscopy: Methods and Protocols 3rd edn, Vol. 1117 (ed. Walker, J. M.) Ch. 33 (Humana Press, New York, 2014).

  49. Schindelin, J. et al. Fiji: an open source platform for biological image analysis. Nat. Methods 9, 676–682 (2012).

    Article  CAS  Google Scholar 

  50. Hillion, F., Kilburn, M. R., Hoppe, P., Messenger, S. & Webers, P. K. The effect of QSA on S, C, O and Siisotopic ratio measurements. Geochim. Cosmochim. Acta 72, A377 (2008).

    Google Scholar 

  51. R Development Core Team. R : A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna, 2008).

  52. Altschul, S. F. et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389–3402 (1997).

    Article  CAS  Google Scholar 

  53. Keeling, P. J. et al. The marine microbial eukaryote transcriptome sequencing project (MMETSP): illuminating the functional diversity of eukaryotic life in the oceans through transcriptome sequencing. PLoS Biol. 12, e1001889 (2014).

    Article  Google Scholar 

  54. Toribio, A. L. et al. European nucleotide archive in 2016. Nucleic Acids Res. 45, 32–36 (2017).

    Article  Google Scholar 

  55. Bray, N. L., Pimentel, H., Melsted, P. & Pachter, L. Near-optimal probabilistic RNA-seq quantification. Nat. Biotechnol. 34, 525–527 (2016).

    Article  CAS  Google Scholar 

  56. Katoh, K., Misawa, K., Kuma, K. & Miyata, T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 30, 3059–3066 (2002).

    Article  CAS  Google Scholar 

  57. Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772–780 (2013).

    Article  CAS  Google Scholar 

  58. Schwarz, G. Estimating dimension of a model. Ann. Stat. 6, 461–464 (1978).

    Article  Google Scholar 

  59. Le, S. Q. & Gascuel, O. An improved general amino acid replacement matrix. Mol. Biol. Evol. 25, 1307–1320 (2008).

    Article  CAS  Google Scholar 

  60. Nguyen, L. T., Schmidt, H. A., von Haeseler, A. & Minh, B. Q. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol. 32, 268–274 (2015).

    Article  CAS  Google Scholar 

  61. Trifinopoulos, J., Nguyen, L. T., von Haeseler, A. & Minh, B. Q. W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Res. 44, 232–235 (2016).

    Article  Google Scholar 

  62. Minh, B. Q., Nguyen, M. A. T. & von Haeseler, A. Ultrafast approximation for phylogenetic bootstrap. Mol. Biol. Evol. 30, 1188–1195 (2013).

    Article  CAS  Google Scholar 

  63. Yu, G. C., Smith, D. K., Zhu, H. C., Guan, Y. & Lam, T. T. Y. GGTREE: an R package for visualization and annotation of phylogenetic trees with their covariates and other associated data. Methods Ecol. Evol. 8, 28–36 (2017).

    Article  Google Scholar 

  64. Kumaresan, D. et al. Aerobic proteobacterial methylotrophs in Movile Cave: genomic and metagenomic analyses. Microbiome 6, 1 (2018).

    Article  Google Scholar 

  65. Todd, J. D. et al. Structural and regulatory genes required to make the gas dimethyl sulfide in bacteria. Science 315, 666–669 (2007).

    Article  CAS  Google Scholar 

  66. Todd, J. D. et al. Molecular dissection of bacterial acrylate catabolism – unexpected links with dimethylsulfoniopropionate catabolism and dimethyl sulfide production. Environ. Microbiol. 12, 327–343 (2010).

    Article  CAS  Google Scholar 

  67. Curson, A. R. J., Sullivan, M. J., Todd, J. D. & Johnston, A. W. B. Identification of genes for dimethyl sulfide production in bacteria in the gut of Atlantic Herring (Clupea harengus). ISME J. 4, 144–146 (2010).

    Article  Google Scholar 

  68. Curson, A. R. J., Fowler, E. K., Dickens, S., Johnston, A. W. B. & Todd, J. D. Multiple DMSP lyases in the gamma-proteobacterium Oceanimonas doudoroffii. Biogeochemistry 110, 109–119 (2012).

    Article  CAS  Google Scholar 

  69. Sun, J. et al. The abundant marine bacterium Pelagibacter simultaneously catabolizes dimethylsulfoniopropionate to the gases dimethyl sulfide and methanethiol. Nat. Microbiol. 1, 16065 (2016).

    Article  CAS  Google Scholar 

  70. Curson, A. R., Rogers, R., Todd, J. D., Brearley, C. A. & Johnston, A. W. Molecular genetic analysis of a dimethylsulfoniopropionate lyase that liberates the climate-changing gas dimethylsulfide in several marine α-proteobacteria and Rhodobacter sphaeroides. Environ. Microbiol. 10, 757–767 (2008).

    Article  CAS  Google Scholar 

  71. Todd, J. D., Curson, A. R. J., Dupont, C. L., Nicholson, P. & Johnston, A. W. B. The ddd P gene, encoding a novel enzyme that converts dimethylsulfoniopropionate into dimethyl sulfide, is widespread in ocean metagenomes and marine bacteria and also occurs in some Ascomycete fungi. Environ. Microbiol. 11, 1376–1385 (2009).

    Article  CAS  Google Scholar 

  72. Todd, J. D. et al. DddQ, a novel, cupin-containing, dimethylsulfoniopropionate lyase in marine roseobacters and in uncultured marine bacteria. Environ. Microbiol. 13, 427–438 (2011).

    Article  CAS  Google Scholar 

  73. Curson, A. R. J., Sullivan, M. J., Todd, J. D. & Johnston, A. W. B. DddY, a periplasmic dimethylsulfoniopropionate lyase found in taxonomically diverse species of Proteobacteria. ISME J. 5, 1191–1200 (2011).

    Article  CAS  Google Scholar 

  74. Todd, J. D., Kirkwood, M., Newton-Payne, S. & Johnston, A. W. B. DddW, a third DMSP lyase in a model Roseobacter marine bacterium, Ruegeria pomeroyi DSS-3. ISME J. 6, 223–226 (2012).

    Article  CAS  Google Scholar 

  75. Alcolombri, U. et al. Identification of the algal dimethyl sulfide-releasing enzyme: a missing link in the marine sulfur cycle. Science 348, 1466–1469 (2015).

    Article  CAS  Google Scholar 

  76. Eddy, S. R. Accelerated profile HMM searches. PLoS Comput. Biol. 7, e1002195 (2011).

    Article  CAS  Google Scholar 

  77. Fish, J. A. et al. FunGene: the functional gene pipeline and repository. Front. Microbiol. 4, 291 (2013).

    Article  Google Scholar 

  78. Price, M. N., Dehal, P. S. & Arkin, A. P. FastTree 2 – approximately maximum-likelihood trees for large alignments. PLoS ONE 5, e9490 (2010).

    Article  Google Scholar 

  79. Letunic, I. & Bork, P. Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res. 44, 242–245 (2016).

    Article  Google Scholar 

  80. Masella, A. P., Bartram, A. K., Truszkowski, J. M., Brown, D. G. & Neufeld, J. D. PANDAseq: paired-end assembler for illumina sequences. BMC Bioinformatics 13, 31 (2012).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

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

Authors and Affiliations

Authors

Contributions

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.

Corresponding author

Correspondence to Jonathan D. Todd.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

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

Life Sciences Reporting Summary

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Curson, A.R.J., Williams, B.T., Pinchbeck, B.J. et al. DSYB catalyses the key step of dimethylsulfoniopropionate biosynthesis in many phytoplankton. Nat Microbiol 3, 430–439 (2018). https://doi.org/10.1038/s41564-018-0119-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41564-018-0119-5

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing