Letter

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

  • Nature Microbiology 2, Article number: 17009 (2017)
  • doi:10.1038/nmicrobiol.2017.9
  • Download Citation
Received:
Accepted:
Published online:

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,​8,​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.

  • Subscribe to Nature Microbiology for full access:

    $59

    Subscribe

Additional access options:

Already a subscriber?  Log in  now or  Register  for online access.

References

  1. 1.

    , , & Chemoattraction to dimethylsulfoniopropionate throughout the marine microbial food web. Science 329, 342–345 (2010).

  2. 2.

    , & The sulfur cycle. Oceanography 20, 117–123 (2007).

  3. 3.

    , , & Catabolism of dimethylsulphoniopropionate: microorganisms, enzymes and genes. Nat. Rev. Microbiol. 9, 849–859 (2011).

  4. 4.

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

  5. 5.

    , , , & Environmental constraints on the production and removal of the climatically active gas dimethylsulphide (DMS) and implications for ecosystem modelling. Biogeochemistry 83, 245–275 (2007).

  6. 6.

    & Strong relationship between DMS and the solar radiation dose over the global surface ocean. Science 315, 506–508 (2007).

  7. 7.

    Dimethylsulfoniopropionate: its sources, role in the marine food web, and biological degradation to dimethylsulfide. Appl. Environ. Microbiol. 68, 5804–5815 (2002).

  8. 8.

    & DMSP in marine macroalgae and macroinvertebrates: distribution, function, and ecological impacts. Aquat. Sci. 69, 394–402 (2007).

  9. 9.

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

  10. 10.

    et al. A new route for synthesis of dimethylsulphoniopropionate in marine algae. Nature 387, 891–894 (1997).

  11. 11.

    , , , & in Biological and Environmental Chemistry of DMSP and Related Sulfonium Compounds (eds Kiene, R. P., Visscher, P. T., Keller, M. D. & Kirst, G. O.) Ch. 9, 97–107 (Plenum, 1996).

  12. 12.

    , , & S-methylmethionine conversion to dimethylsulfoniopropionate: evidence for an unusual transamination reaction. Plant Physiol. 115, 1541–1548 (1997).

  13. 13.

    & Biochemical evidence for two novel enzymes in the biosynthesis of 3-dimethylsulfoniopropionate in Spartina alterniflora. Plant Physiol. 123, 1153–1161 (2000).

  14. 14.

    & Bacterial methionine biosynthesis. Microbiology 160, 1571–1584 (2014).

  15. 15.

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

  16. 16.

    , , & Regulation of biosynthesis of dimethylsulfoniopropionate and its uptake in sterile mutant of Ulva pertusa (Chlorophyta). J. Phycol. 47, 517–523 (2011).

  17. 17.

    , , , & Molecular genetic analysis of a dimethylsulfoniopropionate lyase that liberates the climate-changing gas dimethylsulfide in several marine alpha-proteobacteria and rhodobacter sphaeroides. Environ. Microbiol. 10, 757–767 (2008).

  18. 18.

    , , & Cross-ocean distribution of Rhodobacterales bacteria as primary surface colonizers in temperate coastal marine waters. Appl. Environ. Microbiol. 74, 52–60 (2008).

  19. 19.

    , & Fe–S cluster assembly pathways in bacteria. Microbiol. Mol. Biol. Rev. 72, 110–125 (2008).

  20. 20.

    & Peroxiredoxins in bacterial antioxidant defense. Subcell. Biochem. 44, 143–193 (2007).

  21. 21.

    , , & An antioxidant function for DMSP and DMS in marine algae. Nature 418, 317–320 (2002).

  22. 22.

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

  23. 23.

    , , & Dimethylsulphoniopropionate (DMSP) and related compounds in higher plants. J. Exp. Bot. 55, 1919–1925 (2004).

  24. 24.

    et al. A novel pathway producing dimethylsulphide in bacteria is widespread in soil environments. Nat. Commun. 6, 6579 (2015).

  25. 25.

    , , & Identifying numerically abundant culturable bacteria from complex communities: an example from a lignin enrichment culture. Appl. Environ. Microbiol. 62, 4433–4440 (1996).

  26. 26.

    & in The Prokaryotes: A Handbook on Habitats, Isolation and Identification of Bacteria (eds Starr, M. P., Stolp, H., Trüper, H. G., Balows, A. & Schlegel, H. G.) 1302–1331 (Springer, 1981).

  27. 27.

    , & Molecular Cloning, A Laboratory Manual 2nd edn, Vol. 3 (Cold Spring Harbor Laboratory Press, 1989).

  28. 28.

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

  29. 29.

    & 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).

  30. 30.

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

  31. 31.

    , , , & Regulatable vectors for environmental gene expression in Alphaproteobacteria. Appl. Environ. Microb. 78, 7137–7140 (2012).

  32. 32.

    , , & Improved broad-host-range plasmids for DNA cloning in Gram-negative bacteria. Gene 70, 191–197 (1988).

  33. 33.

    , , & Identifying bacterial genes and endosymbiont DNA with Glimmer. Bioinformatics 23, 673–679 (2007).

  34. 34.

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

  35. 35.

    , & NCBI reference sequences (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins. Nucleic Acids Res. 35, D61–D65 (2007).

  36. 36.

    , , & The COG database: a tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Res. 28, 33–36 (2000).

  37. 37.

    , , , & The KEGG resource for deciphering the genome. Nucleic Acids Res. 32, D277–D280 (2004).

  38. 38.

    et al. Gene ontology: tool for the unification of biology. Nat. Genet. 25, 25–29 (2000).

  39. 39.

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

  40. 40.

    et al. Small mobilizable multipurpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum. Gene 145, 69–73 (1994).

  41. 41.

    , , & Flaviramulus ichthyoenteri sp nov., an N-acylhomoserine lactone-degrading bacterium isolated from the intestine of a flounder (Paralichthys olivaceus), and emended descriptions of the genus Flaviramulus and Flaviramulus basaltis. Int. J. Syst. Evol. Microbiol. 63, 4477–4483 (2013).

  42. 42.

    et al. Evaluation of a new high-throughput method for identifying quorum quenching bacteria. Sci. Rep. 3, 2935 (2013).

  43. 43.

    & Protein content and protein synthesis rates of planktonic marine bacteria. Mar. Ecol. Prog. Ser. 51, 201–213 (1989).

  44. 44.

    , , & Reclassification of marine Agrobacterium species: proposals of Stappia stellulata gen. nov., comb. nov., Stappia aggregata sp. nov., nom. rev., Ruegeria atlantica gen. nov., comb. nov., Ruegeria gelatinovora comb. nov., Ruegeria algicola comb. nov., and Ahrensia kieliense gen. nov., sp. nov., nom. rev. J. Gen. Appl. Microbiol. 44, 201–210 (1998).

  45. 45.

    & Oceanicola granulosus gen. nov., sp. nov. and Oceanicola batsensis sp. nov., poly-β-hydroxybutyrate-producing marine bacteria in the order ‘Rhodobacterales’. Int. J. Syst. Evol. Microbiol. 54, 1129–1136 (2004).

  46. 46.

    , , , & Sagittula stellata gen. nov., sp. nov., a lignin-transforming bacterium from a coastal environment. Int. J. Syst. Bacteriol. 47, 773–780 (1997).

  47. 47.

    , & Amorphus coralli gen. nov., sp. nov., a marine bacterium isolated from coral mucus, belonging to the order Rhizobiales. Int. J. Syst. Evol. Microbiol. 58, 2704–2709 (2008).

  48. 48.

    & Pelagibaca bermudensis gen. nov., sp. nov., a novel marine bacterium within the Roseobacter clade in the order Rhodobacterales. Int. J. Syst. Evol. Microbiol. 56, 855–859 (2006).

  49. 49.

    , , , & Thalassobaculum salexigens sp. nov., a new member of the family Rhodospirillaceae from the NW Mediterranean Sea, and emended description of the genus Thalassobaculum. Int. J. Syst. Evol. Microbiol. 60, 209–213 (2010).

  50. 50.

    et al. Sediminimonas qiaohouensis gen. nov., sp nov., a member of the Roseobacter clade in the order Rhodobacterales. Int. J. Syst. Evol. Microbiol. 59, 1561–1567 (2009).

  51. 51.

    , , , & Atomic force microscopy of a ctpA mutant in Rhizobium leguminosarum reveals surface defects linking CtpA function to biofilm formation. Microbiology 157, 3049–3058 (2011).

  52. 52.

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

  53. 53.

    & Enhancements and modifications of primer design program Primer3. Bioinformatics 23, 1289–1291 (2007).

  54. 54.

    et al. Primer3—new capabilities and interfaces. Nucleic Acids Res. 40, e115 (2012).

  55. 55.

    A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45 (2001).

  56. 56.

    , , , & MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30, 2725–2729 (2013).

  57. 57.

    & An improved general amino acid replacement matrix. Mol. Biol. Evol. 25, 1307–1320 (2008).

Download references

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.

Author information

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

    • Sheng-Hui Zhang
    •  & Gui-Peng Yang
  5. Laboratory for Marine Ecology and Environmental Science, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266071, China

    • Gui-Peng Yang
    •  & Xiao-Hua Zhang

Authors

  1. Search for Andrew R. J. Curson in:

  2. Search for Ji Liu in:

  3. Search for Ana Bermejo Martínez in:

  4. Search for Robert T. Green in:

  5. Search for Yohan Chan in:

  6. Search for Ornella Carrión in:

  7. Search for Beth T. Williams in:

  8. Search for Sheng-Hui Zhang in:

  9. Search for Gui-Peng Yang in:

  10. Search for Philip C. Bulman Page in:

  11. Search for Xiao-Hua Zhang in:

  12. Search for Jonathan D. Todd in:

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.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

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

Supplementary information

PDF files

  1. 1.

    Supplementary Information

    Supplementary Figures 1 and 2; Supplementary Tables 1–5; Supplementary References.