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DMSP biosynthesis by an animal and its role in coral thermal stress response

Nature volume 502, pages 677–680 (2013)Cite this article

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Abstract

Globally, reef-building corals are the most prolific producers of dimethylsulphoniopropionate (DMSP)1,2, a central molecule in the marine sulphur cycle and precursor of the climate-active gas dimethylsulphide3,4. At present, DMSP production by corals is attributed entirely to their algal endosymbiont, Symbiodinium2. Combining chemical, genomic and molecular approaches, we show that coral juveniles produce DMSP in the absence of algal symbionts. DMSP levels increased up to 54% over time in newly settled coral juveniles lacking algal endosymbionts, and further increases, up to 76%, were recorded when juveniles were subjected to thermal stress. We uncovered coral orthologues of two algal genes recently identified in DMSP biosynthesis, strongly indicating that corals possess the enzymatic machinery necessary for DMSP production. Our results overturn the paradigm that photosynthetic organisms are the sole biological source of DMSP, and highlight the double jeopardy represented by worldwide declining coral cover, as the potential to alleviate thermal stress through coral-produced DMSP declines correspondingly.

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Figure 1: Changes in DMSP and acrylate concentrations (mean ± s.e.) in coral juveniles lacking photosynthetic symbionts (n = 6; 40 juveniles per replicate) through a 6-day period after coral settlement.
Figure 2: Effects of thermal stress on adult colonies of the coral Acropora millepora.
Figure 3: Putative DMSP biosynthesis pathway and gene expression of coral orthologues.

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References

  1. Broadbent, A. D. & Jones, G. B. DMS and DMSP in mucus ropes, coral mucus, surface films and sediment pore waters from coral reefs in the Great Barrier Reef. Mar. Freshw. Res. 55, 849–855 (2004)

    CAS  Google Scholar 

  2. Broadbent, A. D., Jones, G. B. & Jones, R. J. DMSP in corals and benthic algae from the Great Barrier Reef. Estuar. Coast. Shelf Sci. 55, 547–555 (2002)

    ADS  CAS  Google Scholar 

  3. Ayers, G. P. & Gras, J. L. Seasonal relationship between cloud condensation nuclei and aerosol methanesulphonate in marine air. Nature 353, 834–835 (1991)

    ADS  CAS  Google Scholar 

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

    ADS  CAS  PubMed  Google Scholar 

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

    ADS  CAS  Google Scholar 

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

    ADS  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  8. Quinn, P. K. & Bates, T. S. The case against climate regulation via oceanic phytoplankton sulphur emissions. Nature 480, 51–56 (2011)

    ADS  CAS  PubMed  Google Scholar 

  9. Yost, D. M., Jones, R., Rowe, C. L. & Mitchelmore, C. L. Quantification of total and particulate dimethylsulfoniopropionate (DMSP) in five Bermudian coral species across a depth gradient. Coral Reefs 31, 561–570 (2012)

    ADS  Google Scholar 

  10. Yost, D. M. & Mitchelmore, C. L. Determination of total and particulate dimethylsulfoniopropionate (DMSP) concentrations in four scleractinian coral species: a comparison of methods. J. Exp. Mar. Biol. Ecol. 395, 72–79 (2010)

    CAS  Google Scholar 

  11. Fischer, E. & Jones, G. B. Atmospheric dimethylsulphide production from corals in the Great Barrier Reef and links to solar radiation, climate and coral bleaching. Biogeochemistry 110, 31–46 (2012)

    CAS  Google Scholar 

  12. Veron, J. E. N. Corals of the World Vol. 1–3 (Australian Institute of Marine Science, 2000)

    Google Scholar 

  13. Tapiolas, D. M., Raina, J. B., Lutz, A., Willis, B. L. & Motti, C. A. Direct measurement of dimethysulfoniopropionate (DMSP) in reef-building corals using quantitative nuclear magnetic resonance (qNMR) spectroscopy. J. Exp. Mar. Biol. Ecol. 443, 85–89 (2013)

    CAS  Google Scholar 

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

    ADS  CAS  PubMed  Google Scholar 

  15. Lesser, M. P. in Coral Reefs: An Ecosystem in Transition (eds Dubinsky, Z. & Stambler, N. ) 405–419 (Springer, 2011)

    Google Scholar 

  16. Strychar, K. B., Sammarco, P. W. & Piva, T. J. Apoptotic and necrotic stages of Symbiodinium (Dinophyceae) cell death activity: bleaching of soft and scleractinian corals. Phycologia 43, 768–777 (2004)

    Google Scholar 

  17. McLenon, A. L. & DiTullio, G. R. Effect of increased temperature on dimethylsulfoniopropionate (DMSP) concentration and methionine synthase activity in Symbiodinium microadriaticum . Biogeochemistry 110, 17–29 (2012)

    CAS  Google Scholar 

  18. Raina, J. B., Dinsdale, E. A., Willis, B. L. & Bourne, D. G. Do the organic sulfur compounds DMSP and DMS drive coral microbial associations? Trends Microbiol. 18, 101–108 (2010)

    CAS  PubMed  Google Scholar 

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

    ADS  CAS  PubMed  Google Scholar 

  20. 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)

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Moya, A. et al. Whole transcriptome analysis of the coral Acropora millepora reveals complex responses to CO2-driven acidification during the initiation of calcification. Mol. Ecol. 21, 2440–2454 (2012)

    CAS  PubMed  Google Scholar 

  22. Shinzato, C. et al. Using the Acropora digitifera genome to understand coral response to environmental change. Nature 476, 320–323 (2011)

    ADS  CAS  PubMed  Google Scholar 

  23. Chen, F., Mackey, A. J., Vermunt, J. K. & Roos, D. S. Assessing performance of orthology detection strategies applied to eukaryotic genomes. PLoS ONE 2, e383 (2007)

    ADS  PubMed  PubMed Central  Google Scholar 

  24. Bayer, T. et al. Symbiodinium transcriptomes: genome insights into the dinoflagellate symbionts of reef-building corals. PLoS ONE 7, e35269 (2012)

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  25. Ito, T., Asano, Y., Tanaka, Y. & Takabe, T. Regulation of biosynthesis of dimethylsulfoniopropionate and its uptake in sterile mutant of Ulva pertusa (Chlorophyta). J. Phycol. 47, 517–523 (2011)

    CAS  PubMed  Google Scholar 

  26. Van Alstyne, K. L., Dominique, V. J. & Muller-Parker, G. Is dimethylsulfoniopropionate (DMSP) produced by the symbionts or the host in an anemone-zooxanthellae symbiosis? Coral Reefs 28, 167–176 (2009)

    ADS  Google Scholar 

  27. Bigg, E. K. & Turvey, D. E. Sources of atmospheric particles over Australia. Atmos. Environ. 12, 1643–1655 (1978)

    ADS  Google Scholar 

  28. Modini, R. L. et al. New particle formation and growth at a remote, sub-tropical coastal location. Atmos. Chem. Phys. 9, 7607–7621 (2009)

    ADS  CAS  Google Scholar 

  29. Leahy, S. M., Kingsford, M. J. & Steinberg, C. R. Do clouds save the Great Barrier Reef? Satellite imagery elucidates the cloud-SST relationship at the local scale. PLoS ONE 8, e70400 (2013)

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  30. De’ath, G., Fabricius, K. E., Sweatman, H. & Puotinen, M. The 27-year decline of coral cover on the Great Barrier Reef and its causes. Proc. Natl Acad. Sci. USA 109, 17995–17999 (2012)

    ADS  PubMed  Google Scholar 

  31. van Oppen, M. J. H., Palstra, F. P., Piquet, A. M. T. & Miller, D. J. Patterns of coral-dinoflagellate associations in Acropora: significance of local availability and physiology of Symbiodinium strains and host-symbiont selectivity. Proc. R. Soc. Lond. B 268, 1759–1767 (2001)

    CAS  Google Scholar 

  32. Wilson, K. et al. Genetic mapping of the black tiger shrimp Penaeusmonodon with amplified fragment length polymorphism. Aquaculture 204, 297–309 (2002)

    CAS  Google Scholar 

  33. Veal, C. J., Holmes, G., Nunez, M., Hoegh-Guldberg, O. & Osborn, J. A comparative study of methods for surface area and three dimensional shape measurement of coral skeletons. Limnol. Oceanogr. Methods 8, 241–253 (2010)

    Google Scholar 

  34. Quinn, G. P. & Keough, M. J. Experimental Design and Data Analysis for Biologists (Cambridge Univ. Press, 2002)

    Google Scholar 

  35. Bourne, D. & Munn, C. Diversity of bacteria associated with the coral Pocilloporada micornis from the Great Barrier Reef. Environ. Microbiol. 7, 1162–1174 (2005)

    CAS  PubMed  Google Scholar 

  36. Suzuki, G., Hayashibara, T., Shirayama, Y. & Fukami, H. Evidence of species-specific habitat selectivity of Acropora corals based on identification of new recruits by two molecular markers. Mar. Ecol. Prog. Ser. 355, 149–159 (2008)

    ADS  CAS  Google Scholar 

  37. Sherwood, A. R., Chan, Y. L. & Presting, G. G. Application of universally amplifying plastid primers to environmental sampling of a stream periphyton community. Mol. Ecol. Res. 8, 1011–1014 (2008)

    CAS  Google Scholar 

  38. Taberlet, P., Gielly, L., Pautou, G. & Bouvet, J. Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Mol. Biol. 17, 1105–1109 (1991)

    CAS  PubMed  Google Scholar 

  39. Marchesi, J. R. et al. Design and evaluation of useful bacterium-specific primers that amplify genes coding for 16S rRNA. Appl. Environ. Microbiol. 64, 795–799 (1998)

    CAS  PubMed  PubMed Central  Google Scholar 

  40. Takai, K. & Horikoshi, K. Rapid detection and quantification of members of the archaeal community by quantitative PCR using fluorogenic probes. Appl. Environ. Microbiol. 66, 5066–5072 (2000)

    CAS  PubMed  PubMed Central  Google Scholar 

  41. White, T. J., Bruns, T., Lee, S. & Taylor, J. Amplification and Direct Sequencing of Fungal Ribosomal RNA Genes for Phylogenetics. PCR Protocols: a Guide to Methods and Applications (ed. Innis, M. ) (Academic, 1990)

    Google Scholar 

  42. Moreno-Hagelsieb, G. & Latimer, K. Choosing BLAST options for better detection of orthologs as reciprocal best hits. Bioinformatics 24, 319–324 (2008)

    CAS  PubMed  Google Scholar 

  43. Raina, J. B., Tapiolas, D., Willis, B. L. & Bourne, D. G. Coral-associated bacteria and their role in the biogeochemical cycling of sulfur. Appl. Environ. Microbiol. 75, 3492–3501 (2009)

    CAS  PubMed  PubMed Central  Google Scholar 

  44. González, J. M. et al. Bacterial community structure associated with a dimethylsulfoniopropionate-producing North Atlantic algal bloom. Appl. Environ. Microbiol. 66, 4237–4246 (2000)

    PubMed  PubMed Central  Google Scholar 

  45. Todd, J. D. et al. DddQ, a novel, cupin-containing, dimethylsulfoniopropionatelyase in marine roseobacters and in uncultured marine bacteria. Environ. Microbiol. 13, 427–438 (2010)

    PubMed  Google Scholar 

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

    ADS  CAS  PubMed  Google Scholar 

  47. Gómez-Consarnau, L., Lindh, M. V., Gasol, J. M. & Pinhassi, J. Structuring of bacterioplankton communities by specific dissolved organic carbon compounds. Environ. Microbiol. 14, 2361–2378 (2012)

    PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  49. Todd, J. D., Curson, A. R. J., Nicholson, P. & Johnston, A. W. B. The dddP 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)

    CAS  PubMed  Google Scholar 

  50. Howard, E. C. et al. Bacterial taxa that limit sulfur flux from the ocean. Science 314, 649–652 (2006)

    ADS  CAS  PubMed  Google Scholar 

  51. Schäfer, H. Isolation of Methylophaga spp. from marine dimethylsulfide degrading enrichment cultures and identification of polypeptides induced during growth on dimethylsulfide. Appl. Environ. Microbiol. 73, 2580–2591 (2007)

    PubMed  PubMed Central  Google Scholar 

  52. Vogt, C. & Fischer, U. Influence of reduced inorganic sulfur compounds and oxygen on DMS oxidation and DMS reduction by the marine purple “nonsulfur” bacterium Rhodovulum sulfidophilum strain W4. Microbiol. Res. 153, 219–226 (1998)

    CAS  Google Scholar 

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Acknowledgements

The authors would like to thank D. Yellowlees, R. Stocker, M. Garren, A. Johnston, W. Dunlap, H. Harrison, P. Warner and E. Botté for valuable comments on the manuscript. We specially thank K. Ritchie for her advice and encouragement. We also thank J. Hicks, P. Barron (Bruker Biospin), A. Negri, T. Harder, J. Tebben, M. Logan and J. Pollock for their assistance. This work was supported by the AMMRF Centre for Microscopy, Characterisation and Analysis (UWA), the ARC Centre of Excellence for Coral Reef Studies and AIMS.

Author information

Author notes

  1. David Abrego & François O. Seneca

    Present address: Present addresses: Natural Science and Public Health, Zayed University, PO Box 144534, Abu Dhabi, United Arab Emirates (D.A.); Kewalo Marine Lab, University of Hawai’i at Mānoa, 41 Ahui Street, Honolulu, Hawai’i 96813, USA (F.O.S.).,

Authors and Affiliations

  1. AIMS@JCU, and School of Marine and Tropical Biology, James Cook University, Townsville, 4811, Queensland, Australia

    Jean-Baptiste Raina, François O. Seneca & Bette L. Willis

  2. Australian Institute of Marine Science, PMB3, Townsville MC, Townsville, Queensland 4810, Australia ,

    Jean-Baptiste Raina, Dianne M. Tapiolas, Adrian Lutz, David Abrego, François O. Seneca, David G. Bourne & Cherie A. Motti

  3. ARC Centre of Excellence for Coral Reef Studies, School of Marine and Tropical Biology, James Cook University, Townsville, 4811, Queensland, Australia

    Jean-Baptiste Raina, Sylvain Forêt, Adrian Lutz & Bette L. Willis

  4. Australian National University, Canberra, Australian Capital Territory 2601, Australia ,

    Sylvain Forêt

  5. AIMS@JCU, and School of Pharmacy and Molecular Sciences, James Cook University, Townsville, 4811, Queensland, Australia

    Adrian Lutz

  6. School of Biological Sciences and Biotechnology, Murdoch University, Perth, 6050, Western Australia, Australia

    Janja Ceh

  7. Centre for Microscopy, Characterisation and Analysis, The University of Western Australia, 35 Stirling Highway, Crawley, Western Australia 6009, Australia ,

    Peta L. Clode

  8. Oceans Institute, the University of Western Australia, 35 Stirling Highway, Crawley, Western Australia 6009, Australia ,

    Peta L. Clode

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  1. Jean-Baptiste Raina
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Contributions

J.-B.R. and A.L. designed the experiments. J.-B.R., C.A.M., D.A. and D.M.T. performed the juvenile experiment. J.-B.R., C.A.M., A.L., F.O.S. and D.M.T. performed the adult experiment. J.-B.R., P.L.C., C.A.M. and D.M.T. analysed the results. S.F. and J.-B.R. identified the candidate genes. J.-B.R. and B.L.W. wrote the manuscript. All authors edited the manuscript before submission.

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Correspondence to Jean-Baptiste Raina.

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Extended data figures and tables

Extended Data Figure 1 Density and photosynthetic efficiency (mean ± s.e.) of Symbiodinium cells within adult colonies of the coral Acropora millepora maintained under control (27 °C) or thermal stress (32 °C) conditions for 10 days.

a, Density of Symbiodinium cells in the same coral fragments through time. b, Comparison of photosystem II photochemical efficiency (maximum quantum yields: FV/FM) through time (repeated measure ANOVA, *P < 0.001; post-hoc simple main effect test, *P < 0.01). See also Extended Data Table 3.

Extended Data Figure 2 Representative transmission electron micrographs showing the effects of thermal stress on the internal structure of endosymbiotic Symbiodinium cells associated with the coral Acropora millepora.

a, c, Symbiodinium cells after 10 days at 27 °C, showing intact cell structures (a) and intact thylakoid membranes of chloroplasts (arrows), the photosynthetic centre of cells (c). b, d, Symbiodinium cells after 10 days at 32 °C, showing structurally degraded cells (b) with highly disrupted thylakoid membranes (arrows) (d). Scale bars, 1 μm. ch, chloroplast; nu, nucleus. e, Percentage of structurally damaged Symbiodinium cells within adult tissue throughout the thermal stress experiment. The numbers above the bars refer to the total number of Symbiodinium cells observed.

Extended Data Figure 3 Phylogenetic distribution of the reductase and methyltransferase orthologues (OrthoMCL groups OG5_131390 and OG5_156314, respectively).

Note the unusually sparse distribution of OG5_156314. In red: co-occurrence of these two enzymes occurs predominantly in DMSP-producing organisms. The only species of bacteria in the OrthoMCL database where these two enzymes occur simultaneously is the marine cyanobacterium Synechococcus.

Extended Data Table 1 Primer pairs used to target the genomic DNA of various microorganisms possibly responsible for DMSP production to assess presence in coral juveniles
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Extended Data Table 2 Sums of squares (SS), mean squares (MS) and significance levels for ANOVAs of the Symbiodinium-free juvenile experiment
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Extended Data Table 3 Sums of square (SS), mean squares (MS) and significance levels for ANOVAs of the thermal stress experiment on adult Acropora millepora corals
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Extended Data Table 4 Description of the reductase and methyltransferase sequences in diatoms, corals and Symbiodinium
Full size table
Extended Data Table 5 Composition of coral juvenile bacterial communities present in the two different coral species at the two temperature regimes after 6 days
Full size table

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Raina, JB., Tapiolas, D., Forêt, S. et al. DMSP biosynthesis by an animal and its role in coral thermal stress response. Nature 502, 677–680 (2013). https://doi.org/10.1038/nature12677

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