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

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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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.

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Authors and Affiliations

Authors

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.

Corresponding author

Correspondence to Jean-Baptiste Raina.

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The authors declare no competing financial interests.

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
Extended Data Table 2 Sums of squares (SS), mean squares (MS) and significance levels for ANOVAs of the Symbiodinium-free juvenile experiment
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
Extended Data Table 4 Description of the reductase and methyltransferase sequences in diatoms, corals and Symbiodinium
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

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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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