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

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

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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, _Symbiodinium_2. 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


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Contact customer support SIMILAR CONTENT BEING VIEWED BY OTHERS DYNAMIC REGULATION OF CORAL ENERGY METABOLISM THROUGHOUT THE DIEL CYCLE Article Open access 16 November 2020 INHIBITING


INOSITOL TRANSPORT DISRUPTS METABOLITE PROFILES AND MIMICS HEAT STRESS IN A MODEL CNIDARIAN-SYMBIODINIACEAE SYMBIOSIS Article Open access 15 May 2025 CORAL ENDOSYMBIONT GROWTH IS ENHANCED BY


METABOLIC INTERACTIONS WITH BACTERIA Article Open access 27 October 2023 ACCESSION CODES PRIMARY ACCESSIONS GENBANK/EMBL/DDBJ * KF619251 * KF619442 REFERENCES * Broadbent, A. D. &


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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 * 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 * 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 * 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 * 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 * Australian National University, Canberra, Australian Capital Territory 2601, Australia , Sylvain Forêt * AIMS@JCU, and School of Pharmacy and Molecular Sciences, James Cook


University, Townsville, 4811, Queensland, Australia Adrian Lutz * School of Biological Sciences and Biotechnology, Murdoch University, Perth, 6050, Western Australia, Australia Janja Ceh *


Centre for Microscopy, Characterisation and Analysis, The University of Western Australia, 35 Stirling Highway, Crawley, Western Australia 6009, Australia , Peta L. Clode * Oceans Institute,


the University of Western Australia, 35 Stirling Highway, Crawley, Western Australia 6009, Australia , Peta L. Clode Authors * Jean-Baptiste Raina View author publications You can also


search for this author inPubMed Google Scholar * Dianne M. Tapiolas View author publications You can also search for this author inPubMed Google Scholar * Sylvain Forêt View author


publications You can also search for this author inPubMed Google Scholar * Adrian Lutz View author publications You can also search for this author inPubMed Google Scholar * David Abrego


View author publications You can also search for this author inPubMed Google Scholar * Janja Ceh View author publications You can also search for this author inPubMed Google Scholar *


François O. Seneca View author publications You can also search for this author inPubMed Google Scholar * Peta L. Clode View author publications You can also search for this author inPubMed 


Google Scholar * David G. Bourne View author publications You can also search for this author inPubMed Google Scholar * Bette L. Willis View author publications You can also search for this


author inPubMed Google Scholar * Cherie A. Motti View author publications You can also search for this author inPubMed Google Scholar 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. ETHICS DECLARATIONS COMPETING INTERESTS 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: _F_V/_F_M) 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_. POWERPOINT SLIDES POWERPOINT SLIDE FOR FIG. 1 POWERPOINT SLIDE FOR FIG. 2 POWERPOINT SLIDE FOR FIG. 3 SOURCE DATA


SOURCE DATA TO FIG. 1 SOURCE DATA TO FIG. 2 RIGHTS AND PERMISSIONS Reprints and permissions ABOUT THIS ARTICLE CITE THIS ARTICLE 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 Download citation * Received: 31 July 2013 *


Accepted: 18 September 2013 * Published: 23 October 2013 * Issue Date: 31 October 2013 * DOI: https://doi.org/10.1038/nature12677 SHARE THIS ARTICLE Anyone you share the following link with


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