Ecology

Gene expression plasticity and frontloading promote thermotolerance in Pocillopora corals

10.24072/pcjournal.79 - Peer Community Journal, Volume 2 (2022), article no. e13.

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Ecosystems worldwide are suffering from climate change. Coral reef ecosystems are globally threatened by increasing sea surface temperatures. However, gene expression plasticity provides the potential for organisms to respond rapidly and effectively to environmental changes, and would be favored in variable environments. In this study, we investigated the thermal stress response in Pocillopora coral colonies from two contrasting environments by exposing them to heat stress. We compared the physiological state, bacterial and Symbiodiniaceae communities (using 16S and ITS2 metabarcoding), and gene expression levels (using RNA-Seq) between control conditions and heat stress (the temperature just below the first signs of compromised health). Colonies from both thermal regimes remained apparently normal and presented open and colored polyps during heat stress, with no change in bacterial and Symbiodiniaceae community composition. In contrast, they differed in their transcriptomic responses. The colonies from Oman displayed a more plastic transcriptome, but some genes had a higher basal expression level (frontloading) compared to the less thermotolerant colonies from New Caledonia. In terms of biological functions, we observed an increase in the expression of stress response genes (including induction of tumor necrosis factor receptors, heat shock proteins, and detoxification of reactive oxygen species), together with a decrease in the expression of genes involved in morpho-anatomical functions. Gene regulation (transcription factors, mobile elements, histone modifications and DNA methylation) appeared to be overrepresented in the Oman colonies, indicating possible epigenetic regulation. These results show that transcriptomic plasticity and frontloading can be co-occurring processes in corals confronted with highly variable thermal regimes.

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DOI: 10.24072/pcjournal.79
Brener-Raffalli, Kelly 1; Vidal-Dupiol, Jeremie 2; Adjeroud, Mehdi 3, 4, 5; Rey, Olivier 1; Romans, Pascal 6; Bonhomme, François 7; Pratlong, Marine 8, 9; Haguenauer, Anne 10; Pillot, Rémi 6; Feuillassier, Lionel 6; Claereboudt, Michel 11; Magalon, Hélène 3, 4, 5; Gélin, Pauline 3, 4, 5; Pontarotti, Pierre 12, 13; Aurelle, Didier 9, 10, 14; Mitta, Guillaume 1, 15; Toulza, Eve 1

1 IHPE, Univ. Montpellier, CNRS, Ifremer, Univ. Perpignan via Domitia, Perpignan France
2 IHPE, Univ. Montpellier, CNRS, Ifremer, Univ. Perpignan via Domitia, Montpellier France
3 ENTROPIE, IRD, Université de la Réunion, CNRS, IFREMER, Université de la Nouvelle-Calédonie, Perpignan, France
4 Laboratoire d’Excellence “CORAIL”, Paris, France
5 PSL Université Paris, USR 3278 CRIOBE EPHE-UPVD-CNRS, Perpignan, France
6 Observatoire Océanologique de Banyuls, Sorbonne Université-CNRS, FR3724, Avenue Pierre Fabre, 66650 Banyuls-sur-Mer, France
7 Institut des Sciences de l'Évolution, Univ. Montpellier, CNRS, IRD, EPHE, Montpellier, France.
8 Aix Marseille Univ, CNRS, Centrale Marseille, I2M, Marseille, France, Equipe Evolution Biologique et Modélisation, Marseille, France
9 Aix Marseille Univ, Université de Toulon, CNRS, IRD, MIO, Marseille, France
10 Aix-Marseille Université, Avignon Université, CNRS, IRD, IMBE, Marseille, France
11 Department of Marine Science and Fisheries, College of Agricultural and Marine Sciences, Sultan Qaboos University, Al-Khod, 123, Sultanate of Oman
12 Aix Marseille Univ, IRD, APHM, Microbe, Evolution, PHylogénie, Infection, IHU Méditerranée Infection, Marseille France. Evolutionary Biology team
13 CNRS SNC5039
14 Institut de Systématique, Evolution, Biodiversité (ISYEB), Muséum National d'Histoire Naturelle, CNRS, Sorbonne Université, EPHE, 57 rue Cuvier, 75005 Paris, France
15 Univ Polynesie Francaise, ILM, IRD, Ifremer, F-98719 Tahiti, French Polynesia, France
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights
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     author = {Brener-Raffalli, Kelly and Vidal-Dupiol, Jeremie and Adjeroud, Mehdi and Rey, Olivier and Romans, Pascal and Bonhomme, Fran\c{c}ois and Pratlong, Marine and Haguenauer, Anne and Pillot, R\'emi and Feuillassier, Lionel and Claereboudt, Michel and Magalon, H\'el\`ene and G\'elin, Pauline and Pontarotti, Pierre and Aurelle, Didier and Mitta, Guillaume and Toulza, Eve},
     title = {Gene expression plasticity and frontloading promote thermotolerance in {<i>Pocillopora</i>} corals},
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Brener-Raffalli, Kelly; Vidal-Dupiol, Jeremie; Adjeroud, Mehdi; Rey, Olivier; Romans, Pascal; Bonhomme, François; Pratlong, Marine; Haguenauer, Anne; Pillot, Rémi; Feuillassier, Lionel; Claereboudt, Michel; Magalon, Hélène; Gélin, Pauline; Pontarotti, Pierre; Aurelle, Didier; Mitta, Guillaume; Toulza, Eve. Gene expression plasticity and frontloading promote thermotolerance in Pocillopora corals. Peer Community Journal, Volume 2 (2022), article  no. e13. doi : 10.24072/pcjournal.79. https://peercommunityjournal.org/articles/10.24072/pcjournal.79/

Peer reviewed and recommended by PCI : 10.24072/pci.ecology.100028

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

[1] Adjeroud, M.; Guérécheau, A.; Vidal-Dupiol, J.; Flot, J.-F.; Arnaud-Haond, S.; Bonhomme, F. Genetic diversity, clonality and connectivity in the scleractinian coral Pocillopora damicornis: a multi-scale analysis in an insular, fragmented reef system, Marine Biology, Volume 161 (2013) no. 3, pp. 531-541 | DOI

[2] Ainsworth, T. D.; Wasmund, K.; Ukani, L.; Seneca, F.; Yellowlees, D.; Miller, D.; Leggat, W. Defining the tipping point. A complex cellular life/death balance in corals in response to stress, Scientific Reports, Volume 1 (2011) no. 1 | DOI

[3] Akaike, H. A new look at the statistical model identification, IEEE Transactions on Automatic Control, Volume 19 (1974) no. 6, pp. 716-723 | DOI

[4] Altschul, S. F.; Gish, W.; Miller, W.; Myers, E. W.; Lipman, D. J. Basic local alignment search tool, Journal of Molecular Biology, Volume 215 (1990) no. 3, pp. 403-410 | DOI

[5] Anders, S.; Pyl, P. T.; Huber, W. HTSeq--a Python framework to work with high-throughput sequencing data, Bioinformatics, Volume 31 (2015) no. 2, pp. 166-169 | DOI

[6] Arnaud-Haond, S.; Belkhir, K. genclone: a computer program to analyse genotypic data, test for clonality and describe spatial clonal organization, Molecular Ecology Notes, Volume 7 (2006) no. 1, pp. 15-17 | DOI

[7] Baird, A. H.; Guest, J. R.; Willis, B. L. Systematic and Biogeographical Patterns in the Reproductive Biology of Scleractinian Corals, Annual Review of Ecology, Evolution, and Systematics, Volume 40 (2009) no. 1, pp. 551-571 | DOI

[8] Baker, A. C. Flexibility and Specificity in Coral-Algal Symbiosis: Diversity, Ecology, and Biogeography of Symbiodinium, Annual Review of Ecology, Evolution, and Systematics, Volume 34 (2003) no. 1, pp. 661-689 | DOI

[9] Barnosky, A. D.; Matzke, N.; Tomiya, S.; Wogan, G. O. U.; Swartz, B.; Quental, T. B.; Marshall, C.; McGuire, J. L.; Lindsey, E. L.; Maguire, K. C.; Mersey, B.; Ferrer, E. A. Has the Earth’s sixth mass extinction already arrived?, Nature, Volume 471 (2011) no. 7336, pp. 51-57 | DOI

[10] Barshis, D. J.; Ladner, J. T.; Oliver, T. A.; Seneca, F. O.; Traylor-Knowles, N.; Palumbi, S. R. Genomic basis for coral resilience to climate change, Proceedings of the National Academy of Sciences, Volume 110 (2013) no. 4, pp. 1387-1392 | DOI

[11] Bates, D.; Mächler, M.; Bolker, B.; Walker, S. Fitting Linear Mixed-Effects Models Usinglme4, Journal of Statistical Software, Volume 67 (2015) no. 1, pp. 1-48 | DOI

[12] Bellantuono, A. J.; Granados-Cifuentes, C.; Miller, D. J.; Hoegh-Guldberg, O.; Rodriguez-Lanetty, M. Coral Thermal Tolerance: Tuning Gene Expression to Resist Thermal Stress, PLoS ONE, Volume 7 (2012) no. 11 | DOI

[13] Bellantuono, A. J.; Hoegh-Guldberg, O.; Rodriguez-Lanetty, M. Resistance to thermal stress in corals without changes in symbiont composition, Proceedings of the Royal Society B: Biological Sciences, Volume 279 (2012) no. 1731, pp. 1100-1107 | DOI

[14] Bellwood, D. R.; Hughes, T. P.; Folke, C.; Nyström, M. Confronting the coral reef crisis, Nature, Volume 429 (2004) no. 6994, pp. 827-833 | DOI

[15] Benjamini, Y.; Hochberg, Y. Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing, Journal of the Royal Statistical Society: Series B (Methodological), Volume 57 (1995) no. 1, pp. 289-300 | DOI

[16] Berkelmans, R.; van Oppen, M. J. The role of zooxanthellae in the thermal tolerance of corals: a ‘nugget of hope’ for coral reefs in an era of climate change, Proceedings of the Royal Society B: Biological Sciences, Volume 273 (2006) no. 1599, pp. 2305-2312 | DOI

[17] Blankenberg, D.; Gordon, A.; Von Kuster, G.; Coraor, N.; Taylor, J.; Nekrutenko, A. Manipulation of FASTQ data with Galaxy, Bioinformatics, Volume 26 (2010) no. 14, pp. 1783-1785 | DOI

[18] Bordenstein, S. R.; Theis, K. R. Host Biology in Light of the Microbiome: Ten Principles of Holobionts and Hologenomes, PLOS Biology, Volume 13 (2015) no. 8 | DOI

[19] Bourne, D. G.; Munn, C. B. Diversity of bacteria associated with the coral Pocillopora damicornis from the Great Barrier Reef, Environmental Microbiology, Volume 7 (2005) no. 8, pp. 1162-1174 | DOI

[20] Brener-Raffalli, K.; Clerissi, C.; Vidal-Dupiol, J.; Adjeroud, M.; Bonhomme, F.; Pratlong, M.; Aurelle, D.; Mitta, G.; Toulza, E. Thermal regime and host clade, rather than geography, drive Symbiodinium and bacterial assemblages in the scleractinian coral Pocillopora damicornis sensu lato, Microbiome, Volume 6 (2018) no. 1 | DOI

[21] Brown, B.; Downs, C.; Dunne, R.; Gibb, S. Exploring the basis of thermotolerance in the reef coral Goniastrea aspera, Marine Ecology Progress Series, Volume 242 (2002), pp. 119-129 | DOI

[22] Coles, S. L.; Riegl, B. M. Thermal tolerances of reef corals in the Gulf: A review of the potential for increasing coral survival and adaptation to climate change through assisted translocation, Marine Pollution Bulletin, Volume 72 (2013) no. 2, pp. 323-332 | DOI

[23] Conesa, A.; Madrigal, P.; Tarazona, S.; Gomez-Cabrero, D.; Cervera, A.; McPherson, A.; Szcześniak, M. W.; Gaffney, D. J.; Elo, L. L.; Zhang, X.; Mortazavi, A. A survey of best practices for RNA-seq data analysis, Genome Biology, Volume 17 (2016) no. 1 | DOI

[24] Cróquer, A.; Bastidas, C.; Elliott, A.; Sweet, M. Bacterial assemblages shifts from healthy to yellow band disease states in the dominant reef coralMontastraea faveolata, Environmental Microbiology Reports, Volume 5 (2013) no. 1, pp. 90-96 | DOI

[25] Danchin, É. Avatars of information: towards an inclusive evolutionary synthesis, Trends in Ecology & Evolution, Volume 28 (2013) no. 6, pp. 351-358 | DOI

[26] Dixon, G. B.; Davies, S. W.; Aglyamova, G. V.; Meyer, E.; Bay, L. K.; Matz, M. V. Genomic determinants of coral heat tolerance across latitudes, Science, Volume 348 (2015) no. 6242, pp. 1460-1462 | DOI

[27] Dobin, A.; Davis, C. A.; Schlesinger, F.; Drenkow, J.; Zaleski, C.; Jha, S.; Batut, P.; Chaisson, M.; Gingeras, T. R. STAR: ultrafast universal RNA-seq aligner, Bioinformatics, Volume 29 (2013) no. 1, pp. 15-21 | DOI

[28] Escudié, F.; Auer, L.; Bernard, M.; Mariadassou, M.; Cauquil, L.; Vidal, K.; Maman, S.; Hernandez-Raquet, G.; Combes, S.; Pascal, G. FROGS: Find, Rapidly, OTUs with Galaxy Solution, Bioinformatics, Volume 34 (2017) no. 8, pp. 1287-1294 | DOI

[29] Fan, T.; Lin, K.; Kuo, F.; Soong, K.; Liu, L.; Fang, L. Diel patterns of larval release by five brooding scleractinian corals, Marine Ecology Progress Series, Volume 321 (2006), pp. 133-142 | DOI

[30] Gélin, P.; Fauvelot, C.; Mehn, V.; Bureau, S.; Rouzé, H.; Magalon, H. Superclone Expansion, Long-Distance Clonal Dispersal and Local Genetic Structuring in the Coral Pocillopora damicornis Type β in Reunion Island, South Western Indian Ocean, PLOS ONE, Volume 12 (2017) no. 1 | DOI

[31] Gélin, P.; Pirog, A.; Fauvelot, C.; Magalon, H. High genetic differentiation and low connectivity in the coral Pocillopora damicornis type β at different spatial scales in the Southwestern Indian Ocean and the Tropical Southwestern Pacific, Marine Biology, Volume 165 (2018) no. 10 | DOI

[32] Gélin, P.; Postaire, B.; Fauvelot, C.; Magalon, H. Reevaluating species number, distribution and endemism of the coral genus Pocillopora Lamarck, 1816 using species delimitation methods and microsatellites, Molecular Phylogenetics and Evolution, Volume 109 (2017), pp. 430-446 | DOI

[33] Giardine, B.; Riemer, C.; Hardison, R. C.; Burhans, R.; Elnitski, L.; Shah, P.; Zhang, Y.; Blankenberg, D.; Albert, I.; Taylor, J.; Miller, W.; Kent, W. J.; Nekrutenko, A. Galaxy: A platform for interactive large-scale genome analysis, Genome Research, Volume 15 (2005) no. 10, pp. 1451-1455 | DOI

[34] Guerrero R; Margulis L; Berlanga M Symbiogenesis: the holobiont as a unit of evolution. , International Microbiology, Volume 16 (2013), pp. 133-143 | DOI

[35] Haguenauer, A.; Zuberer, F.; Ledoux, J.-B.; Aurelle, D. Adaptive abilities of the Mediterranean red coral Corallium rubrum in a heterogeneous and changing environment: from population to functional genetics, Journal of Experimental Marine Biology and Ecology, Volume 449 (2013), pp. 349-357 | DOI

[36] Harrison PL; Wallace CC Reproduction, dispersal and recruitment of scleractinian corals In: Ecosystems of the world (1990), pp. 133-207

[37] Herman, J. J.; Spencer, H. G.; Donohue, K.; Sultan, S. E. How stable ‘should’ epigenetic modifications be? Insights from adaptive plasticity and bet hedging, Evolution, Volume 68 (2013) no. 3, pp. 632-643 | DOI

[38] Hernandez-Agreda, A.; Gates, R. D.; Ainsworth, T. D. Defining the Core Microbiome in Corals’ Microbial Soup, Trends in Microbiology, Volume 25 (2017) no. 2, pp. 125-140 | DOI

[39] Hoegh-Guldberg, O.; Mumby, P. J.; Hooten, A. J.; Steneck, R. S.; Greenfield, P.; Gomez, E.; Harvell, C. D.; Sale, P. F.; Edwards, A. J.; Caldeira, K.; Knowlton, N.; Eakin, C. M.; Iglesias-Prieto, R.; Muthiga, N.; Bradbury, R. H.; Dubi, A.; Hatziolos, M. E. Coral Reefs Under Rapid Climate Change and Ocean Acidification, Science, Volume 318 (2007) no. 5857, pp. 1737-1742 | DOI

[40] de Hoon, M.; Imoto, S.; Nolan, J.; Miyano, S. Open source clustering software, Bioinformatics, Volume 20 (2004) no. 9, pp. 1453-1454 | DOI

[41] Hughes, T. P.; Baird, A. H.; Bellwood, D. R.; Card, M.; Connolly, S. R.; Folke, C.; Grosberg, R.; Hoegh-Guldberg, O.; Jackson, J. B. C.; Kleypas, J.; Lough, J. M.; Marshall, P.; Nyström, M.; Palumbi, S. R.; Pandolfi, J. M.; Rosen, B.; Roughgarden, J. Climate Change, Human Impacts, and the Resilience of Coral Reefs, Science, Volume 301 (2003) no. 5635, pp. 929-933 | DOI

[42] Hughes, T. P.; Barnes, M. L.; Bellwood, D. R.; Cinner, J. E.; Cumming, G. S.; Jackson, J. B. C.; Kleypas, J.; van de Leemput, I. A.; Lough, J. M.; Morrison, T. H.; Palumbi, S. R.; van Nes, E. H.; Scheffer, M. Coral reefs in the Anthropocene, Nature, Volume 546 (2017) no. 7656, pp. 82-90 | DOI

[43] Hughes, T. P.; Kerry, J. T.; Álvarez-Noriega, M.; Álvarez-Romero, J. G.; Anderson, K. D.; Baird, A. H.; Babcock, R. C.; Beger, M.; Bellwood, D. R.; Berkelmans, R.; Bridge, T. C.; Butler, I. R.; Byrne, M.; Cantin, N. E.; Comeau, S.; Connolly, S. R.; Cumming, G. S.; Dalton, S. J.; Diaz-Pulido, G.; Eakin, C. M.; Figueira, W. F.; Gilmour, J. P.; Harrison, H. B.; Heron, S. F.; Hoey, A. S.; Hobbs, J.-P. A.; Hoogenboom, M. O.; Kennedy, E. V.; Kuo, C.-y.; Lough, J. M.; Lowe, R. J.; Liu, G.; McCulloch, M. T.; Malcolm, H. A.; McWilliam, M. J.; Pandolfi, J. M.; Pears, R. J.; Pratchett, M. S.; Schoepf, V.; Simpson, T.; Skirving, W. J.; Sommer, B.; Torda, G.; Wachenfeld, D. R.; Willis, B. L.; Wilson, S. K. Global warming and recurrent mass bleaching of corals, Nature, Volume 543 (2017) no. 7645, pp. 373-377 | DOI

[44] Jablonka, E. The evolutionary implications of epigenetic inheritance, Interface Focus, Volume 7 (2017) no. 5 | DOI

[45] Jombart, T.; Devillard, S.; Balloux, F. Discriminant analysis of principal components: a new method for the analysis of genetically structured populations, BMC Genetics, Volume 11 (2010) no. 1 | DOI

[46] Kenkel, C. D.; Matz, M. V. Gene expression plasticity as a mechanism of coral adaptation to a variable environment, Nature Ecology & Evolution, Volume 1 (2016) no. 1 | DOI

[47] Kenkel, C. D.; Meyer, E.; Matz, M. V. Gene expression under chronic heat stress in populations of the mustard hill coral (Porites astreoides) from different thermal environments, Molecular Ecology, Volume 22 (2013) no. 16, pp. 4322-4334 | DOI

[48] Klindworth, A.; Pruesse, E.; Schweer, T.; Peplies, J.; Quast, C.; Horn, M.; Glöckner, F. O. Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies, Nucleic Acids Research, Volume 41 (2012) no. 1 | DOI

[49] Lajeunesse, T.; Trench, R. Biogeography of two species of Symbiodinium (Freudenthal) inhabiting the intertidal sea anemone Anthopleura elegantissima (Brandt), The Biological Bulletin, Volume 199 (2000) no. 2, pp. 126-134 | DOI

[50] LaJeunesse, T. C.; Parkinson, J. E.; Gabrielson, P. W.; Jeong, H. J.; Reimer, J. D.; Voolstra, C. R.; Santos, S. R. Systematic Revision of Symbiodiniaceae Highlights the Antiquity and Diversity of Coral Endosymbionts, Current Biology, Volume 28 (2018) no. 16 | DOI

[51] Lande, R. Adaptation to an extraordinary environment by evolution of phenotypic plasticity and genetic assimilation, Journal of Evolutionary Biology, Volume 22 (2009) no. 7, pp. 1435-1446 | DOI

[52] Le Nohaïc, M.; Ross, C. L.; Cornwall, C. E.; Comeau, S.; Lowe, R.; McCulloch, M. T.; Schoepf, V. Marine heatwave causes unprecedented regional mass bleaching of thermally resistant corals in northwestern Australia, Scientific Reports, Volume 7 (2017) no. 1 | DOI

[53] Li, J.; Chen, Q.; Long, L.-J.; Dong, J.-D.; Yang, J.; Zhang, S. Bacterial dynamics within the mucus, tissue and skeleton of the coral Porites lutea during different seasons, Scientific Reports, Volume 4 (2014) no. 1 | DOI

[54] Little, A. F.; van Oppen, M. J. H.; Willis, B. L. Flexibility in Algal Endosymbioses Shapes Growth in Reef Corals, Science, Volume 304 (2004) no. 5676, pp. 1492-1494 | DOI

[55] Littman, R. A.; Bourne, D. G.; Willis, B. L. Responses of coral-associated bacterial communities to heat stress differ withSymbiodiniumtype on the same coral host, Molecular Ecology, Volume 19 (2010) no. 9, pp. 1978-1990 | DOI

[56] Love, M. I.; Huber, W.; Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2, Genome Biology, Volume 15 (2014) no. 12 | DOI

[57] Magoc, T.; Salzberg, S. L. FLASH: fast length adjustment of short reads to improve genome assemblies, Bioinformatics, Volume 27 (2011) no. 21, pp. 2957-2963 | DOI

[58] Mahé, F.; Rognes, T.; Quince, C.; de Vargas, C.; Dunthorn, M. Swarm: robust and fast clustering method for amplicon-based studies, PeerJ, Volume 2 (2014) | DOI

[59] Maor-Landaw, K.; Levy, O. Gene expression profiles during short-term heat stress; branchingvs.massive Scleractinian corals of the Red Sea, PeerJ, Volume 4 (2016) | DOI

[60] Margulis L ; Fester R Symbiosis as a Source of Evolutionary Innovation: Speciation and Morphogenesis, MIT Press, Cambridge, MA, USA, 1991

[61] Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads, EMBnet.journal, Volume 17 (2011) no. 1 | DOI

[62] Matz, M. V.; Treml, E. A.; Aglyamova, G. V.; van Oppen, M. J. H.; Bay, L. K. Potential for rapid genetic adaptation to warming in a Great Barrier Reef coral, PLoS Genet., Volume 19 (2017) | DOI

[63] Maumus, F.; Allen, A. E.; Mhiri, C.; Hu, H.; Jabbari, K.; Vardi, A.; Grandbastien, M.-A.; Bowler, C. Potential impact of stress activated retrotransposons on genome evolution in a marine diatom, BMC Genomics, Volume 10 (2009) no. 1 | DOI

[64] Mayfield, A. B.; Wang, L.-H.; Tang, P.-C.; Fan, T.-Y.; Hsiao, Y.-Y.; Tsai, C.-L.; Chen, C.-S. Assessing the Impacts of Experimentally Elevated Temperature on the Biological Composition and Molecular Chaperone Gene Expression of a Reef Coral, PLoS ONE, Volume 6 (2011) no. 10 | DOI

[65] Mayfield, A. B.; Wang, Y.; Chen, C.; Chen, S.; Lin, C. Dual‐compartmental transcriptomic + proteomic analysis of a marine endosymbiosis exposed to environmental change, Molecular Ecology, Volume 25 (2016) no. 23, pp. 5944-5958 | DOI

[66] Mayfield, A. B.; Wang, Y.; Chen, C.; Lin, C.; Chen, S. Compartment‐specific transcriptomics in a reef‐building coral exposed to elevated temperatures, Molecular Ecology, Volume 23 (2014) no. 23, pp. 5816-5830 | DOI

[67] McFall-Ngai, M.; Hadfield, M. G.; Bosch, T. C. G.; Carey, H. V.; Domazet-Lošo, T.; Douglas, A. E.; Dubilier, N.; Eberl, G.; Fukami, T.; Gilbert, S. F.; Hentschel, U.; King, N.; Kjelleberg, S.; Knoll, A. H.; Kremer, N.; Mazmanian, S. K.; Metcalf, J. L.; Nealson, K.; Pierce, N. E.; Rawls, J. F.; Reid, A.; Ruby, E. G.; Rumpho, M.; Sanders, J. G.; Tautz, D.; Wernegreen, J. J. Animals in a bacterial world, a new imperative for the life sciences, Proceedings of the National Academy of Sciences, Volume 110 (2013) no. 9, pp. 3229-3236 | DOI

[68] McMurdie, P. J.; Holmes, S. phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data, PLoS ONE, Volume 8 (2013) no. 4 | DOI

[69] Meyer, J. L.; Rodgers, J. M.; Dillard, B. A.; Paul, V. J.; Teplitski, M. Epimicrobiota Associated with the Decay and Recovery of Orbicella Corals Exhibiting Dark Spot Syndrome, Frontiers in Microbiology, Volume 7 (2016) | DOI

[70] Neave, M. J.; Apprill, A.; Ferrier-Pagès, C.; Voolstra, C. R. Diversity and function of prevalent symbiotic marine bacteria in the genus Endozoicomonas, Applied Microbiology and Biotechnology, Volume 100 (2016) no. 19, pp. 8315-8324 | DOI

[71] Neave, M. J.; Rachmawati, R.; Xun, L.; Michell, C. T.; Bourne, D. G.; Apprill, A.; Voolstra, C. R. Differential specificity between closely related corals and abundant Endozoicomonas endosymbionts across global scales, The ISME Journal, Volume 11 (2016) no. 1, pp. 186-200 | DOI

[72] Oliver, T. A.; Palumbi, S. R. Many corals host thermally resistant symbionts in high-temperature habitat, Coral Reefs, Volume 30 (2010) no. 1, pp. 241-250 | DOI

[73] Palumbi, S. R.; Barshis, D. J.; Traylor-Knowles, N.; Bay, R. A. Mechanisms of reef coral resistance to future climate change, Science, Volume 344 (2014) no. 6186, pp. 895-898 | DOI

[74] Pante, E.; Puillandre, N.; Viricel, A.; Arnaud-Haond, S.; Aurelle, D.; Castelin, M.; Chenuil, A.; Destombe, C.; Forcioli, D.; Valero, M.; Viard, F.; Samadi, S. Species are hypotheses: avoid connectivity assessments based on pillars of sand, Molecular Ecology, Volume 24 (2015) no. 3, pp. 525-544 | DOI

[75] Pantos, O.; Bongaerts, P.; Dennis, P. G.; Tyson, G. W.; Hoegh-Guldberg, O. Habitat-specific environmental conditions primarily control the microbiomes of the coral Seriatopora hystrix, The ISME Journal, Volume 9 (2015) no. 9, pp. 1916-1927 | DOI

[76] Peixoto, R. S.; Rosado, P. M.; Leite, D. C. d. A.; Rosado, A. S.; Bourne, D. G. Beneficial Microorganisms for Corals (BMC): Proposed Mechanisms for Coral Health and Resilience, Frontiers in Microbiology, Volume 8 (2017) | DOI

[77] Pinzón, J. H.; Sampayo, E.; Cox, E.; Chauka, L. J.; Chen, C. A.; Voolstra, C. R.; LaJeunesse, T. C. Blind to morphology: genetics identifies several widespread ecologically common species and few endemics among Indo-Pacific cauliflower corals (Pocillopora , Scleractinia), Journal of Biogeography, Volume 40 (2013) no. 8, pp. 1595-1608 | DOI

[78] Polato, N. R.; Voolstra, C. R.; Schnetzer, J.; DeSalvo, M. K.; Randall, C. J.; Szmant, A. M.; Medina, M.; Baums, I. B. Location-Specific Responses to Thermal Stress in Larvae of the Reef-Building Coral Montastraea faveolata, PLoS ONE, Volume 5 (2010) no. 6 | DOI

[79] Pratlong, M.; Haguenauer, A.; Chabrol, O.; Klopp, C.; Pontarotti, P.; Aurelle, D. The red coral (Corallium rubrum) transcriptome: a new resource for population genetics and local adaptation studies, Molecular Ecology Resources, Volume 15 (2015) no. 5, pp. 1205-1215 | DOI

[80] Pritchard, J. K.; Stephens, M.; Donnelly, P. Inference of Population Structure Using Multilocus Genotype Data, Genetics, Volume 155 (2000) no. 2, pp. 945-959 | DOI

[81] Quigley, K. M.; Davies, S. W.; Kenkel, C. D.; Willis, B. L.; Matz, M. V.; Bay, L. K. Deep-Sequencing Method for Quantifying Background Abundances of Symbiodinium Types: Exploring the Rare Symbiodinium Biosphere in Reef-Building Corals, PLoS ONE, Volume 9 (2014) no. 4 | DOI

[82] Reaka-Kudla ML The Global Biodiversity of Coral Reefs: A comparison with Rain Forests In: Biodiversity II: Understanding and protecting our biological resources (eds Solis MA., Reaka-Kudla ML, Wilson DE, & Wilson EO) (1997), pp. 83-108 | DOI

[83] Reusch, T. B. H. Climate change in the oceans: evolutionary versus phenotypically plastic responses of marine animals and plants, Evolutionary Applications, Volume 7 (2013) no. 1, pp. 104-122 | DOI

[84] Riegl, B. M.; Purkis, S. J.; Al-Cibahy, A. S.; Abdel-Moati, M. A.; Hoegh-Guldberg, O. Present Limits to Heat-Adaptability in Corals and Population-Level Responses to Climate Extremes, PLoS ONE, Volume 6 (2011) no. 9 | DOI

[85] Rogers, A.; Harborne, A. R.; Brown, C. J.; Bozec, Y.-M.; Castro, C.; Chollett, I.; Hock, K.; Knowland, C. A.; Marshell, A.; Ortiz, J. C.; Razak, T.; Roff, G.; Samper-Villarreal, J.; Saunders, M. I.; Wolff, N. H.; Mumby, P. J. Anticipative management for coral reef ecosystem services in the 21st century, Global Change Biology, Volume 21 (2015) no. 2, pp. 504-514 | DOI

[86] Rognes, T.; Flouri, T.; Nichols, B.; Quince, C.; Mahé, F. VSEARCH: a versatile open source tool for metagenomics, PeerJ, Volume 4 (2016) | DOI

[87] Rohwer, F.; Seguritan, V.; Azam, F.; Knowlton, N. Diversity and distribution of coral-associated bacteria, Marine Ecology Progress Series, Volume 243 (2002), pp. 1-10 | DOI

[88] Rosenberg, E.; Koren, O.; Reshef, L.; Efrony, R.; Zilber-Rosenberg, I. The role of microorganisms in coral health, disease and evolution, Nature Reviews Microbiology, Volume 5 (2007) no. 5, pp. 355-362 | DOI

[89] Saldanha, A. J. Java Treeview--extensible visualization of microarray data, Bioinformatics, Volume 20 (2004) no. 17, pp. 3246-3248 | DOI

[90] Sato, Y.; Willis, B. L.; Bourne, D. G. Successional changes in bacterial communities during the development of black band disease on the reef coral, Montipora hispida, The ISME Journal, Volume 4 (2009) no. 2, pp. 203-214 | DOI

[91] Schmidt-Roach, S.; Miller, K. J.; Lundgren, P.; Andreakis, N. With eyes wide open: a revision of species within and closely related to thePocillopora damicornisspecies complex (Scleractinia; Pocilloporidae) using morphology and genetics, Zoological Journal of the Linnean Society, Volume 170 (2014) no. 1, pp. 1-33 | DOI

[92] Suggett, D. J.; Warner, M. E.; Leggat, W. Symbiotic Dinoflagellate Functional Diversity Mediates Coral Survival under Ecological Crisis, Trends in Ecology & Evolution, Volume 32 (2017) no. 10, pp. 735-745 | DOI

[93] Supek, F.; Bošnjak, M.; Škunca, N.; Šmuc, T. REVIGO Summarizes and Visualizes Long Lists of Gene Ontology Terms, PLoS ONE, Volume 6 (2011) no. 7 | DOI

[94] Theis, K. R.; Dheilly, N. M.; Klassen, J. L.; Brucker, R. M.; Baines, J. F.; Bosch, T. C. G.; Cryan, J. F.; Gilbert, S. F.; Goodnight, C. J.; Lloyd, E. A.; Sapp, J.; Vandenkoornhuyse, P.; Zilber-Rosenberg, I.; Rosenberg, E.; Bordenstein, S. R. Getting the Hologenome Concept Right: an Eco-Evolutionary Framework for Hosts and Their Microbiomes, mSystems, Volume 1 (2016) no. 2 | DOI

[95] Torda, G.; Donelson, J. M.; Aranda, M.; Barshis, D. J.; Bay, L.; Berumen, M. L.; Bourne, D. G.; Cantin, N.; Foret, S.; Matz, M.; Miller, D. J.; Moya, A.; Putnam, H. M.; Ravasi, T.; van Oppen, M. J. H.; Thurber, R. V.; Vidal-Dupiol, J.; Voolstra, C. R.; Watson, S.-A.; Whitelaw, E.; Willis, B. L.; Munday, P. L. Rapid adaptive responses to climate change in corals, Nature Climate Change, Volume 7 (2017) no. 9, pp. 627-636 | DOI

[96] Trapnell, C.; Williams, B. A.; Pertea, G.; Mortazavi, A.; Kwan, G.; van Baren, M. J.; Salzberg, S. L.; Wold, B. J.; Pachter, L. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation, Nature Biotechnology, Volume 28 (2010) no. 5, pp. 511-515 | DOI

[97] van Oppen, M. J. H.; Oliver, J. K.; Putnam, H. M.; Gates, R. D. Building coral reef resilience through assisted evolution, Proceedings of the National Academy of Sciences, Volume 112 (2015) no. 8, pp. 2307-2313 | DOI

[98] van Woesik, R.; Sakai, K.; Ganase, A.; Loya, Y. Revisiting the winners and the losers a decade after coral bleaching, Marine Ecology Progress Series, Volume 434 (2011), pp. 67-76 | DOI

[99] Veron JEN; Stafford-Smith M Corals of the world., Australian Institute of Marine Science, Townsville MC, Qld, Australia, 2000

[100] Vidal-Dupiol, J.; Chaparro, C.; Pratlong, M.; Pontarotti, P.; Grunau, C.; Mitta, G. Sequencing, de novo assembly and annotation of the genome of the scleractinian coral, Pocillopora acuta, bioRxiv | DOI

[101] Vidal-Dupiol, J.; Dheilly, N. M.; Rondon, R.; Grunau, C.; Cosseau, C.; Smith, K. M.; Freitag, M.; Adjeroud, M.; Mitta, G. Thermal Stress Triggers Broad Pocillopora damicornis Transcriptomic Remodeling, while Vibrio coralliilyticus Infection Induces a More Targeted Immuno-Suppression Response, PLoS ONE, Volume 9 (2014) no. 9 | DOI

[102] Vidal-Dupiol, J.; Adjeroud, M.; Roger, E.; Foure, L.; Duval, D.; Mone, Y.; Ferrier-Pages, C.; Tambutte, E.; Tambutte, S.; Zoccola, D.; Allemand, D.; Mitta, G. Coral bleaching under thermal stress: putative involvement of host/symbiont recognition mechanisms, BMC Physiology, Volume 9 (2009) no. 1 | DOI

[103] Weis, V. M. Cellular mechanisms of Cnidarian bleaching: stress causes the collapse of symbiosis, Journal of Experimental Biology, Volume 211 (2008) no. 19, pp. 3059-3066 | DOI

[104] Whitaker, K. Genetic evidence for mixed modes of reproduction in the coral Pocillopora damicornis and its effect on population structure, Marine Ecology Progress Series, Volume 306 (2006), pp. 115-124 | DOI

[105] Ziegler, M.; Seneca, F. O.; Yum, L. K.; Palumbi, S. R.; Voolstra, C. R. Bacterial community dynamics are linked to patterns of coral heat tolerance, Nature Communications, Volume 8 (2017) no. 1 | DOI

[106] Zilber-Rosenberg, I.; Rosenberg, E. Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution, FEMS Microbiology Reviews, Volume 32 (2008) no. 5, pp. 723-735 | DOI

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