Comparative genomics explains the evolutionary success of reef-forming corals

• Published in: eLife Vol. 5
• Main Authors: Bhattacharya, Debashish, Agrawal, Shobhit, Aranda, Manuel, Baumgarten, Sebastian, Belcaid, Mahdi, Drake, Jeana L, Erwin, Douglas, Foret, Sylvian, Gates, Ruth D, Gruber, David F, Kamel, Bishoy, Lesser, Michael P, Levy, Oren, Liew, Yi Jin, MacManes, Matthew, Mass, Tali, Medina, Monica, Mehr, Shaadi, Meyer, Eli, Price, Dana C, Putnam, Hollie M, Qiu, Huan, Shinzato, Chuya, Shoguchi, Eiichi, Stokes, Alexander J, Tambutté, Sylvie, Tchernov, Dan, Voolstra, Christian R, Wagner, Nicole, Walker, Charles W, Weber, Andreas PM, Weis, Virginia, Zelzion, Ehud, Zoccola, Didier, Falkowski, Paul G
• Format: Journal Article
• Language: English
• Published: England eLife Science Publications, Ltd 24.05.2016; eLife Sciences Publications Ltd; eLife Sciences Publications, Ltd
• Subjects: Adaptation, Physiological - genetics; Animals; Anthozoa - classification; Anthozoa - genetics; Anthozoa - growth & development; Anthozoa - metabolism; Apoptosis; Biological Evolution; biomineralization; Calcification, Physiologic - genetics; Calcium Carbonate - chemistry; Calcium Carbonate - metabolism; Cnidaria; Coral Reefs; Corals; DNA sequencing; Ecology; Environmental stress; Evolution; Evolutionary Biology; Evolutionary genetics; Gene transfer; Gene Transfer, Horizontal; Genes; Genetic aspects; Genome; Genomes; Genomics; Genomics - methods; horizontal gene transfer; Hydrogen-Ion Concentration; Light; Light effects; Marine biology; Metabolic Networks and Pathways - genetics; Methods; Museums; Nucleotide sequencing; pH effects; Photosynthesis - physiology; Phylogenetics; Phylogeny; Physiology; Proteins; Reactive nitrogen species; Reactive Nitrogen Species - metabolism; Reactive oxygen species; Reactive Oxygen Species - metabolism; Science; Scleractinia; stress response; Stress, Physiological; Symbionts; symbiosis; Symbiosis - physiology; Temperature; Trees; United States > US; ecology; symbiotsis; corals; evolutionary biology; stress response; biomineralization; genomics; horizontal gene transfer
• ISSN: 2050-084X; 2050-084X
• DOI: 10.7554/eLife.13288

Transcriptome and genome data from twenty stony coral species and a selection of reference bilaterians were studied to elucidate coral evolutionary history. We identified genes that encode the proteins responsible for the precipitation and aggregation of the aragonite skeleton on which the organisms live, and revealed a network of environmental sensors that coordinate responses of the host animals to temperature, light, and pH. Furthermore, we describe a variety of stress-related pathways, including apoptotic pathways that allow the host animals to detoxify reactive oxygen and nitrogen species that are generated by their intracellular photosynthetic symbionts, and determine the fate of corals under environmental stress. Some of these genes arose through horizontal gene transfer and comprise at least 0.2% of the animal gene inventory. Our analysis elucidates the evolutionary strategies that have allowed symbiotic corals to adapt and thrive for hundreds of millions of years. For millions of years, reef-building stony corals have created extensive habitats for numerous marine plants and animals in shallow tropical seas. Stony corals consist of many small, tentacled animals called polyps. These polyps secrete a mineral called aragonite to create the reef – an external ‘skeleton’ that supports and protects the corals. Photosynthesizing algae live inside the cells of stony corals, and each species depends on the other to survive. The algae produce the coral’s main source of food, although they also produce some waste products that can harm the coral if they build up inside cells. If the oceans become warmer and more acidic, the coral are more likely to become stressed and expel the algae from their cells in a process known as coral bleaching. This makes the coral more likely to die or become diseased. Corals have survived previous periods of ocean warming, although it is not known how they evolved to do so. The evolutionary history of an organism can be traced by studying its genome – its complete set of DNA – and the RNA molecules encoded by these genes. Bhattacharya et al. performed this analysis for twenty stony coral species, and compared the resulting genome and RNA sequences with the genomes of other related marine organisms, such as sea anemones and sponges. In particular, Bhattacharya et al. examined “ortholog” groups of genes, which are present in different species and evolved from a common ancestral gene. This analysis identified the genes in the corals that encode the proteins responsible for constructing the aragonite skeleton. The coral genome also encodes a network of environmental sensors that coordinate how the polyps respond to temperature, light and acidity. Bhattacharya et al. also uncovered a variety of stress-related pathways, including those that detoxify the polyps of the damaging molecules generated by algae, and the pathways that enable the polyps to adapt to environmental stress. Many of these genes were recruited from other species in a process known as horizontal gene transfer. The oceans are expected to become warmer and more acidic in the coming centuries. Provided that humans do not physically destroy the corals’ habitats, the evidence found by Bhattacharya et al. suggests that the genome of the corals contains the diversity that will allow them to adapt to these new conditions.