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      The Skeletal Proteome of the Coral Acropora millepora: The Evolution of Calcification by Co-Option and Domain Shuffling

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          Abstract

          In corals, biocalcification is a major function that may be drastically affected by ocean acidification (OA). Scleractinian corals grow by building up aragonitic exoskeletons that provide support and protection for soft tissues. Although this process has been extensively studied, the molecular basis of biocalcification is poorly understood. Notably lacking is a comprehensive catalog of the skeleton-occluded proteins—the skeletal organic matrix proteins (SOMPs) that are thought to regulate the mineral deposition. Using a combination of proteomics and transcriptomics, we report the first survey of such proteins in the staghorn coral Acropora millepora. The organic matrix (OM) extracted from the coral skeleton was analyzed by mass spectrometry and bioinformatics, enabling the identification of 36 SOMPs. These results provide novel insights into the molecular basis of coral calcification and the macroevolution of metazoan calcifying systems, whereas establishing a platform for studying the impact of OA at molecular level. Besides secreted proteins, extracellular regions of transmembrane proteins are also present, suggesting a close control of aragonite deposition by the calicoblastic epithelium. In addition to the expected SOMPs (Asp/Glu-rich, galaxins), the skeletal repertoire included several proteins containing known extracellular matrix domains. From an evolutionary perspective, the number of coral-specific proteins is low, many SOMPs having counterparts in the noncalcifying cnidarians. Extending the comparison with the skeletal OM proteomes of other metazoans allowed the identification of a pool of functional domains shared between phyla. These data suggest that co-option and domain shuffling may be general mechanisms by which the trait of calcification has evolved.

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          Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming

          Ocean acidification represents a threat to marine species worldwide, and forecasting the ecological impacts of acidification is a high priority for science, management, and policy. As research on the topic expands at an exponential rate, a comprehensive understanding of the variability in organisms' responses and corresponding levels of certainty is necessary to forecast the ecological effects. Here, we perform the most comprehensive meta-analysis to date by synthesizing the results of 228 studies examining biological responses to ocean acidification. The results reveal decreased survival, calcification, growth, development and abundance in response to acidification when the broad range of marine organisms is pooled together. However, the magnitude of these responses varies among taxonomic groups, suggesting there is some predictable trait-based variation in sensitivity, despite the investigation of approximately 100 new species in recent research. The results also reveal an enhanced sensitivity of mollusk larvae, but suggest that an enhanced sensitivity of early life history stages is not universal across all taxonomic groups. In addition, the variability in species' responses is enhanced when they are exposed to acidification in multi-species assemblages, suggesting that it is important to consider indirect effects and exercise caution when forecasting abundance patterns from single-species laboratory experiments. Furthermore, the results suggest that other factors, such as nutritional status or source population, could cause substantial variation in organisms' responses. Last, the results highlight a trend towards enhanced sensitivity to acidification when taxa are concurrently exposed to elevated seawater temperature.
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            Using the Acropora digitifera genome to understand coral responses to environmental change.

            Despite the enormous ecological and economic importance of coral reefs, the keystone organisms in their establishment, the scleractinian corals, increasingly face a range of anthropogenic challenges including ocean acidification and seawater temperature rise. To understand better the molecular mechanisms underlying coral biology, here we decoded the approximately 420-megabase genome of Acropora digitifera using next-generation sequencing technology. This genome contains approximately 23,700 gene models. Molecular phylogenetics indicate that the coral and the sea anemone Nematostella vectensis diverged approximately 500 million years ago, considerably earlier than the time over which modern corals are represented in the fossil record (∼240 million years ago). Despite the long evolutionary history of the endosymbiosis, no evidence was found for horizontal transfer of genes from symbiont to host. However, unlike several other corals, Acropora seems to lack an enzyme essential for cysteine biosynthesis, implying dependency of this coral on its symbionts for this amino acid. Corals inhabit environments where they are frequently exposed to high levels of solar radiation, and analysis of the Acropora genome data indicates that the coral host can independently carry out de novo synthesis of mycosporine-like amino acids, which are potent ultraviolet-protective compounds. In addition, the coral innate immunity repertoire is notably more complex than that of the sea anemone, indicating that some of these genes may have roles in symbiosis or coloniality. A number of genes with putative roles in calcification were identified, and several of these are restricted to corals. The coral genome provides a platform for understanding the molecular basis of symbiosis and responses to environmental changes.
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              Declining coral calcification on the Great Barrier Reef.

              Reef-building corals are under increasing physiological stress from a changing climate and ocean absorption of increasing atmospheric carbon dioxide. We investigated 328 colonies of massive Porites corals from 69 reefs of the Great Barrier Reef (GBR) in Australia. Their skeletal records show that throughout the GBR, calcification has declined by 14.2% since 1990, predominantly because extension (linear growth) has declined by 13.3%. The data suggest that such a severe and sudden decline in calcification is unprecedented in at least the past 400 years. Calcification increases linearly with increasing large-scale sea surface temperature but responds nonlinearly to annual temperature anomalies. The causes of the decline remain unknown; however, this study suggests that increasing temperature stress and a declining saturation state of seawater aragonite may be diminishing the ability of GBR corals to deposit calcium carbonate.
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                Author and article information

                Journal
                Mol Biol Evol
                Mol. Biol. Evol
                molbev
                molbiolevol
                Molecular Biology and Evolution
                Oxford University Press
                0737-4038
                1537-1719
                September 2013
                12 June 2013
                12 June 2013
                : 30
                : 9
                : 2099-2112
                Affiliations
                1UMR 6282 CNRS, Biogéosciences, Université de Bourgogne, Dijon, France
                2Computational Science Section, Informatics Institute, Universiteit van Amsterdam, Amsterdam, The Netherlands
                3ARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, Queensland, Australia
                4UMR 7245 CNRS, MCAM, Muséum National d’Histoire Naturelle (MNHN), Paris, France
                5IFR 128 BioSciences Gerland-Lyon Sud, UMR 5086 CNRS, Institut de Biologie et Chimie des Protéines, Université de Lyon, Lyon, France
                Author notes

                Associate editor: Charles Delwiche

                Data deposition: Protein sequence data reported in this article have been deposited in the UniProt Knowledgebase (accession nos. B3EWY[6-9], B3EWZ[0-9], B3EX0[0-2], B7W112, B7W114, B7WFQ1, B8RJM0, B8UU51, B8UU59, G8HTB6 B8UU74, D9IQ16, B8UU78, B8V7P3, B8V7Q1, B8V7R6, B8V7S0, B7T7N1, B8VIV4, B8VIU6, B8VIW9, B8VIX3, and B8WI85).

                Article
                mst109
                10.1093/molbev/mst109
                3748352
                23765379
                131e17b0-5cb8-4fd8-bcf7-9127e033604c
                © The Author 2013. Published by Oxford University Press.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License ( http://creativecommons.org/licenses/by-nc/3.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com

                Page count
                Pages: 14
                Categories
                Discoveries

                Molecular biology

                biomineralization, calcium carbonate skeleton, scleractinian, proteomics, evolution

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