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      Transcriptomic Changes in Coral Holobionts Provide Insights into Physiological Challenges of Future Climate and Ocean Change

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          Abstract

          Tropical reef-building coral stress levels will intensify with the predicted rising atmospheric CO 2 resulting in ocean temperature and acidification increase. Most studies to date have focused on the destabilization of coral-dinoflagellate symbioses due to warming oceans, or declining calcification due to ocean acidification. In our study, pH and temperature conditions consistent with the end-of-century scenarios of the Intergovernmental Panel on Climate Change (IPCC) caused major changes in photosynthesis and respiration, in addition to decreased calcification rates in the coral Acropora millepora. Population density of symbiotic dinoflagellates ( Symbiodinium) under high levels of ocean acidification and temperature (Representative Concentration Pathway, RCP8.5) decreased to half of that found under present day conditions, with photosynthetic and respiratory rates also being reduced by 40%. These physiological changes were accompanied by evidence for gene regulation of calcium and bicarbonate transporters along with components of the organic matrix. Metatranscriptomic RNA-Seq data analyses showed an overall down regulation of metabolic transcripts, and an increased abundance of transcripts involved in circadian clock control, controlling the damage of oxidative stress, calcium signaling/homeostasis, cytoskeletal interactions, transcription regulation, DNA repair, Wnt signaling and apoptosis/immunity/ toxins. We suggest that increased maintenance costs under ocean acidification and warming, and diversion of cellular ATP to pH homeostasis, oxidative stress response, UPR and DNA repair, along with metabolic suppression, may underpin why Acroporid species tend not to thrive under future environmental stress. Our study highlights the potential increased energy demand when the coral holobiont is exposed to high levels of ocean warming and acidification.

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          Most cited references42

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          Ocean acidification: the other CO2 problem.

          Rising atmospheric carbon dioxide (CO2), primarily from human fossil fuel combustion, reduces ocean pH and causes wholesale shifts in seawater carbonate chemistry. The process of ocean acidification is well documented in field data, and the rate will accelerate over this century unless future CO2 emissions are curbed dramatically. Acidification alters seawater chemical speciation and biogeochemical cycles of many elements and compounds. One well-known effect is the lowering of calcium carbonate saturation states, which impacts shell-forming marine organisms from plankton to benthic molluscs, echinoderms, and corals. Many calcifying species exhibit reduced calcification and growth rates in laboratory experiments under high-CO2 conditions. Ocean acidification also causes an increase in carbon fixation rates in some photosynthetic organisms (both calcifying and noncalcifying). The potential for marine organisms to adapt to increasing CO2 and broader implications for ocean ecosystems are not well known; both are high priorities for future research. Although ocean pH has varied in the geological past, paleo-events may be only imperfect analogs to current conditions.
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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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              Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms.

              Ocean acidification is a pervasive stressor that could affect many marine organisms and cause profound ecological shifts. A variety of biological responses to ocean acidification have been measured across a range of taxa, but this information exists as case studies and has not been synthesized into meaningful comparisons amongst response variables and functional groups. We used meta-analytic techniques to explore the biological responses to ocean acidification, and found negative effects on survival, calcification, growth and reproduction. However, there was significant variation in the sensitivity of marine organisms. Calcifying organisms generally exhibited larger negative responses than non-calcifying organisms across numerous response variables, with the exception of crustaceans, which calcify but were not negatively affected. Calcification responses varied significantly amongst organisms using different mineral forms of calcium carbonate. Organisms using one of the more soluble forms of calcium carbonate (high-magnesium calcite) can be more resilient to ocean acidification than less soluble forms (calcite and aragonite). Additionally, there was variation in the sensitivities of different developmental stages, but this variation was dependent on the taxonomic group. Our analyses suggest that the biological effects of ocean acidification are generally large and negative, but the variation in sensitivity amongst organisms has important implications for ecosystem responses. © 2010 Blackwell Publishing Ltd/CNRS.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                28 October 2015
                2015
                : 10
                : 10
                : e0139223
                Affiliations
                [1 ]Australian Institute of Marine Science, PMB 3, Townsville MC, Queensland, Australia
                [2 ]School of Biological Sciences, The University of Queensland, St Lucia, Queensland, Australia
                [3 ]School of Agriculture and Food Sciences, The University of Queensland, St Lucia, Queensland, Australia
                [4 ]Scripps Institution of Oceanography, University of California San Diego, La Jolla, California, United States of America
                [5 ]University of Queensland Centre for Clinical Research, The University of Queensland, Herston, Queensland, Australia
                [6 ]Global Change Institute and ARC Centre of Excellence for Coral Reef Studies, The University of Queensland, St Lucia, Queensland, Australia
                Pennsylvania State University, UNITED STATES
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: PK DK OH SD. Performed the experiments: PK. Analyzed the data: PK CKKC EYSL DE NR. Wrote the paper: PK CKKC DK EYSL NR DE OH SD.

                Article
                PONE-D-15-13112
                10.1371/journal.pone.0139223
                4624983
                26510159
                a807d381-29fb-470a-8ded-d4458e7cc76a
                Copyright @ 2015

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited

                History
                : 26 March 2015
                : 9 September 2015
                Page count
                Figures: 5, Tables: 3, Pages: 30
                Funding
                This work was funded by the Australian Research Council. The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript.
                Categories
                Research Article
                Custom metadata
                The RNA-seq reads used in this study have been submitted to NCBI under BioProject accession number PRJNA269992.

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                Uncategorized

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