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      Light Respiratory Processes and Gross Photosynthesis in Two Scleractinian Corals

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          Abstract

          The light dependency of respiratory activity of two scleractinian corals was examined using O 2 microsensors and CO 2 exchange measurements. Light respiration increased strongly but asymptotically with elevated irradiance in both species. Light respiration in Pocillopora damicornis was higher than in Pavona decussata under low irradiance, indicating species-specific differences in light-dependent metabolic processes. Overall, the coral P. decussata exhibited higher CO 2 uptake rates than P. damicornis over the experimental irradiance range. P. decussata also harboured twice as many algal symbionts and higher total protein biomass compared to P. damicornis, possibly resulting in self-shading of the symbionts and/or changes in host tissue specific light distribution. Differences in light respiration and CO 2 availability could be due to host-specific characteristics that modulate the symbiont microenvironment, its photosynthesis, and hence the overall performance of the coral holobiont.

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          Most cited references15

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          Cohesive molecular genetic data delineate species diversity in the dinoflagellate genus Symbiodinium.

          The diversity of symbiotic dinoflagellates (Symbiodinium) in pocilloporid corals originating from various reef habitats surrounding Heron Island, southern Great Barrier Reef, was examined by targeting ribosomal, mitochondrial, and chloroplast genes using six methods that analyse for sequence differences. The ability of each of 13 genetic analyses to characterize eight ecologically distinct Symbiodinium spp. was dependent on the level of conservation of the gene region targeted and the technique used. Other than differences in resolution, phylogenetic reconstructions using nuclear and organelle gene sequences were complementary and when combined produced a well-resolved phylogeny. Analysis of the ribosomal internal transcribed spacers using denaturing gradient gel electrophoresis fingerprinting in combination with sequencing of dominant bands provided a precise method for rapidly resolving and characterizing symbionts into ecologically and evolutionarily distinct units of diversity. Single-stranded conformation polymorphisms of the nuclear ribosomal large subunit (D1/D2 domain) identified the same number of ecologically distinct Symbiodinium spp., but profiles were less distinctive. The repetitive sequencing of bacterially cloned ITS2 polymerase chain reaction amplifications generated numerous sequence variants that clustered together according to the symbiont under analysis. The phylogenetic relationships between these clusters show how intragenomic variation in the ribosomal array diverges among closely related eukaryotic genomes. The strong correlation between phylogenetically independent lineages with different ecological and physiological attributes establishes a clear basis for assigning species designations to members of the genus Symbiodinium.
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            Carbonic anhydrase in the scleractinian coral Stylophora pistillata: characterization, localization, and role in biomineralization.

            Carbonic anhydrases (CA) play an important role in biomineralization from invertebrates to vertebrates. Previous experiments have investigated the role of CA in coral calcification, mainly by pharmacological approaches. This study reports the molecular cloning, sequencing, and immunolocalization of a CA isolated from the scleractinian coral Stylophora pistillata, named STPCA. Results show that STPCA is a secreted form of alpha-CA, which possesses a CA catalytic function, similar to the secreted human CAVI. We localized this enzyme at the calicoblastic ectoderm level, which is responsible for the precipitation of the skeleton. This localization supports the role of STPCA in the calcification process. In symbiotic scleractinian corals, calcification is stimulated by light, a phenomenon called "light-enhanced calcification" (LEC). The mechanism by which symbiont photosynthesis stimulates calcification is still enigmatic. We tested the hypothesis that coral genes are differentially expressed under light and dark conditions. By real-time PCR, we investigated the differential expression of STPCA to determine its role in the LEC phenomenon. Results show that the STPCA gene is expressed 2-fold more during the dark than the light. We suggest that in the dark, up-regulation of the STPCA gene represents a mechanism to cope with night acidosis.
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              Sources and mechanisms of inorganic carbon transport for coral calcification and photosynthesis.

              The sources and mechanisms of inorganic carbon transport for scleractinian coral calcification and photosynthesis were studied using a double labelling technique with H(14)CO(3) and (45)Ca. Clones of Stylophora pistillata that had developed into microcolonies were examined. Compartmental and pharmacological analyses of the distribution of(45)Ca and H(14)CO(3) in the coelenteron, tissues and skeleton were performed in dark or light conditions or in the presence of various seawater HCO(3)(-) concentrations. For calcification, irrespective of the lighting conditions, the major source of dissolved inorganic carbon (DIC) is metabolic CO(2) (70-75% of total CaCO(3) deposition), while only 25-30% originates from the external medium (seawater carbon pool). These results are in agreement with the observation that metabolic CO(2) production in the light is at least six times greater than is required for calcification. This source is dependent on carbonic anhydrase activity because it is sensitive to ethoxyzolamide. Seawater DIC is transferred from the external medium to the coral skeleton by two different pathways: from sea water to the coelenteron, the passive paracellular pathway is largely sufficient, while a DIDS-sensitive transcellular pathway appears to mediate the flux across calicoblastic cells. Irrespective of the source, an anion exchanger performs the secretion of DIC at the site of calcification. Furthermore, a fourfold light-enhanced calcification of Stylophora pistillata microcolonies was measured. This stimulation was only effective after a lag of 10 min. These results are discussed in the context of light-enhanced calcification. Characterisation of the DIC supply for symbiotic dinoflagellate photosynthesis demonstrated the presence of a DIC pool within the tissues. The size of this pool was dependent on the lighting conditions, since it increased 39-fold after 3 h of illumination. Passive DIC equilibration through oral tissues between sea water and the coelenteric cavity is insufficient to supply this DIC pool, suggesting that there is an active transepithelial absorption of inorganic carbon sensitive to DIDS, ethoxyzolamide and iodide. These results confirm the presence of CO(2)-concentrating mechanisms in coral cells. The tissue pool is not, however, used as a source for calcification since no significant lag phase in the incorporation of external seawater DIC was measured.
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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, USA )
                1932-6203
                2014
                31 October 2014
                : 9
                : 10
                : e110814
                Affiliations
                [1 ]Plant Functional Biology and Climate Change Cluster, School of the Environment, University of Technology, Sydney, Ultimo, New South Wales, Australia
                [2 ]Centre for Marine Bio-Innovation and Sydney Institute of Marine Science, School of Biological, Earth and Environmental Sciences, The University of New South Wales, Sydney, New South Wales, Australia
                [3 ]Marine Biological Section, Department of Biology, University of Copenhagen, Helsingør, Denmark
                [4 ]Singapore Centre on Environmental Life Sciences Engineering, School of Biological Sciences, Nanyang Technological University, Singapore, Singapore
                Auckland University of Technology, New Zealand
                Author notes

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

                N/A. Conceived and designed the experiments: VS AWDL DW MK PJR. Performed the experiments: VS DW AWDL. Analyzed the data: VS DW AWDL. Contributed reagents/materials/analysis tools: VS DW MK PJR. Wrote the paper: VS DW RH MK AWDL PJR.

                ¶ AWDL and PJR are joint last authors on this work.

                Article
                PONE-D-14-23162
                10.1371/journal.pone.0110814
                4216011
                25360746
                ee71cbc3-e989-4740-93d0-f5f966f0bfbe
                Copyright @ 2014

                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
                : 28 May 2014
                : 25 September 2014
                Page count
                Pages: 9
                Funding
                This work was funded by grant #DP110105200 awarded by the Australian Research Council, http://www.arc.gov.au to PR and the Danish Council for Independent Research| Natural Science, http://ufm.dk/en/research-and-innovation/councils-and-commissions/the-danish-council-for-independent-research/the-council-1/the-danish-council-for-independent-research-natural-sciences to MK, as well as Postgraduate scholarships from the University of Technology, Sydney to VS and DW. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Chronobiology
                Daylight
                Ecology
                Coastal Ecology
                Ecophysiology
                Marine Ecology
                Marine Biology
                Physiology
                Plant Science
                Earth Sciences
                Marine and Aquatic Sciences
                Aquatic Environments
                Marine Environments
                Ecology and Environmental Sciences
                Custom metadata
                The authors confirm that all data underlying the findings are fully available without restriction. All relevant data are within the paper.

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