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      First Evidence of an Important Organic Matter Trophic Pathway between Temperate Corals and Pelagic Microbial Communities

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          Abstract

          Mucus, i.e., particulate and dissolved organic matter (POM, DOM) released by corals, acts as an important energy carrier in tropical ecosystems, but little is known on its ecological role in temperate environments. This study assessed POM and DOM production by the temperate coral Cladocora caespitosa under different environmental conditions. The subsequent enzymatic degradation, growth of prokaryotes and virus-like particles (VLPs) as well as changes in the structure of the prokaryotic communities were also monitored. C. caespitosa produced an important quantity of mucus, which varied according to the environmental conditions (from 37.8 to 67.75 nmol carbon h -1 cm -2), but remained higher or comparable to productions observed in tropical corals. It has an important nutritional value, as highlighted by the high content in dissolved nitrogen (50% to 90% of the organic matter released). Organic matter was rapidly degraded by prokaryotes’ enzymatic activities, and due to its nitrogen content, aminopeptidase activity was 500 fold higher than the α-glucosidase activity. Prokaryotes, as well as VLPs, presented a rapid growth in the mucus, with prokaryote production rates as high as 0.31 μg h -1 L -1. Changes in bacterial and archaeal communities were observed in the ageing mucus and between mucus and the water column, suggesting a clear impact of mucus on microorganism diversity. Overall, our results show that the organic matter released by temperate corals, such as C. caespitosa, which can form reef structures in the Mediterranean Sea, stimulates microbial activity and thereby functions as a significant carbon and nitrogen supplier to the microbial loop.

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          Most cited references13

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          Water flow modulates the response of coral reef communities to ocean acidification

          By the end of the century coral reefs likely will be affected negatively by ocean acidification (OA), but both the effects of OA on coral communities and the crossed effects of OA with other physical environmental variables are lacking. One of the least considered physical parameters is water flow, which is surprising considering its strong role in modulating the physiology of reef organisms and communities. In the present study, the effects of flow were tested on coral reef communities maintained in outdoor flumes under ambient pCO2 and high pCO2 (1300 μatm). Net calcification of coral communities, including sediments, was affected by both flow and pCO2 with calcification correlated positively with flow under both pCO2 treatments. The effect of flow was less evident for sediments where dissolution exceeded precipitation of calcium carbonate under all flow speeds at high pCO2. For corals and calcifying algae there was a strong flow effect, particularly at high pCO2 where positive net calcification was maintained at night in the high flow treatment. Our results demonstrate the importance of water flow in modulating the coral reef community response to OA and highlight the need to consider this parameter when assessing the effects of OA on coral reefs.
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            Down under the tunic: bacterial biodiversity hotspots and widespread ammonia-oxidizing archaea in coral reef ascidians.

            Ascidians are ecologically important components of marine ecosystems yet the ascidian microbiota remains largely unexplored beyond a few model species. We used 16S rRNA gene tag pyrosequencing to provide a comprehensive characterization of microbial symbionts in the tunic of 42 Great Barrier Reef ascidian samples representing 25 species. Results revealed high bacterial biodiversity (3 217 unique operational taxonomic units (OTU0.03) from 19 described and 14 candidate phyla) and the widespread occurrence of ammonia-oxidizing Thaumarchaeota in coral reef ascidians (24 of 25 host species). The ascidian microbiota was clearly differentiated from seawater microbial communities and included symbiont lineages shared with other invertebrate hosts as well as unique, ascidian-specific phylotypes. Several rare seawater microbes were markedly enriched (200-700 fold) in the ascidian tunic, suggesting that the rare biosphere of seawater may act as a conduit for horizontal symbiont transfer. However, most OTUs (71%) were rare and specific to single hosts and a significant correlation between host relatedness and symbiont community similarity was detected, indicating a high degree of host-specificity and potential role of vertical transmission in structuring these communities. We hypothesize that the complex ascidian microbiota revealed herein is maintained by the dynamic microenvironments within the ascidian tunic, offering optimal conditions for different metabolic pathways such as ample chemical substrate (ammonia-rich host waste) and physical habitat (high oxygen, low irradiance) for nitrification. Thus, ascidian hosts provide unique and fertile niches for diverse microorganisms and may represent an important and previously unrecognized habitat for nitrite/nitrate regeneration in coral reef ecosystems.
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              Microbes enriched in seawater after addition of coral mucus.

              We investigated which microbial taxa in coastal Red Sea water were stimulated by addition of mucus from the coral Fungia sp. Decreases in the concentration and C/N ratio of particulate organic material during short-term incubations (50 h) were paralleled by a steep rise in the number of Gammaproteobacteria, particularly Alteromonadaceae, followed by Vibrionaceae. Two almost identical genotypes affiliated with Alteromonas macleodii accounted for up to >85% of all Alteromonadaceae (45% of the total cells) in the mucus-amended enrichments but were rare in unamended control incubations and in ambient seawater. A. macleodii-like bacteria might thus be important in the transfer of organic carbon from coral mucus to the pelagic microbial food webs of coral reefs.
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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
                14 October 2015
                2015
                : 10
                : 10
                : e0139175
                Affiliations
                [1 ]Department of marine biology, Ecophysiology team, Centre Scientifique de Monaco, Monaco, Monaco
                [2 ]UMR CARRTEL, INRA, Station d’Hydrobiologie Lacustre, Thonon-les-Bains, France
                CAS, CHINA
                Author notes

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

                Conceived and designed the experiments: JAF CFP SR SJ. Performed the experiments: JAF BL SJ. Analyzed the data: JAF CFP SR SJ. Contributed reagents/materials/analysis tools: JAF CFP SR BL SJ. Wrote the paper: JAF CFP SR SJ.

                [¤]

                Current address: Department of experimental limnology, Leibniz-Institute of Freshwater Ecology and Inland Fisheries, Stechlin, Germany

                Article
                PONE-D-15-24782
                10.1371/journal.pone.0139175
                4605525
                26466126
                4d05e9f9-65f9-4bb9-bcea-0a30b712854d
                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
                : 9 June 2015
                : 8 September 2015
                Page count
                Figures: 8, Tables: 1, Pages: 22
                Funding
                The funding for this study came from the government of the principality of Monaco.
                Categories
                Research Article
                Custom metadata
                All relevant data are within the paper and its Supporting Information file.

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