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Warm seawater temperature promotes substrate colonization by the blue coral, Heliopora coerulea

BACKGROUND: Heliopora coerulea, the blue coral, is a reef building octocoral that is reported to have a higher optimum temperature for growth compared to most scleractinian corals. This octocoral has been observed to grow over both live and dead scleractinians and to dominate certain reefs in the In...

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Autores principales: Guzman, Christine, Atrigenio, Michael, Shinzato, Chuya, Aliño, Porfirio, Conaco, Cecilia
Formato: Online Artículo Texto
Lenguaje:English
Publicado: PeerJ Inc. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6768060/
https://www.ncbi.nlm.nih.gov/pubmed/31579631
http://dx.doi.org/10.7717/peerj.7785
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author Guzman, Christine
Atrigenio, Michael
Shinzato, Chuya
Aliño, Porfirio
Conaco, Cecilia
author_facet Guzman, Christine
Atrigenio, Michael
Shinzato, Chuya
Aliño, Porfirio
Conaco, Cecilia
author_sort Guzman, Christine
collection PubMed
description BACKGROUND: Heliopora coerulea, the blue coral, is a reef building octocoral that is reported to have a higher optimum temperature for growth compared to most scleractinian corals. This octocoral has been observed to grow over both live and dead scleractinians and to dominate certain reefs in the Indo-Pacific region. The molecular mechanisms underlying the ability of H. coerulea to tolerate warmer seawater temperatures and to effectively compete for space on the substrate remain to be elucidated. METHODS: In this study, we subjected H. coerulea colonies to various temperatures for up to 3 weeks. The growth and photosynthetic efficiency rates of the coral colonies were measured. We then conducted pairwise comparisons of gene expression among the different coral tissue regions to identify genes and pathways that are expressed under different temperature conditions. RESULTS: A horizontal growth rate of 1.13 ± 0.25 mm per week was observed for corals subjected to 28 or 31 °C. This growth rate was significantly higher compared to corals exposed at 26 °C. This new growth was characterized by the extension of whitish tissue at the edges of the colony and was enriched for a matrix metallopeptidase, a calcium and integrin binding protein, and other transcripts with unknown function. Tissues at the growth margin and the adjacent calcified encrusting region were enriched for transcripts related to proline and riboflavin metabolism, nitrogen utilization, and organic cation transport. The calcified digitate regions, on the other hand, were enriched for transcripts encoding proteins involved in cell-matrix adhesion, translation, receptor-mediated endocytosis, photosynthesis, and ion transport. Functions related to lipid biosynthesis, extracellular matrix formation, cell migration, and oxidation-reduction processes were enriched at the growth margin in corals subjected for 3 weeks to 28 or 31 °C relative to corals at 26 °C. In the digitate region of the coral, transcripts encoding proteins that protect against oxidative stress, modify cell membrane composition, and mediate intercellular signaling pathways were enriched after just 24 h of exposure to 31 °C compared to corals at 28 °C. The overall downregulation of gene expression observed after 3 weeks of sustained exposure to 31 °C is likely compensated by symbiont metabolism. DISCUSSION: These findings reveal that the different regions of H. coerulea have variable gene expression profiles and responses to temperature variation. Under warmer conditions, the blue coral invests cellular resources toward extracellular matrix formation and cellular migration at the colony margins, which may promote rapid tissue growth and extension. This mechanism enables the coral to colonize adjacent reef substrates and successfully overgrow slower growing scleractinian corals that may already be more vulnerable to warming ocean waters.
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spelling pubmed-67680602019-10-02 Warm seawater temperature promotes substrate colonization by the blue coral, Heliopora coerulea Guzman, Christine Atrigenio, Michael Shinzato, Chuya Aliño, Porfirio Conaco, Cecilia PeerJ Computational Biology BACKGROUND: Heliopora coerulea, the blue coral, is a reef building octocoral that is reported to have a higher optimum temperature for growth compared to most scleractinian corals. This octocoral has been observed to grow over both live and dead scleractinians and to dominate certain reefs in the Indo-Pacific region. The molecular mechanisms underlying the ability of H. coerulea to tolerate warmer seawater temperatures and to effectively compete for space on the substrate remain to be elucidated. METHODS: In this study, we subjected H. coerulea colonies to various temperatures for up to 3 weeks. The growth and photosynthetic efficiency rates of the coral colonies were measured. We then conducted pairwise comparisons of gene expression among the different coral tissue regions to identify genes and pathways that are expressed under different temperature conditions. RESULTS: A horizontal growth rate of 1.13 ± 0.25 mm per week was observed for corals subjected to 28 or 31 °C. This growth rate was significantly higher compared to corals exposed at 26 °C. This new growth was characterized by the extension of whitish tissue at the edges of the colony and was enriched for a matrix metallopeptidase, a calcium and integrin binding protein, and other transcripts with unknown function. Tissues at the growth margin and the adjacent calcified encrusting region were enriched for transcripts related to proline and riboflavin metabolism, nitrogen utilization, and organic cation transport. The calcified digitate regions, on the other hand, were enriched for transcripts encoding proteins involved in cell-matrix adhesion, translation, receptor-mediated endocytosis, photosynthesis, and ion transport. Functions related to lipid biosynthesis, extracellular matrix formation, cell migration, and oxidation-reduction processes were enriched at the growth margin in corals subjected for 3 weeks to 28 or 31 °C relative to corals at 26 °C. In the digitate region of the coral, transcripts encoding proteins that protect against oxidative stress, modify cell membrane composition, and mediate intercellular signaling pathways were enriched after just 24 h of exposure to 31 °C compared to corals at 28 °C. The overall downregulation of gene expression observed after 3 weeks of sustained exposure to 31 °C is likely compensated by symbiont metabolism. DISCUSSION: These findings reveal that the different regions of H. coerulea have variable gene expression profiles and responses to temperature variation. Under warmer conditions, the blue coral invests cellular resources toward extracellular matrix formation and cellular migration at the colony margins, which may promote rapid tissue growth and extension. This mechanism enables the coral to colonize adjacent reef substrates and successfully overgrow slower growing scleractinian corals that may already be more vulnerable to warming ocean waters. PeerJ Inc. 2019-09-27 /pmc/articles/PMC6768060/ /pubmed/31579631 http://dx.doi.org/10.7717/peerj.7785 Text en © 2019 Guzman et al. https://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, reproduction and adaptation in any medium and for any purpose provided that it is properly attributed. For attribution, the original author(s), title, publication source (PeerJ) and either DOI or URL of the article must be cited.
spellingShingle Computational Biology
Guzman, Christine
Atrigenio, Michael
Shinzato, Chuya
Aliño, Porfirio
Conaco, Cecilia
Warm seawater temperature promotes substrate colonization by the blue coral, Heliopora coerulea
title Warm seawater temperature promotes substrate colonization by the blue coral, Heliopora coerulea
title_full Warm seawater temperature promotes substrate colonization by the blue coral, Heliopora coerulea
title_fullStr Warm seawater temperature promotes substrate colonization by the blue coral, Heliopora coerulea
title_full_unstemmed Warm seawater temperature promotes substrate colonization by the blue coral, Heliopora coerulea
title_short Warm seawater temperature promotes substrate colonization by the blue coral, Heliopora coerulea
title_sort warm seawater temperature promotes substrate colonization by the blue coral, heliopora coerulea
topic Computational Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6768060/
https://www.ncbi.nlm.nih.gov/pubmed/31579631
http://dx.doi.org/10.7717/peerj.7785
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