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A multi-trait systems approach reveals a response cascade to bleaching in corals

BACKGROUND: Climate change causes the breakdown of the symbiotic relationships between reef-building corals and their photosynthetic symbionts (genus Symbiodinium), with thermal anomalies in 2015–2016 triggering the most widespread mass coral bleaching on record and unprecedented mortality on the Gr...

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Autores principales: Gardner, Stephanie G., Raina, Jean-Baptiste, Nitschke, Matthew R., Nielsen, Daniel A., Stat, Michael, Motti, Cherie A., Ralph, Peter J., Petrou, Katherina
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5719617/
https://www.ncbi.nlm.nih.gov/pubmed/29216891
http://dx.doi.org/10.1186/s12915-017-0459-2
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author Gardner, Stephanie G.
Raina, Jean-Baptiste
Nitschke, Matthew R.
Nielsen, Daniel A.
Stat, Michael
Motti, Cherie A.
Ralph, Peter J.
Petrou, Katherina
author_facet Gardner, Stephanie G.
Raina, Jean-Baptiste
Nitschke, Matthew R.
Nielsen, Daniel A.
Stat, Michael
Motti, Cherie A.
Ralph, Peter J.
Petrou, Katherina
author_sort Gardner, Stephanie G.
collection PubMed
description BACKGROUND: Climate change causes the breakdown of the symbiotic relationships between reef-building corals and their photosynthetic symbionts (genus Symbiodinium), with thermal anomalies in 2015–2016 triggering the most widespread mass coral bleaching on record and unprecedented mortality on the Great Barrier Reef. Targeted studies using specific coral stress indicators have highlighted the complexity of the physiological processes occurring during thermal stress, but have been unable to provide a clear mechanistic understanding of coral bleaching. RESULTS: Here, we present an extensive multi-trait-based study in which we compare the thermal stress responses of two phylogenetically distinct and widely distributed coral species, Acropora millepora and Stylophora pistillata, integrating 14 individual stress indicators over time across a simulated thermal anomaly. We found that key stress responses were conserved across both taxa, with the loss of symbionts and the activation of antioxidant mechanisms occurring well before collapse of the physiological parameters, including gross oxygen production and chlorophyll a. Our study also revealed species-specific traits, including differences in the timing of antioxidant regulation, as well as drastic differences in the production of the sulfur compound dimethylsulfoniopropionate during bleaching. Indeed, the concentration of this antioxidant increased two-fold in A. millepora after the corals started to bleach, while it decreased 70% in S. pistillata. CONCLUSIONS: We identify a well-defined cascading response to thermal stress, demarking clear pathophysiological reactions conserved across the two species, which might be central to fully understanding the mechanisms triggering thermally induced coral bleaching. These results highlight that bleaching is a conserved mechanism, but specific adaptations linked to the coral’s antioxidant capacity drive differences in the sensitivity and thus tolerance of each coral species to thermal stress. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12915-017-0459-2) contains supplementary material, which is available to authorized users.
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spelling pubmed-57196172017-12-08 A multi-trait systems approach reveals a response cascade to bleaching in corals Gardner, Stephanie G. Raina, Jean-Baptiste Nitschke, Matthew R. Nielsen, Daniel A. Stat, Michael Motti, Cherie A. Ralph, Peter J. Petrou, Katherina BMC Biol Research Article BACKGROUND: Climate change causes the breakdown of the symbiotic relationships between reef-building corals and their photosynthetic symbionts (genus Symbiodinium), with thermal anomalies in 2015–2016 triggering the most widespread mass coral bleaching on record and unprecedented mortality on the Great Barrier Reef. Targeted studies using specific coral stress indicators have highlighted the complexity of the physiological processes occurring during thermal stress, but have been unable to provide a clear mechanistic understanding of coral bleaching. RESULTS: Here, we present an extensive multi-trait-based study in which we compare the thermal stress responses of two phylogenetically distinct and widely distributed coral species, Acropora millepora and Stylophora pistillata, integrating 14 individual stress indicators over time across a simulated thermal anomaly. We found that key stress responses were conserved across both taxa, with the loss of symbionts and the activation of antioxidant mechanisms occurring well before collapse of the physiological parameters, including gross oxygen production and chlorophyll a. Our study also revealed species-specific traits, including differences in the timing of antioxidant regulation, as well as drastic differences in the production of the sulfur compound dimethylsulfoniopropionate during bleaching. Indeed, the concentration of this antioxidant increased two-fold in A. millepora after the corals started to bleach, while it decreased 70% in S. pistillata. CONCLUSIONS: We identify a well-defined cascading response to thermal stress, demarking clear pathophysiological reactions conserved across the two species, which might be central to fully understanding the mechanisms triggering thermally induced coral bleaching. These results highlight that bleaching is a conserved mechanism, but specific adaptations linked to the coral’s antioxidant capacity drive differences in the sensitivity and thus tolerance of each coral species to thermal stress. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12915-017-0459-2) contains supplementary material, which is available to authorized users. BioMed Central 2017-12-07 /pmc/articles/PMC5719617/ /pubmed/29216891 http://dx.doi.org/10.1186/s12915-017-0459-2 Text en © Gardner et al. 2017 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Gardner, Stephanie G.
Raina, Jean-Baptiste
Nitschke, Matthew R.
Nielsen, Daniel A.
Stat, Michael
Motti, Cherie A.
Ralph, Peter J.
Petrou, Katherina
A multi-trait systems approach reveals a response cascade to bleaching in corals
title A multi-trait systems approach reveals a response cascade to bleaching in corals
title_full A multi-trait systems approach reveals a response cascade to bleaching in corals
title_fullStr A multi-trait systems approach reveals a response cascade to bleaching in corals
title_full_unstemmed A multi-trait systems approach reveals a response cascade to bleaching in corals
title_short A multi-trait systems approach reveals a response cascade to bleaching in corals
title_sort multi-trait systems approach reveals a response cascade to bleaching in corals
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5719617/
https://www.ncbi.nlm.nih.gov/pubmed/29216891
http://dx.doi.org/10.1186/s12915-017-0459-2
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