Epigenome-associated phenotypic acclimatization to ocean acidification in a reef-building coral

There are increasing concerns that the current rate of climate change might outpace the ability of reef-building corals to adapt to future conditions. Work on model systems has shown that environmentally induced alterations in DNA methylation can lead to phenotypic acclimatization. While DNA methyla...

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Published in:Science Advances
Main Authors: Liew, Yi Jin, Zoccola, Didier, Li, Yong, Tambutté, Eric, Venn, Alexander A., Michell, Craig, Cui, Guoxin, Deutekom, Eva S., Kaandorp, Jaap A., Voolstra, Christian R., Forêt, Sylvain, Allemand, Denis, Tambutté, Sylvie, Aranda, Manuel
Other Authors: Red Sea Research Center (RSRC), Biological and Environmental Sciences and Engineering (BESE) Division, Bioscience Program, Marine Science Program, Centre Scientifique de Monaco, Department of Marine Biology, , Monaco, Department of Environmental and Biological Sciences, University of Eastern Finland, Joensuu, , Finland, Computational Science Lab, Faculty of Science, University of Amsterdam, Amsterdam, , Netherlands, Research School of Biology, Australian National University, Canberra, ACT, , Australia
Format: Article in Journal/Newspaper
Language:unknown
Published: American Association for the Advancement of Science (AAAS) 2018
Subjects:
Online Access:http://hdl.handle.net/10754/625479
https://doi.org/10.1126/sciadv.aar8028
https://doi.org/10.1101/188227
id ftkingabdullahun:oai:repository.kaust.edu.sa:10754/625479
record_format openpolar
institution Open Polar
collection King Abdullah University of Science and Technology: KAUST Repository
op_collection_id ftkingabdullahun
language unknown
topic Epigenetics
DNA methylation
coral reef
cnidarian
ocean acidification
spellingShingle Epigenetics
DNA methylation
coral reef
cnidarian
ocean acidification
Liew, Yi Jin
Zoccola, Didier
Li, Yong
Tambutté, Eric
Venn, Alexander A.
Michell, Craig
Cui, Guoxin
Deutekom, Eva S.
Kaandorp, Jaap A.
Voolstra, Christian R.
Forêt, Sylvain
Allemand, Denis
Tambutté, Sylvie
Aranda, Manuel
Epigenome-associated phenotypic acclimatization to ocean acidification in a reef-building coral
topic_facet Epigenetics
DNA methylation
coral reef
cnidarian
ocean acidification
description There are increasing concerns that the current rate of climate change might outpace the ability of reef-building corals to adapt to future conditions. Work on model systems has shown that environmentally induced alterations in DNA methylation can lead to phenotypic acclimatization. While DNA methylation has been reported in corals and is thought to associate with phenotypic plasticity, potential mechanisms linked to changes in whole-genome methylation have yet to be elucidated. We show that DNA methylation significantly reduces spurious transcription in the coral Stylophora pistillata. Furthermore, we find that DNA methylation also reduces transcriptional noise by fine-tuning the expression of highly expressed genes. Analysis of DNA methylation patterns of corals subjected to long-term pH stress showed widespread changes in pathways regulating cell cycle and body size. Correspondingly, we found significant increases in cell and polyp sizes that resulted in more porous skeletons, supporting the hypothesis that linear extension rates are maintained under conditions of reduced calcification. These findings suggest an epigenetic component in phenotypic acclimatization that provides corals with an additional mechanism to cope with environmental change. We thank D. Desgre, N. Caminiti-Segonds, and N. Techer for assistance in coral husbandry; the King Abdullah University of Science and Technology (KAUST) Sequencing Core Facility for the sequencing of the libraries; N. Techer for cell size measurements; P. Alemanno and C. Sattonnet (Polyclinique Saint Jean, Cagnes-sur-Mer, France) for access to the micro-CT; and M. V. Matz and two anonymous reviewers for valuable feedback on our preprint and manuscript. This publication is based on work supported by the KAUST Office of Sponsored Research under award no. FCC/1/1973-22-01. Part of this study was conducted as part of the Centre Scientifique de Monaco Research Program, which is supported by the Government of the Principality of Monaco.
author2 Red Sea Research Center (RSRC)
Biological and Environmental Sciences and Engineering (BESE) Division
Bioscience Program
Marine Science Program
Centre Scientifique de Monaco, Department of Marine Biology, , Monaco
Department of Environmental and Biological Sciences, University of Eastern Finland, Joensuu, , Finland
Computational Science Lab, Faculty of Science, University of Amsterdam, Amsterdam, , Netherlands
Research School of Biology, Australian National University, Canberra, ACT, , Australia
format Article in Journal/Newspaper
author Liew, Yi Jin
Zoccola, Didier
Li, Yong
Tambutté, Eric
Venn, Alexander A.
Michell, Craig
Cui, Guoxin
Deutekom, Eva S.
Kaandorp, Jaap A.
Voolstra, Christian R.
Forêt, Sylvain
Allemand, Denis
Tambutté, Sylvie
Aranda, Manuel
author_facet Liew, Yi Jin
Zoccola, Didier
Li, Yong
Tambutté, Eric
Venn, Alexander A.
Michell, Craig
Cui, Guoxin
Deutekom, Eva S.
Kaandorp, Jaap A.
Voolstra, Christian R.
Forêt, Sylvain
Allemand, Denis
Tambutté, Sylvie
Aranda, Manuel
author_sort Liew, Yi Jin
title Epigenome-associated phenotypic acclimatization to ocean acidification in a reef-building coral
title_short Epigenome-associated phenotypic acclimatization to ocean acidification in a reef-building coral
title_full Epigenome-associated phenotypic acclimatization to ocean acidification in a reef-building coral
title_fullStr Epigenome-associated phenotypic acclimatization to ocean acidification in a reef-building coral
title_full_unstemmed Epigenome-associated phenotypic acclimatization to ocean acidification in a reef-building coral
title_sort epigenome-associated phenotypic acclimatization to ocean acidification in a reef-building coral
publisher American Association for the Advancement of Science (AAAS)
publishDate 2018
url http://hdl.handle.net/10754/625479
https://doi.org/10.1126/sciadv.aar8028
https://doi.org/10.1101/188227
genre Ocean acidification
genre_facet Ocean acidification
op_relation bioproject:PRJNA386774
http://advances.sciencemag.org/content/4/6/eaar8028
Liew YJ, Zoccola D, Li Y, Tambutté E, Venn AA, et al. (2018) Epigenome-associated phenotypic acclimatization to ocean acidification in a reef-building coral. Science Advances 4: eaar8028. Available: http://dx.doi.org/10.1126/sciadv.aar8028.
doi:10.1126/sciadv.aar8028
doi:10.1101/188227
2375-2548
Science Advances
http://hdl.handle.net/10754/625479
op_rights This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial license, which permits use, distribution, and reproduction in any medium, so long as the resultant use is not for commercial advantage and provided the original work is properly cited.
http://creativecommons.org/licenses/by-nc/4.0/
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container_title Science Advances
container_volume 4
container_issue 6
container_start_page eaar8028
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spelling ftkingabdullahun:oai:repository.kaust.edu.sa:10754/625479 2023-12-31T10:21:34+01:00 Epigenome-associated phenotypic acclimatization to ocean acidification in a reef-building coral Liew, Yi Jin Zoccola, Didier Li, Yong Tambutté, Eric Venn, Alexander A. Michell, Craig Cui, Guoxin Deutekom, Eva S. Kaandorp, Jaap A. Voolstra, Christian R. Forêt, Sylvain Allemand, Denis Tambutté, Sylvie Aranda, Manuel Red Sea Research Center (RSRC) Biological and Environmental Sciences and Engineering (BESE) Division Bioscience Program Marine Science Program Centre Scientifique de Monaco, Department of Marine Biology, , Monaco Department of Environmental and Biological Sciences, University of Eastern Finland, Joensuu, , Finland Computational Science Lab, Faculty of Science, University of Amsterdam, Amsterdam, , Netherlands Research School of Biology, Australian National University, Canberra, ACT, , Australia 2018-11-25T07:31:37Z application/pdf application/vnd.openxmlformats-officedocument.spreadsheetml.sheet http://hdl.handle.net/10754/625479 https://doi.org/10.1126/sciadv.aar8028 https://doi.org/10.1101/188227 unknown American Association for the Advancement of Science (AAAS) bioproject:PRJNA386774 http://advances.sciencemag.org/content/4/6/eaar8028 Liew YJ, Zoccola D, Li Y, Tambutté E, Venn AA, et al. (2018) Epigenome-associated phenotypic acclimatization to ocean acidification in a reef-building coral. Science Advances 4: eaar8028. Available: http://dx.doi.org/10.1126/sciadv.aar8028. doi:10.1126/sciadv.aar8028 doi:10.1101/188227 2375-2548 Science Advances http://hdl.handle.net/10754/625479 This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial license, which permits use, distribution, and reproduction in any medium, so long as the resultant use is not for commercial advantage and provided the original work is properly cited. http://creativecommons.org/licenses/by-nc/4.0/ Epigenetics DNA methylation coral reef cnidarian ocean acidification Article 2018 ftkingabdullahun https://doi.org/10.1126/sciadv.aar802810.1101/188227 2023-12-02T20:18:31Z There are increasing concerns that the current rate of climate change might outpace the ability of reef-building corals to adapt to future conditions. Work on model systems has shown that environmentally induced alterations in DNA methylation can lead to phenotypic acclimatization. While DNA methylation has been reported in corals and is thought to associate with phenotypic plasticity, potential mechanisms linked to changes in whole-genome methylation have yet to be elucidated. We show that DNA methylation significantly reduces spurious transcription in the coral Stylophora pistillata. Furthermore, we find that DNA methylation also reduces transcriptional noise by fine-tuning the expression of highly expressed genes. Analysis of DNA methylation patterns of corals subjected to long-term pH stress showed widespread changes in pathways regulating cell cycle and body size. Correspondingly, we found significant increases in cell and polyp sizes that resulted in more porous skeletons, supporting the hypothesis that linear extension rates are maintained under conditions of reduced calcification. These findings suggest an epigenetic component in phenotypic acclimatization that provides corals with an additional mechanism to cope with environmental change. We thank D. Desgre, N. Caminiti-Segonds, and N. Techer for assistance in coral husbandry; the King Abdullah University of Science and Technology (KAUST) Sequencing Core Facility for the sequencing of the libraries; N. Techer for cell size measurements; P. Alemanno and C. Sattonnet (Polyclinique Saint Jean, Cagnes-sur-Mer, France) for access to the micro-CT; and M. V. Matz and two anonymous reviewers for valuable feedback on our preprint and manuscript. This publication is based on work supported by the KAUST Office of Sponsored Research under award no. FCC/1/1973-22-01. Part of this study was conducted as part of the Centre Scientifique de Monaco Research Program, which is supported by the Government of the Principality of Monaco. Article in Journal/Newspaper Ocean acidification King Abdullah University of Science and Technology: KAUST Repository Science Advances 4 6 eaar8028