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Dynamic regulation of coral energy metabolism throughout the diel cycle

Coral reefs are naturally exposed to daily and seasonal variations in environmental oxygen levels, which can be exacerbated in intensity and duration by anthropogenic activities. However, coral’s diel oxygen dynamics and fermentative pathways remain poorly understood. Here, continuous oxygen microel...

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Autores principales: Linsmayer, Lauren Buckley, Deheyn, Dimitri Dominique, Tomanek, Lars, Tresguerres, Martin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7669893/
https://www.ncbi.nlm.nih.gov/pubmed/33199772
http://dx.doi.org/10.1038/s41598-020-76828-2
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author Linsmayer, Lauren Buckley
Deheyn, Dimitri Dominique
Tomanek, Lars
Tresguerres, Martin
author_facet Linsmayer, Lauren Buckley
Deheyn, Dimitri Dominique
Tomanek, Lars
Tresguerres, Martin
author_sort Linsmayer, Lauren Buckley
collection PubMed
description Coral reefs are naturally exposed to daily and seasonal variations in environmental oxygen levels, which can be exacerbated in intensity and duration by anthropogenic activities. However, coral’s diel oxygen dynamics and fermentative pathways remain poorly understood. Here, continuous oxygen microelectrode recordings in the coral diffusive boundary layer revealed hyperoxia during daytime and hypoxia at nighttime resulting from net photosynthesis and net respiration, respectively. The activities of the metabolic enzymes citrate synthase (CS), malate dehydrogenase, and strombine dehydrogenase remained constant throughout the day/night cycle, suggesting that energy metabolism was regulated through adjustments in metabolite fluxes and not through changes in enzyme abundance. Liquid chromatography-mass spectrometry analyses identified strombine as coral’s main fermentative end product. Strombine levels peaked as oxygen became depleted at dusk, indicating increased fermentation rates at the onset of nightly hypoxia, and again at dawn as photosynthesis restored oxygen and photosynthate supply. When these peaks were excluded from the analyses, average strombine levels during the day were nearly double those at night, indicating sifnificant fermentation rates even during aerobic conditions. These results highlight the dynamic changes in oxygen levels in the coral diffusive boundary layer, and the importance of fermentative metabolism for coral biology.
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spelling pubmed-76698932020-11-18 Dynamic regulation of coral energy metabolism throughout the diel cycle Linsmayer, Lauren Buckley Deheyn, Dimitri Dominique Tomanek, Lars Tresguerres, Martin Sci Rep Article Coral reefs are naturally exposed to daily and seasonal variations in environmental oxygen levels, which can be exacerbated in intensity and duration by anthropogenic activities. However, coral’s diel oxygen dynamics and fermentative pathways remain poorly understood. Here, continuous oxygen microelectrode recordings in the coral diffusive boundary layer revealed hyperoxia during daytime and hypoxia at nighttime resulting from net photosynthesis and net respiration, respectively. The activities of the metabolic enzymes citrate synthase (CS), malate dehydrogenase, and strombine dehydrogenase remained constant throughout the day/night cycle, suggesting that energy metabolism was regulated through adjustments in metabolite fluxes and not through changes in enzyme abundance. Liquid chromatography-mass spectrometry analyses identified strombine as coral’s main fermentative end product. Strombine levels peaked as oxygen became depleted at dusk, indicating increased fermentation rates at the onset of nightly hypoxia, and again at dawn as photosynthesis restored oxygen and photosynthate supply. When these peaks were excluded from the analyses, average strombine levels during the day were nearly double those at night, indicating sifnificant fermentation rates even during aerobic conditions. These results highlight the dynamic changes in oxygen levels in the coral diffusive boundary layer, and the importance of fermentative metabolism for coral biology. Nature Publishing Group UK 2020-11-16 /pmc/articles/PMC7669893/ /pubmed/33199772 http://dx.doi.org/10.1038/s41598-020-76828-2 Text en © The Author(s) 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Linsmayer, Lauren Buckley
Deheyn, Dimitri Dominique
Tomanek, Lars
Tresguerres, Martin
Dynamic regulation of coral energy metabolism throughout the diel cycle
title Dynamic regulation of coral energy metabolism throughout the diel cycle
title_full Dynamic regulation of coral energy metabolism throughout the diel cycle
title_fullStr Dynamic regulation of coral energy metabolism throughout the diel cycle
title_full_unstemmed Dynamic regulation of coral energy metabolism throughout the diel cycle
title_short Dynamic regulation of coral energy metabolism throughout the diel cycle
title_sort dynamic regulation of coral energy metabolism throughout the diel cycle
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7669893/
https://www.ncbi.nlm.nih.gov/pubmed/33199772
http://dx.doi.org/10.1038/s41598-020-76828-2
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