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Thermally tolerant intertidal triplefin fish (Tripterygiidae) sustain ATP dynamics better than subtidal species under acute heat stress

Temperature is a key factor that affects all levels of organization. Minute shifts away from thermal optima result in detrimental effects that impact growth, reproduction and survival. Metabolic rates of ectotherms are especially sensitive to temperature and for organisms exposed to high acute tempe...

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Autores principales: Willis, Jaime R., Hickey, Anthony J. R., Devaux, Jules B. L.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8155050/
https://www.ncbi.nlm.nih.gov/pubmed/34040122
http://dx.doi.org/10.1038/s41598-021-90575-y
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author Willis, Jaime R.
Hickey, Anthony J. R.
Devaux, Jules B. L.
author_facet Willis, Jaime R.
Hickey, Anthony J. R.
Devaux, Jules B. L.
author_sort Willis, Jaime R.
collection PubMed
description Temperature is a key factor that affects all levels of organization. Minute shifts away from thermal optima result in detrimental effects that impact growth, reproduction and survival. Metabolic rates of ectotherms are especially sensitive to temperature and for organisms exposed to high acute temperature changes, in particular intertidal species, energetic processes are often negatively impacted. Previous investigations exploring acute heat stress have implicated cardiac mitochondrial function in determining thermal tolerance. The brain, however, is by weight, one of the most metabolically active and arguably the most temperature sensitive organ. It is essentially aerobic and entirely reliant on oxidative phosphorylation to meet energetic demands, and as temperatures rise, mitochondria become less efficient at synthesising the amount of ATP required to meet the increasing demands. This leads to an energetic crisis. Here we used brain homogenate of three closely related triplefin fish species (Bellapiscis medius, Forsterygion lapillum, and Forsterygion varium) and measured respiration and ATP dynamics at three temperatures (15, 25 and 30 °C). We found that the intertidal B. medius and F. lapillum were able to maintain rates of ATP production above rates of ATP hydrolysis at high temperatures, compared to the subtidal F. varium, which showed no difference in rates at 30 °C. These results showed that brain mitochondria became less efficient at temperatures below their respective species thermal limits, and that energetic surplus of ATP synthesis over hydrolysis narrows. In subtidal species synthesis matches hydrolysis, leaving no scope to elevate ATP supply.
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spelling pubmed-81550502021-05-27 Thermally tolerant intertidal triplefin fish (Tripterygiidae) sustain ATP dynamics better than subtidal species under acute heat stress Willis, Jaime R. Hickey, Anthony J. R. Devaux, Jules B. L. Sci Rep Article Temperature is a key factor that affects all levels of organization. Minute shifts away from thermal optima result in detrimental effects that impact growth, reproduction and survival. Metabolic rates of ectotherms are especially sensitive to temperature and for organisms exposed to high acute temperature changes, in particular intertidal species, energetic processes are often negatively impacted. Previous investigations exploring acute heat stress have implicated cardiac mitochondrial function in determining thermal tolerance. The brain, however, is by weight, one of the most metabolically active and arguably the most temperature sensitive organ. It is essentially aerobic and entirely reliant on oxidative phosphorylation to meet energetic demands, and as temperatures rise, mitochondria become less efficient at synthesising the amount of ATP required to meet the increasing demands. This leads to an energetic crisis. Here we used brain homogenate of three closely related triplefin fish species (Bellapiscis medius, Forsterygion lapillum, and Forsterygion varium) and measured respiration and ATP dynamics at three temperatures (15, 25 and 30 °C). We found that the intertidal B. medius and F. lapillum were able to maintain rates of ATP production above rates of ATP hydrolysis at high temperatures, compared to the subtidal F. varium, which showed no difference in rates at 30 °C. These results showed that brain mitochondria became less efficient at temperatures below their respective species thermal limits, and that energetic surplus of ATP synthesis over hydrolysis narrows. In subtidal species synthesis matches hydrolysis, leaving no scope to elevate ATP supply. Nature Publishing Group UK 2021-05-26 /pmc/articles/PMC8155050/ /pubmed/34040122 http://dx.doi.org/10.1038/s41598-021-90575-y Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/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/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Willis, Jaime R.
Hickey, Anthony J. R.
Devaux, Jules B. L.
Thermally tolerant intertidal triplefin fish (Tripterygiidae) sustain ATP dynamics better than subtidal species under acute heat stress
title Thermally tolerant intertidal triplefin fish (Tripterygiidae) sustain ATP dynamics better than subtidal species under acute heat stress
title_full Thermally tolerant intertidal triplefin fish (Tripterygiidae) sustain ATP dynamics better than subtidal species under acute heat stress
title_fullStr Thermally tolerant intertidal triplefin fish (Tripterygiidae) sustain ATP dynamics better than subtidal species under acute heat stress
title_full_unstemmed Thermally tolerant intertidal triplefin fish (Tripterygiidae) sustain ATP dynamics better than subtidal species under acute heat stress
title_short Thermally tolerant intertidal triplefin fish (Tripterygiidae) sustain ATP dynamics better than subtidal species under acute heat stress
title_sort thermally tolerant intertidal triplefin fish (tripterygiidae) sustain atp dynamics better than subtidal species under acute heat stress
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8155050/
https://www.ncbi.nlm.nih.gov/pubmed/34040122
http://dx.doi.org/10.1038/s41598-021-90575-y
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