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

Abstract 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 ac...

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Autores principales: Jaime R. Willis, Anthony J. R. Hickey, Jules B. L. Devaux
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Publicado: Nature Portfolio 2021
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Acceso en línea:https://doaj.org/article/5e37441785ec4cc7af6aba19227ba2ad
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spelling oai:doaj.org-article:5e37441785ec4cc7af6aba19227ba2ad2021-12-02T16:53:01ZThermally tolerant intertidal triplefin fish (Tripterygiidae) sustain ATP dynamics better than subtidal species under acute heat stress10.1038/s41598-021-90575-y2045-2322https://doaj.org/article/5e37441785ec4cc7af6aba19227ba2ad2021-05-01T00:00:00Zhttps://doi.org/10.1038/s41598-021-90575-yhttps://doaj.org/toc/2045-2322Abstract 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.Jaime R. WillisAnthony J. R. HickeyJules B. L. DevauxNature PortfolioarticleMedicineRScienceQENScientific Reports, Vol 11, Iss 1, Pp 1-10 (2021)
institution DOAJ
collection DOAJ
language EN
topic Medicine
R
Science
Q
spellingShingle Medicine
R
Science
Q
Jaime R. Willis
Anthony J. R. Hickey
Jules B. L. Devaux
Thermally tolerant intertidal triplefin fish (Tripterygiidae) sustain ATP dynamics better than subtidal species under acute heat stress
description Abstract 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.
format article
author Jaime R. Willis
Anthony J. R. Hickey
Jules B. L. Devaux
author_facet Jaime R. Willis
Anthony J. R. Hickey
Jules B. L. Devaux
author_sort Jaime R. Willis
title 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_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_sort thermally tolerant intertidal triplefin fish (tripterygiidae) sustain atp dynamics better than subtidal species under acute heat stress
publisher Nature Portfolio
publishDate 2021
url https://doaj.org/article/5e37441785ec4cc7af6aba19227ba2ad
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AT anthonyjrhickey thermallytolerantintertidaltriplefinfishtripterygiidaesustainatpdynamicsbetterthansubtidalspeciesunderacuteheatstress
AT julesbldevaux thermallytolerantintertidaltriplefinfishtripterygiidaesustainatpdynamicsbetterthansubtidalspeciesunderacuteheatstress
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