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Flexible Thermal Sensitivity of Mitochondrial Oxygen Consumption and Substrate Oxidation in Flying Insect Species

Mitochondria have been suggested to be paramount for temperature adaptation in insects. Considering the large range of environments colonized by this taxon, we hypothesized that species surviving large temperature changes would be those with the most flexible mitochondria. We thus investigated the r...

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Autores principales: Menail, Hichem A., Cormier, Simon B., Ben Youssef, Mariem, Jørgensen, Lisa Bjerregaard, Vickruck, Jess L., Morin, Pier, Boudreau, Luc H., Pichaud, Nicolas
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9081799/
https://www.ncbi.nlm.nih.gov/pubmed/35547573
http://dx.doi.org/10.3389/fphys.2022.897174
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author Menail, Hichem A.
Cormier, Simon B.
Ben Youssef, Mariem
Jørgensen, Lisa Bjerregaard
Vickruck, Jess L.
Morin, Pier
Boudreau, Luc H.
Pichaud, Nicolas
author_facet Menail, Hichem A.
Cormier, Simon B.
Ben Youssef, Mariem
Jørgensen, Lisa Bjerregaard
Vickruck, Jess L.
Morin, Pier
Boudreau, Luc H.
Pichaud, Nicolas
author_sort Menail, Hichem A.
collection PubMed
description Mitochondria have been suggested to be paramount for temperature adaptation in insects. Considering the large range of environments colonized by this taxon, we hypothesized that species surviving large temperature changes would be those with the most flexible mitochondria. We thus investigated the responses of mitochondrial oxidative phosphorylation (OXPHOS) to temperature in three flying insects: the honeybee (Apis mellifera carnica), the fruit fly (Drosophila melanogaster) and the Colorado potato beetle (Leptinotarsa decemlineata). Specifically, we measured oxygen consumption in permeabilized flight muscles of these species at 6, 12, 18, 24, 30, 36, 42 and 45°C, sequentially using complex I substrates, proline, succinate, and glycerol-3-phosphate (G3P). Complex I respiration rates (CI-OXPHOS) were very sensitive to temperature in honeybees and fruit flies with high oxygen consumption at mid-range temperatures but a sharp decline at high temperatures. Proline oxidation triggers a major increase in respiration only in potato beetles, following the same pattern as CI-OXPHOS for honeybees and fruit flies. Moreover, both succinate and G3P oxidation allowed an important increase in respiration at high temperatures in honeybees and fruit flies (and to a lesser extent in potato beetles). However, when reaching 45°C, this G3P-induced respiration rate dropped dramatically in fruit flies. These results demonstrate that mitochondrial functions are more resilient to high temperatures in honeybees compared to fruit flies. They also indicate an important but species-specific mitochondrial flexibility for substrate oxidation to sustain high oxygen consumption levels at high temperatures and suggest previously unknown adaptive mechanisms of flying insects’ mitochondria to temperature.
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spelling pubmed-90817992022-05-10 Flexible Thermal Sensitivity of Mitochondrial Oxygen Consumption and Substrate Oxidation in Flying Insect Species Menail, Hichem A. Cormier, Simon B. Ben Youssef, Mariem Jørgensen, Lisa Bjerregaard Vickruck, Jess L. Morin, Pier Boudreau, Luc H. Pichaud, Nicolas Front Physiol Physiology Mitochondria have been suggested to be paramount for temperature adaptation in insects. Considering the large range of environments colonized by this taxon, we hypothesized that species surviving large temperature changes would be those with the most flexible mitochondria. We thus investigated the responses of mitochondrial oxidative phosphorylation (OXPHOS) to temperature in three flying insects: the honeybee (Apis mellifera carnica), the fruit fly (Drosophila melanogaster) and the Colorado potato beetle (Leptinotarsa decemlineata). Specifically, we measured oxygen consumption in permeabilized flight muscles of these species at 6, 12, 18, 24, 30, 36, 42 and 45°C, sequentially using complex I substrates, proline, succinate, and glycerol-3-phosphate (G3P). Complex I respiration rates (CI-OXPHOS) were very sensitive to temperature in honeybees and fruit flies with high oxygen consumption at mid-range temperatures but a sharp decline at high temperatures. Proline oxidation triggers a major increase in respiration only in potato beetles, following the same pattern as CI-OXPHOS for honeybees and fruit flies. Moreover, both succinate and G3P oxidation allowed an important increase in respiration at high temperatures in honeybees and fruit flies (and to a lesser extent in potato beetles). However, when reaching 45°C, this G3P-induced respiration rate dropped dramatically in fruit flies. These results demonstrate that mitochondrial functions are more resilient to high temperatures in honeybees compared to fruit flies. They also indicate an important but species-specific mitochondrial flexibility for substrate oxidation to sustain high oxygen consumption levels at high temperatures and suggest previously unknown adaptive mechanisms of flying insects’ mitochondria to temperature. Frontiers Media S.A. 2022-04-25 /pmc/articles/PMC9081799/ /pubmed/35547573 http://dx.doi.org/10.3389/fphys.2022.897174 Text en Copyright © 2022 Menail, Cormier, Ben Youssef, Jørgensen, Vickruck, Morin, Boudreau and Pichaud. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Physiology
Menail, Hichem A.
Cormier, Simon B.
Ben Youssef, Mariem
Jørgensen, Lisa Bjerregaard
Vickruck, Jess L.
Morin, Pier
Boudreau, Luc H.
Pichaud, Nicolas
Flexible Thermal Sensitivity of Mitochondrial Oxygen Consumption and Substrate Oxidation in Flying Insect Species
title Flexible Thermal Sensitivity of Mitochondrial Oxygen Consumption and Substrate Oxidation in Flying Insect Species
title_full Flexible Thermal Sensitivity of Mitochondrial Oxygen Consumption and Substrate Oxidation in Flying Insect Species
title_fullStr Flexible Thermal Sensitivity of Mitochondrial Oxygen Consumption and Substrate Oxidation in Flying Insect Species
title_full_unstemmed Flexible Thermal Sensitivity of Mitochondrial Oxygen Consumption and Substrate Oxidation in Flying Insect Species
title_short Flexible Thermal Sensitivity of Mitochondrial Oxygen Consumption and Substrate Oxidation in Flying Insect Species
title_sort flexible thermal sensitivity of mitochondrial oxygen consumption and substrate oxidation in flying insect species
topic Physiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9081799/
https://www.ncbi.nlm.nih.gov/pubmed/35547573
http://dx.doi.org/10.3389/fphys.2022.897174
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