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

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Flexible Thermal Sensitivity of Mitochondrial Oxygen Consumption and Substrate Oxidation in Flying Insect Species. / Menail, Hichem A.; Cormier, Simon B.; Ben Youssef, Mariem et al.

In: Frontiers in Physiology, Vol. 13, 897174, 25.04.2022.

Research output: Contribution to journal/Conference contribution in journal/Contribution to newspaperJournal articleResearchpeer-review

Harvard

Menail, HA, Cormier, SB, Ben Youssef, M, Jørgensen, LB, Vickruck, JL, Morin, P, Boudreau, LH & Pichaud, N 2022, 'Flexible Thermal Sensitivity of Mitochondrial Oxygen Consumption and Substrate Oxidation in Flying Insect Species', Frontiers in Physiology, vol. 13, 897174. https://doi.org/10.3389/fphys.2022.897174

APA

Menail, H. A., Cormier, S. B., Ben Youssef, M., Jørgensen, L. B., Vickruck, J. L., Morin, P., Boudreau, L. H., & Pichaud, N. (2022). Flexible Thermal Sensitivity of Mitochondrial Oxygen Consumption and Substrate Oxidation in Flying Insect Species. Frontiers in Physiology, 13, [897174]. https://doi.org/10.3389/fphys.2022.897174

CBE

Menail HA, Cormier SB, Ben Youssef M, Jørgensen LB, Vickruck JL, Morin P, Boudreau LH, Pichaud N. 2022. Flexible Thermal Sensitivity of Mitochondrial Oxygen Consumption and Substrate Oxidation in Flying Insect Species. Frontiers in Physiology. 13:Article 897174. https://doi.org/10.3389/fphys.2022.897174

MLA

Vancouver

Menail HA, Cormier SB, Ben Youssef M, Jørgensen LB, Vickruck JL, Morin P et al. Flexible Thermal Sensitivity of Mitochondrial Oxygen Consumption and Substrate Oxidation in Flying Insect Species. Frontiers in Physiology. 2022 Apr 25;13:897174. doi: 10.3389/fphys.2022.897174

Author

Menail, Hichem A. ; Cormier, Simon B. ; Ben Youssef, Mariem et al. / Flexible Thermal Sensitivity of Mitochondrial Oxygen Consumption and Substrate Oxidation in Flying Insect Species. In: Frontiers in Physiology. 2022 ; Vol. 13.

Bibtex

@article{673bfbad06aa42eb81fd1152702f9a49,
title = "Flexible Thermal Sensitivity of Mitochondrial Oxygen Consumption and Substrate Oxidation in Flying Insect Species",
abstract = "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{\textquoteright} mitochondria to temperature.",
keywords = "Apis mellifera carnica, Drosophila melanogaster, glycerol-3-phosphate, Leptinotarsa decemlineata, metabolic adaptation, proline, succinate, temperature",
author = "Menail, {Hichem A.} and Cormier, {Simon B.} and {Ben Youssef}, Mariem and J{\o}rgensen, {Lisa Bjerregaard} and Vickruck, {Jess L.} and Pier Morin and Boudreau, {Luc H.} and Nicolas Pichaud",
note = "Publisher Copyright: Copyright {\textcopyright} 2022 Menail, Cormier, Ben Youssef, J{\o}rgensen, Vickruck, Morin, Boudreau and Pichaud.",
year = "2022",
month = apr,
day = "25",
doi = "10.3389/fphys.2022.897174",
language = "English",
volume = "13",
journal = "Frontiers in Physiology",
issn = "1664-042X",
publisher = "Frontiers Media S.A",

}

RIS

TY - JOUR

T1 - Flexible Thermal Sensitivity of Mitochondrial Oxygen Consumption and Substrate Oxidation in Flying Insect Species

AU - Menail, Hichem A.

AU - Cormier, Simon B.

AU - Ben Youssef, Mariem

AU - Jørgensen, Lisa Bjerregaard

AU - Vickruck, Jess L.

AU - Morin, Pier

AU - Boudreau, Luc H.

AU - Pichaud, Nicolas

N1 - Publisher Copyright: Copyright © 2022 Menail, Cormier, Ben Youssef, Jørgensen, Vickruck, Morin, Boudreau and Pichaud.

PY - 2022/4/25

Y1 - 2022/4/25

N2 - 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.

AB - 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.

KW - Apis mellifera carnica

KW - Drosophila melanogaster

KW - glycerol-3-phosphate

KW - Leptinotarsa decemlineata

KW - metabolic adaptation

KW - proline

KW - succinate

KW - temperature

UR - http://www.scopus.com/inward/record.url?scp=85129837308&partnerID=8YFLogxK

U2 - 10.3389/fphys.2022.897174

DO - 10.3389/fphys.2022.897174

M3 - Journal article

C2 - 35547573

AN - SCOPUS:85129837308

VL - 13

JO - Frontiers in Physiology

JF - Frontiers in Physiology

SN - 1664-042X

M1 - 897174

ER -