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

Hichem A Menail; Simon B Cormier; Mariem Ben Youssef; Lisa Bjerregaard Jørgensen; Jess L Vickruck; Pier Morin Jr; Luc H Boudreau; Nicolas Pichaud

doi:10.3389/fphys.2022.897174

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

Front Physiol. 2022 Apr 25:13:897174. doi: 10.3389/fphys.2022.897174. eCollection 2022.

Authors

Hichem A Menail^{1

2}, Simon B Cormier^{1

2}, Mariem Ben Youssef², Lisa Bjerregaard Jørgensen³, Jess L Vickruck⁴, Pier Morin Jr², Luc H Boudreau^{1

2}, Nicolas Pichaud^{1

2}

Affiliations

¹ New Brunswick Centre for Precision Medicine, Moncton, NB, Canada.
² Department of Chemistry and Biochemistry, Université de Moncton, Moncton, NB, Canada.
³ Zoophysiology, Department of Biology, Aarhus University, Aarhus, Denmark.
⁴ Fredericton Research and Development Centre, Agriculture and Agri-Food Canada, Fredericton, NB, Canada.

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' mitochondria to temperature.

Keywords: Apis mellifera carnica; Drosophila melanogaster; Leptinotarsa decemlineata; glycerol-3-phosphate; metabolic adaptation; proline; succinate; temperature.