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’ mitochondria to temperature.

Coping with global warming: Adult thermal thresholds in four pestiferous Anastrepha species determined under experimental laboratory conditions and development/survival times of immatures and adults under natural field conditions

“…For example, transgenic flies with overexpression of HSP70 are more tolerant to higher temperatures but with the cost of reduced growth, survival, and egg hatch when compared to wild-type flies ( Krebs and Feder, 1997 ). More recently, Moloń et al (2020) documented an inverse relationship between metabolic rate and lifespan in the same fly species (also see Menail et al, 2022 ). In our case, A .…”

“…For example, transgenic flies with overexpression of HSP70 are more tolerant to higher temperatures but with the cost of reduced growth, survival, and egg hatch when compared to wild-type flies (Krebs and Feder, 1997). More recently, Moloń et al (2020) documented an inverse relationship between metabolic rate and lifespan in the same fly species (also see Menail et al, 2022). In our case, A. ludens females are known to invest significantly in costly ovary development and oogenesis (Aluja et al, 2001) which added to the activation to heat stress response mechanisms, may explain why they lived for shorter periods than males.…”

Balanced mitochondrial function at low temperature is linked to cold adaptation inDrosophilaspecies

“…CC-BY-ND 4.0 International license perpetuity. It is made available under a preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in The copyright holder for this this version posted December 22, 2022. ; https://doi.org/10.1101/2022.12.22.521616 doi: bioRxiv preprint alternative substrates at low temperature has also been found with additions of succinate and G3P in D. melanogaster and honeybees (Menail et al, 2022), or with addition of succinate in warm-acclimated mayfly larvae (Havird et al, 2020) and a planarian (Scott et al, 2019). Thus, when considering Q10 for maximal OCR coupled to phosphorylation (after G3P injection) between 10 and 1°C we found more similar thermal sensitivities (Q10 for the four most sensitive species = 3.2 and Q10 for the three most tolerant species = 2.6) (Fig.…”

“…The critical thermal minima (CT min ) is seemingly unaffected by oxygen availability at low temperature (Boardman et al, 2016; Stevens et al, 2010) and cold exposure, even below CT min , is usually not associated with a decrease in total ATP concentration (Colinet, 2011; Koštál et al, 2004; MacMillan et al, 2012; Williams et al, 2018). Nevertheless, it has been discussed whether mitochondrial capacity including the electron transport system (ETS) and associated oxidative phosphorylation is compromised/modified by low temperature in insects (Colinet et al, 2017; Lubawy et al, 2022; Menail et al, 2022; Wood and Nordin, 1980).…”

“…Similar tendencies were reported for cold-acclimated mayfly larvae that retained relatively higher respiration capacity and mitochondrial coupling (RCR) at low temperature compared to their warm-acclimated conspecifics (Havird et al, 2020). Cold-induced changes in insect mitochondrial capacity and coupling could also be associated with unbalanced temperature effects on different complexes in the electron transport system (Havird et al, 2020; Menail et al, 2022). For example, Menail et al (2022) observed significant decreases in oxygen consumption rate (OCR) of complex I (CI-OXPHOS) in D. melanogaster and honeybees at low temperature (6-12 °C) compared to OCRs at a benign temperature (18 °C).…”