Cold adaptation does not alter ATP homeostasis during cold exposure in Drosophila melanogaster

Abstract

In insects and other ectotherms, cold temperatures cause a coma resulting from loss of neuromuscular function, during which ionic and metabolic homeostasis are progressively lost. Cold adaptation improves homeostasis during cold exposure, but the ultimate targets of selection are still an open question. Cold acclimation and adaptation remodels mitochondrial metabolism in insects, suggesting that aerobic energy production during cold exposure could be a target of selection. Here, we test the hypothesis that cold adaptation improves the ability to maintain rates of aerobic energy production during cold exposure by using P NMR on live flies. Using lines of Drosophila melanogaster artificially selected for fast and slow recovery from a cold coma, we show that cold exposure does not lower ATP levels and that cold adaptation does not alter aerobic ATP production during cold exposure. Cold-hardy and cold-susceptible lines both experienced a brief transition to anaerobic metabolism during cooling, but this was rapidly reversed during cold exposure, suggesting that oxidative phosphorylation was sufficient to meet energy demands below the critical thermal minimum, even in cold-susceptible flies. We thus reject the hypothesis that performance under mild low temperatures is set by aerobic ATP supply limitations in D. melanogaster, excluding oxygen and capacity limitation as a weak link in energy supply. This work suggests that the modulations to mitochondrial metabolism resulting from cold acclimation or adaptation may arise from selection on a biosynthetic product(s) of those pathways rather than selection on ATP supply during cold exposure. This article is protected by copyright. All rights reserved.

Sestrin regulates acute chill coma recovery in Drosophila melanogaster

“…Both acute and chronic exposure to low temperatures can influence energy metabolism ( Williams et al, 2014 ). Cold-resistant flies have greater metabolic plasticity and have elevated levels of metabolic intermediates during acute cold stress despite no changes in ATP concentration ( MacMillan et al, 2016 ; Williams et al, 2016 , 2018 ). It has been proposed that this is due to increased metabolic turnover to support the energetic demands of cryoprotectant biosynthesis or cellular repair ( Williams et al, 2018 ).…”

“…Cold-resistant flies have greater metabolic plasticity and have elevated levels of metabolic intermediates during acute cold stress despite no changes in ATP concentration ( MacMillan et al, 2016 ; Williams et al, 2016 , 2018 ). It has been proposed that this is due to increased metabolic turnover to support the energetic demands of cryoprotectant biosynthesis or cellular repair ( Williams et al, 2018 ). If this is the case, Sestrin may be an important regulator of energy metabolism by signaling through AMPK and Spargel to stimulate substrate uptake, TCA flux, and substrate oxidation during cold stress ( Supruniuk et al, 2017 ).…”

“…The speed by which an individual fly resumes active transport and other energetically demanding processes during chill coma recovery may depend on ATP availability/production. However, recent work has shown no difference in ATP availability during acute cold exposure between cold-resistant and cold-susceptible flies, suggesting that ATP reduction may not be a determining factor in recovery ( MacMillan and Sinclair, 2011 ; Williams et al, 2018 ).…”

“…It has been proposed that higher tricarboxylic acid (TCA) cycle flux and substrate oxidation may be important in the synthesis of metabolic intermediates that have cryoprotective functions or are involved in cellular repair of damage incurred from cold stress (e.g. membrane repair) ( Williams et al, 2016 , 2018 ). Several metabolomics studies have found higher concentrations of metabolic intermediates in cold-resistant flies after acute cold exposure, indicating altered metabolism ( Enriquez et al, 2018 ; MacMillan et al, 2016 ; Williams et al, 2014 ).…”

Biological buffers and the impacts of climate change

“…The interplay of ecological and evolutionary dynamics is directly relevant to the impact of evolutionary buffering, but these dynamics are still inadequately studied. Williams et al (2018) provide an exemplar exploration of the physiological mechanisms and costs of genetic adaptation to low body temperatures. At issue is whether oxygen limitation affects energy supplies (Pörtner et al 2017(Pörtner et al , 2018Jutfelt et al 2018).…”