Abstract
Stress hormones and their impacts on whole organism metabolic rates are usually considered as appropriate proxies for animal energy budget that is the foundation of numerous concepts and models aiming at predicting individual and population responses to environmental stress. However, the dynamics of energy re-allocation under stress make the link between metabolism and corticosterone complex and still unclear. Using ectopic application of corticosterone for 3, 11 and 21 days, we estimated a time effect of stress in a lizard (Zootoca vivipara). We then investigated whole organism metabolism, muscle cellular O2 consumption and liver mitochondrial oxidative phosphorylation processes (O2 consumption and ATP production) and ROS production. The data showed that while skeletal muscle is not impacted, stress regulates the liver mitochondrial functionality in a time-dependent manner with opposing pictures between the different time expositions to corticosterone. While 3 days exposition is characterized by lower ATP synthesis rate and high H2O2 release with no change in the rate of oxygen consumption, the 11 days exposition reduced all three fluxes of about 50%. Oxidative phosphorylation capacities in liver mitochondria of lizard treated with corticosterone for 21 days was similar to the hepatic mitochondrial capacities in lizards that received no corticosterone treatment but with 40% decrease in H2O2 production. This new mitochondrial functioning allows a better capacity to respond to the energetic demands imposed by the environment but do not influence whole organism metabolism. In conclusion, global mitochondrial functioning has to be considered to better understand the proximal causes of the energy budget under stressful periods.
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The datasets generated during the current study are available from the corresponding author on reasonable request.
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Acknowledgements
We are thankful to field assistants and technical staff for their support, especially Beatriz Decencière, Simon Agostini, Victorien, Virginie and Amandine. We thank Olivier Lourdais for renting the respirometry equipment. We also thanks the three anonymous referees that help to improve the manuscript.
Funding
This study was funded by the Centre National de la Recherche Scientifique (CNRS), the Agence Nationale de la Recherche (ANR-13-JSV7-0011-01 to S.M.) and the Région Île-de-France R2DS program (grant 2013-08 to S.M., J.F.L.G. and R.J.). This work has also benefited from technical and human resources provided by CEREEP-Ecotron IleDeFrance (CNRS/ENS UMS 3194), which is supported by Regional Council of Ile-de-France under the DIM Program R2DS bearing the reference I-05-098/R and the program "Investissements d'Avenir" launched by the French government and implemented by ANR with the reference ANR-11-INBS-0001 AnaEE France.
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Conceptualization: YV, SM, DR, JFLG, CR; Methodology: DR, YV, SM, CR, JFLG; Validation: DR, YV; Formal analysis: DR, JFLG, AD, CR, YV; Investigation: DR, JFLG, SM, AD, CR, YV; Writing—original draft: YV, DR; Writing—review & editing: YV, SM, DR, JFLG, AD.
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The present investigation was carried out according to the ethical principles of the Préfecture de Seine-et-Marne under agreement A77-341-1.
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Voituron, Y., Roussel, D., Le Galliard, JF. et al. Mitochondrial oxidative phosphorylation response overrides glucocorticoid-induced stress in a reptile. J Comp Physiol B 192, 765–774 (2022). https://doi.org/10.1007/s00360-022-01454-5
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DOI: https://doi.org/10.1007/s00360-022-01454-5