Oxidative phosphorylation efficiency, proton conductance and reactive oxygen species production of liver mitochondria correlates with body mass in frogs

Author:

Roussel Damien1,Salin Karine12,Dumet Adeline1,Romestaing Caroline1,Rey Benjamin34,Voituron Yann1

Affiliation:

1. Laboratoire d'Ecologie des Hydrosystèmes Naturels et Anthropisés, UMR 5023, CNRS, Université de Lyon 1, Lyon, France

2. Institute of Biodiversity, Animal Health and Comparative Medicine, University of Glasgow, Glasgow, Scotland

3. Laboratoire de Biométrie et Biologie Évolutive, UMR 5558, CNRS, Université de Lyon 1, Lyon, France

4. Brain Function Research Group, School of Physiology, Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa

Abstract

Body size is a central biological parameter affecting most biological processes (especially energetics) and mitochondria is a key organelle controlling metabolism and is also the cell's main source of chemical energy. However, the link between body size and mitochondrial function is still unclear, especially in ectotherms. In this study, we investigated several parameters of mitochondrial bioenergetics in the liver of three closely related species of frogs (the common frog Rana temporaria, the marsh frog Pelophylax ridibundus and the bull frog Lithobates catesbeiana). These particular species were chosen due to their differences in adult body mass. We found that the mitochondrial coupling efficiency was markedly increased with animal size, which lead to a higher ATP production (+70%) in the larger frogs (L. catesbeiana) compared to the smaller frogs (R. temporaria). This was essentially driven by a strong negative dependence of mitochondrial proton conductance on body mass. Liver mitochondria from the larger frogs (L. catesbeiana) displayed 50% of the proton conductance of mitochondria from the smaller frogs (R. temporaria). Contrary to our prediction, the low mitochondrial proton conductance measured in L. catesbeiana was not associated with higher radical oxygen species production. Instead, liver mitochondria from the larger individuals produced significantly lower radical oxygen species than those from the smaller frogs. Collectively, the data shows that key bioenergetics parameters of mitochondria (proton leak, ATP production efficiency and radical oxygen species production) are correlated with body mass in frogs. This research expands our understanding of the relationship between mitochondrial function and the evolution of allometric scaling in ectotherms.

Publisher

The Company of Biologists

Subject

Insect Science,Molecular Biology,Animal Science and Zoology,Aquatic Science,Physiology,Ecology, Evolution, Behavior and Systematics

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