Surviving the drought: burrowing frogs save energy by increasing mitochondrial coupling

Abstract

SUMMARY During dormancy energy conservation is a key priority and as such dormant animals undergo a major metabolic depression to conserve their limited endogenous fuel supplies. Mitochondrial coupling efficiency, the efficiency with which mitochondria convert oxygen into ATP, significantly affects aerobic metabolism and thus to maximise energy savings during dormancy it has been hypothesised that coupling efficiency should increase. However, previous studies have shown coupling efficiency to be maintained or even to decrease. In this study we measured state 3 and state 4 mitochondrial respiration in the muscle of the burrowing frog, Cyclorana alboguttata and calculated the respiratory control ratio as a measure of coupling efficiency. After 7 months in aestivation, C. alboguttata significantly reduced oxygen consumption of isolated mitochondria by 83% and, unlike other dormant animals,the frogs appeared to decrease rates of proton leak to a greater extent than ATP synthesis, consistent with an increase in mitochondrial coupling efficiency. The significant energy savings observed at the mitochondrial level were reflected at higher levels of biological organisation, with tissue oxygen consumption depressed by as much as 81% and whole animal metabolic rate by 82%. Cyclorana alboguttata can survive in a dormant state for several years and we propose the hypothesis that energy efficiency is increased during aestivation.