Adjustments in control of mitochondrial respiratory capacity while facing temperature fluctuations

Abstract

As the world's climate changes, life faces an evolving thermal environment. Mitochondrial oxidative phosphorylation (OXPHOS) is critical to ensure sufficient cellular energy production, and it is strongly influenced by temperature. The thermally-induced changes to the regulation by specific steps within the OXPHOS process are poorly understood. In our study, we used the eurythermal species of planarian Dugesia tigrina to study the thermal sensitivity of the OXPHOS process at 10, 15, 20, 25, 30°C. We conducted cold acclimation experiments where we measured the adjustment of specific steps at two assay temperatures (10 and 20°C) following four weeks of acclimation under normal (22°C) or low (5°C) temperature conditions. At the low temperature, the contribution of the NADH pathway to the maximal OXPHOS capacity, in a combined pathway (NADH and succinate) was reduced. There was partial compensation by an increased contribution of the succinate pathway. As the temperature decreases, OXPHOS becomes more limited by the capacity of the phosphorylation system. Acclimation to the low temperature resulted in positive adjustments of the NADH pathway capacity due, at least in part, to an increase in complex I activity. The acclimation also resulted in a better match between OXPHOS and phosphorylation system capacities. Both of these adjustments following acclimation were specific to the low assay temperature. We conclude that there is substantial plasticity in the mitochondrial OXPHOS process following thermal acclimation in D. tigrina, and this is likely contributing to the wide thermal range of the species.