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Animals at the extremes: hibernation and torpor
Animals at the extremes: hibernation and torpor

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5.3 Mitochondrial adaptations

During the winter months, whilst hibernating vertebrates maintain a very low metabolic rate, major reorganization of mitochondrial metabolism occurs. The phenomenon has been studied in some detail in frogs which, although not hibernators in the true sense, can endure very low water temperatures under the conditions of profound hypoxia that exist when they lie dormant for long periods below the surface. In contrast to normoxic conditions, the muscle mitochondria of dormant frogs depress their metabolic rate by up to 75%. Since muscles comprise a large part of the body mass, depression of their mitochondria decreases the overall oxidative metabolism of the frog profoundly. Although uptake of oxygen into mitochondria is decreased both in normoxic hypothermia and in the anoxic conditions of dormant frogs, only in the latter are long-term adaptations observed. Such adaptations include an increased affinity of mitochondria for dissolved oxygen, a reduction in the activity of mitochondrial enzymes, a reduction in the activity of the electron transfer chain and a reduction in the proton leak across the inner mitochondrial membrane.

In normoxic mammalian muscle mitochondria, it has been estimated that over 30% of the standard metabolic rate comprises the movement of protons into the mitochondrial matrix which is uncoupled from ATP synthesis (see Section 3.4). The electrochemical gradient (and hence the potential energy available from oxidative phosphorylation) across the inner mitochondrial membrane is maintained by the ‘proton-motive force’ (PMF), measurable as the potential difference across the membrane. At a time when energy substrate is very scarce, the proton leak is counterproductive for energy conservation.

To reduce energy wastage, the inner membrane ATP-synthase in frog muscle begins to catalyse the reverse reaction, releasing energy by ATP hydrolysis, to maintain the proton gradient across the membrane. The small amount of energy required to reduce the cycling of protons to a level equalling their rate of supply from the electron transfer chain is more than compensated for by the increased efficiency of the anoxic mitochondrion. This principle is illustrated in Figure 30. Under normoxic conditions, the passive flow of protons from the intermembrane space of the mitochodrion into the matrix is increased as the potential difference across the membrane rises. This gradient is nearly absent in the anoxic mitochondrion (Boutilier and St-Pierre, 2002).

Kinetics of frog skeletal muscle mito-chondrial proton leak during normoxia and in anoxia
Boutilier, R. G. and St-Pierre, J. (2002) Adaptive plasticity of skeletal muscle energetics in hibernating frogs: mitochondrial proton leak during metabolic depression, Journal of Experimental Biology, 205. Copyright © Company of Biologists Ltd
Figure 30 Kinetics of frog skeletal muscle mitochondrial proton leak during normoxia and in anoxia

It is not surprising that this phenomenon is also seen in mammals that hibernate on land, such as the arctic ground squirrel. The supply of lipid to the mitochondria of the heart and BAT is substantially increased during hibernation, as shown by the increased production of fatty-acid binding proteins that deliver fatty acids to the enzyme complex catalysing β-oxidation.