Oxidative metabolism in thermogenic tissues of the swordfish and mako shark

Mitochondria isolated from the heater organ of the swordfish Xiphias gladius and the warm lateral red muscle of the mako shark Isurus oxyrinchus display respiratory control, indicating that uncoupling of oxidative phosphorylation is not important in heat production. The mitochondria of the swordfish heater organ resemble those of mammalian brown adipose tissue in their substrate preferences, oxidizing pyruvate plus malate, palmitoyl carnitine, and α‐glycerophosphate at high rates. The high hexokinase levels in the heater organ indicate exogenous glucose is an important energy source. The high activity of cytosolic α‐glycerophosphate dehydrogenase and the high rates of mitochondrial oxidation of α‐glycerophosphate indicate that cytosolic redox is balanced via the α‐glycerophosphate cycle. Calcium stimulates mitochondrial α‐glycerophosphate oxidation, and it is proposed that calcium released from the sarcoplasmic reticulum may act as the signal coupling enhanced rates of substrate oxidation with calcium transport. Based on mitochondrial respiration rates, heat generation by the intact heater organ was calculated. Complete oxidation of glucose produces heat at a greater rate than oxidation of lipids. Nevertheless, oxidation of either substrate could produce sufficient heat to maintain tissue temperature 10°C above ambient at 20°C. The mitochondria from the red muscle of the mako shark oxidize pyruvate plus malate, glutamine, glutamate, proline, and β‐hydroxybutyrate at high rates. Palmitoyl carnitine was not oxidized. The respiration rates are similar to those described for mitochondria isolated from “cold” muscle of other elasmobranchs. Therefore, it does not appear that mako shark red muscle mitochondria are specialized for thermogenesis.