Skeletal muscle metabolism in sea-acclimatized king penguins: II. Improved efficiency of mitochondrial bioenergetics

Abstract

At fledging, juvenile king penguins (Aptenodytes patagonicus) must overcome the tremendous energetic constraints imposed by their marine habitat, including during sustained extensive swimming activity and deep dives in cold seawater. Both endurance swimming and skeletal muscle thermogenesis require high mitochondrial respiratory capacity while the submerged part of dive cycles repeatedly and greatly reduce oxygen availability imposing a need for solutions to conserve oxygen. The aim of the present study was to determine in vitro whether skeletal muscle mitochondria become more “thermogenic” to sustain heat production or more “economical” to conserve oxygen in sea-acclimatized immature penguins as compared with terrestrial juveniles. Rates of mitochondrial oxidative phosphorylation were measured in permeabilized fibers and mitochondria from the pectoralis muscle. Mitochondrial ATP synthesis and coupling efficiency were measured in isolated muscle mitochondria. The mitochondrial activities of respiratory chain complexes and citrate synthase were also assessed. The results showed that respiration, ATP synthesis and respiratory chain complex activities in pectoralis muscles were increased by sea acclimatization. Further, muscle mitochondria were on average 30% to 45% more energy efficient in sea-acclimatized immatures than in pre-fledging juveniles, depending on the respiratory substrate used (pyruvate; palmitoyl-carnitine). Hence, sea acclimatization favors the development of economical management of oxygen, decreasing the oxygen needed to produce a given amount of ATP. This mitochondrial phenotype may improve dive performance during the early marine life of king penguins, by extending their aerobic dive limit.

Avian red blood cell mitochondria produce more heat in winter than in autumn

“…The relative degree of coupling of the ETS to ATP production may thus depend on the animal's needs. For example, energy‐limited animals may reduce the proton leak so that ATP production is maintained despite lower overall substrate oxidation rate 16‐19 or made more effective for a given mitochondrial respiration rate 20 . Conversely, increased demands for heat production may lead to greater proton leakage and decreased coupling.…”

“…For example, energy-limited animals may reduce the proton leak so that ATP production is maintained despite lower overall substrate oxidation rate [16][17][18][19] or made more effective for a given mitochondrial respiration rate. 20 Conversely, increased demands for heat production may lead to greater proton leakage and decreased coupling. This has been studied especially in the mitochondria-rich brown adipose tissue (BAT) of mammals where uncoupling is the basis for non-shivering thermogenesis.…”

Plasticity of mitochondrial function safeguards phosphorylating respiration during in vitro simulation of rest-phase hypothermia

“…Thus, there could be scope to adjust the coupling of ETS to ATP production according to the animal's need. For example, increased mitochondrial coupling during energy limitation makes ATP production more effective for a given respiration rate [26][27][28][29] . It could, thus, be speculated that improved coupling could secure adequate ATP production even when the overall energy expenditure of the cell is reduced, such as when heat production must remain high, but substrate delivery is reduced because rest-phase hypothermia causes the mitochondria to work at a slower pace.…”

A whole blood approach improves speed and accuracy when measuring mitochondrial respiration in intact avian hematocytes

“…2008; Bourguignon et al . 2017; Roussel et al . 2020), or more thermogenic to aid endothermic heat production (Walter & Seebacher 2009).…”