Skeletal muscle heterogeneity in fasting-induced mitochondrial oxidative phosphorylation flexibility in cold-acclimated ducklings

Abstract

Starvation remains particularly challenging for endotherms that remain active in cold environments or during winter. The aim of this study was to determine whether fasting-induced mitochondrial coupling flexibility depends upon the phenotype of skeletal muscles. The rates of oxidative phosphorylation and mitochondrial efficiency were measured in pectoralis (glycolytic) and gastrocnemius (oxidative) muscles from cold-acclimated ducklings (Cairina moschata). Pyruvate and palmitoyl-L-carnitine were used in the presence of malate as respiratory substrates. Plasma metabolites, skeletal muscle concentrations of triglycerides, glycogen and total protein and mitochondrial levels of oxidative phosphorylation complexes were also quantified. Results from fed ad libitum ducklings were compared to ducklings allowed to fast for 4 days. During the 4 days of nutritional treatment, birds remained in the cold, at 4°C. It is reported that 4 days of starvation preferentially affected the pectoralis muscles, inducing an up-regulation of mitochondrial efficiency, which was associated with a reduction of both total muscle and mitochondrial oxidative phosphorylation protein and an increase of intramuscular lipid concentrations. By contrast, fasting decreased the activity of oxidative phosphorylation but did not alter the coupling efficiency and protein expressions of mitochondria isolated from the gastrocnemius muscles. Hence, the adjustment of mitochondrial efficiency to fasting depends upon the muscle phenotype of cold-acclimated birds. Furthermore, these results suggest that the reduced cost of mitochondrial ATP production in pectoralis muscles may triggers lipid storage within this tissue and help to sustain an important metabolic homeostatic function of skeletal muscles, which is to maintain levels of amino acids in the circulation during the fast.