Mitochondrial Activity Localization in the Skeletal Muscle and Its Individual Fibers Across Tetrapods

Mitochondria exhibit a complex spatially organized distribution within muscle, tailored to the energy requirements of ATPases and contractile filaments, which exhibit precise intracellular positioning. Mitochondrial distribution varies across longitudinal and transverse axes as well as based on fiber composition within the muscle. The differential mitochondrial capacity can be localized in muscle by succinate dehydrogenase (SDH) activity. Given the distinct energy requirements of the fore-limb and hind-limb muscles, this study aimed to investigate the distribution of mitochondrial activity within individual fibers and their composition within fascicles across different tetrapod taxa. We analyzed pectoralis and gastrocnemius from toad, garden lizard, duck, pigeon, quail, chicken, rat, rabbit, goat, and buffalo. The study revealed unique patterns of mitochondrial activity distribution within the same muscle across various tetrapods. Toad and lizard muscles showed mostly fibers with intermediate SDH-activity (SDH^Int) in both muscles. The muscles only from birds and mammals exhibited fibers with negligible SDH-activity termed SDH^Low, which might indicate that such fibers are evolutionarily more recent. Interestingly, avian pectoralis showed a very unique fiber composition compared to mammals, which displayed a mosaic pattern of different fibers. Among mammals, slow-grazers (buffaloes, goats) had higher percentages of SDH^High and SDH^Int fibers, whereas sprint-runners (rats, rabbits) possessed a high abundance of SDH^Low fibers. These findings provide evidence for localized mitochondrial enrichment as an adaptation strategy to create muscle group heterogeneity. SUMMARY STATEMENT: This study characterizes the spatial distribution of mitochondrial activity in skeletal muscle across tetrapods, from the single-fiber scale to the fascicular level.