Mitochondrial respiration capacity impacts gill tissue regeneration in Atlantic salmon

Gill regeneration in fish varies inter- and intra-specifically. The latter may be associated with myriad factors including capacity of energy metabolism. This study investigated whether mitochondrial respiration capacity influences the degree of gill regeneration and features of mitochondria in regenerated tissue by feeding fish an experimental diet aimed at modulating mitochondrial efficiency. Atlantic salmon reared on standard and experimental diet were subjected to 50% filament resection on a subset of filaments on the ventral and dorsal regions of the first gill arch. Mitochondrial respiration and citrate synthase activity (CSA) were measured in the resected tips of filaments (week-0) and then in the regenerated tissue at 20 weeks post-resection (week-20). The degree of filament regeneration was measured at week-20. The experimental diet reduced CSA and respiratory control ratio (RCR), and increased proton leak at week-0, which was associated with a 30% reduction in tissue regeneration compared with fish on standard diet. While CSA increased in the regenerated tissue of experimental diet fish, there was a decline in other metrics of mitochondrial respiration including state 3, proton leak and RCR irrespective of diet. Overall, mitochondrial respiration efficiency at week-0 was positively correlated with the degree of subsequent gill tissue regeneration. Additionally, state 3 respiration and proton leak at week-20 were positively correlated with tissue regeneration, whereas CSA exhibited a negative relationship. Our results indicate that the capacity of mitochondrial respiration may at least partially explain the inter-individual variation in tissue regeneration, but mitochondrial function in the regenerating tissue may be limited.