Origins of variation in muscle cytochrome c oxidase activity within and between fish species

Abstract

Mitochondrial content, central to aerobic metabolism, is thought to be controlled by a few transcriptional master regulators, including nuclear respiratory factor 1 (NRF-1), NRF-2 and peroxisome proliferator-activated receptor-γ coactivator-1α (PGC-1α). Though well studied in mammals, the mechanisms by which these factors control mitochondrial content have been less studied in lower vertebrates. We evaluated the role of these transcriptional regulators in seasonal changes in white muscle cytochrome c oxidase (COX) activity in eight local fish species representing five families: Centrarchidae, Umbridae, Esocidae, Gasterosteidae and Cyprinidae. Amongst centrarchids, COX activity was significantly higher in winter for pumpkinseed (2-fold) and black crappie (1.3-fold) but not bluegill or largemouth bass. In esociforms, winter COX activity was significantly higher in central mudminnow (3.5-fold) but not northern pike. COX activity was significantly higher in winter-acclimatized brook stickleback (2-fold) and northern redbelly dace (3-fold). Though mudminnow COX activity increased in winter, lab acclimation to winter temperatures did not alter COX activity, suggesting a role for non-thermal cues. When mRNA was measured for putative master regulators of mitochondria, there was little evidence for a uniform relationship between COX activity and any of NRF-1, NRF-2α or PGC-1α mRNA levels Collectively, these studies argue against a simple temperature-dependent mitochondrial response ubiquitous in fish, and suggest that pathways which control mitochondrial content in fish may differ in important ways from those of the better studied mammals.