The molecular basis of aerobic metabolic remodeling differs between oxidative muscle and liver of threespine sticklebacks in response to cold acclimation

Abstract

We sought to determine the molecular basis of elevations in aerobic metabolic capacity in the oxidative muscle and liver of Gasterosteus aculeatus in response to cold acclimation. Fishes were cold- or warm-acclimated for 9 wk and harvested on days 1, 2, and 3 and weeks 1, 4, and 9 of cold acclimation at 8 degrees C, and on day 1 and week 9 of warm acclimation at 20 degrees C. Mitochondrial volume density was quantified using transmission electron microscopy and stereological techniques in warm- and cold-acclimated fishes harvested after 9 wk at 20 or 8 degrees C. Changes in aerobic metabolic capacity were assessed by measuring the maximal activity of citrate synthase (CS) and cytochrome-c oxidase (COX) in fishes harvested throughout the acclimation period. Transcript levels of the aerobic metabolic genes CS, COXIII, and COXIV, and known regulators of mitochondrial biogenesis, including peroxisome proliferator-activated receptor-gamma coactivators-1alpha and -1beta (PGC-1alpha and PGC-1beta), nuclear respiratory factor-1 (NRF-1), and mitochondrial transcription factor-A were measured in fishes harvested throughout the acclimation period using quantitative real-time PCR. The maximal activities of CS and COX increased in response to cold acclimation in both tissues, but mitochondrial volume density only increased in oxidative muscle (P < 0.05). The time course for changes in aerobic metabolic capacity differed between liver and muscle. The expression of CS increased within 1 wk of cold acclimation in liver and was correlated with an increase in mRNA levels of NRF-1 and PGC-1beta. Transcript levels of aerobic metabolic genes increased later in oxidative muscle, between weeks 4 and 9 of cold acclimation and were correlated with an increase in mRNA levels of NRF-1 and PGC-1alpha. These results show that aerobic metabolic remodeling differs between liver and muscle in response to cold acclimation and may be triggered by different stimuli.