Muscle metabolic remodeling in response to endurance exercise in salmonids

Abstract

Phenotypic plasticity of skeletal muscle is relevant to swimming performance and metabolism in fishes, especially those that undergo extreme locomotory feats, such as seasonal migration. However, the influence of endurance exercise and the molecular mechanisms coordinating this remodeling are not well understood. The present study examines muscle metabolic remodeling associated with endurance exercise in fed rainbow trout as compared to migrating salmon. Trout were swum for 4 weeks at 1.5 BL/s, a speed similar to that of migrating salmon and red and white muscles were sampled after each week. We quantified changes in key enzymes in aerobic and carbohydrate metabolism [citrate synthase (CS), β-hydroxyacyl-CoA dehydrogenase (HOAD), hexokinase (HK)] and changes in mRNA expression of major regulators of metabolic phenotype (AMPK, PPARs) and lipid (carnitine palmitoyltransferase, CPT I), protein (aspartate aminotransferase, AST) and carbohydrate (HK) oxidation pathways. After 1 week of swimming substantial increases were seen in AMPK and PPARα mRNA expression and of their downstream target genes, CPTI and HK in red muscle. However, significant changes in CS and HK activity occurred only after 4 weeks. In contrast, there were few changes in mRNA expression and enzyme activities in white muscle over the 4-weeks. Red muscle results mimic those found in migrating salmon suggesting a strong influence of exercise on red muscle phenotype. In white muscle, only changes in AMPK and PPAR expression were similar to that seen with migrating salmon. However, in contrast to exercise alone, in natural migration HK decreased while AST increased suggesting that white muscle plays a role in supplying fuel and intermediates possibly through tissue breakdown during prolonged fasting. Dissecting individual and potentially synergistic effects of multiple stressors will enable us to determine major drivers of the metabolic phenotype and their impacts on whole animal performance.

Environmental enrichment improves growth and fillet quality in rainbow trout

“…68 Under multiple stressors, including increased exercise, enzyme levels like HK are known to increase in salmonids. 69 As with LDH, it was quite similar across treatments in the current study. The only difference was regarding fasted CUC fish, with approximately twice the values compared with RFC and CON.…”

“…HK enzyme is responsible for initiating the glycolytic pathway 65 and is used as an indicator of carbohydrate use, helping to keep blood glucose levels stable 68 . Under multiple stressors, including increased exercise, enzyme levels like HK are known to increase in salmonids 69 . As with LDH, it was quite similar across treatments in the current study.…”

Growth-promoting effects of sustained swimming in fingerlings of gilthead sea bream (Sparus aurata L.)

“…In contrast, the same study showed that mitochondrial activity and CS in particular are down-regulated by multiple sensory perception stressors. White muscle CS activity also increases under moderate activity in zebrafish (Danio rerio) (McCelland et al 2006), but a significant reduction has been observed in rainbow trout after four weeks at 1.5 BL•s -1 (Morash et al 2014), which demonstrates a complex and sometimes contradictory regulation. In exercised brown trout (Salmo trutta), the COX activity of skeletal muscle also increased at a low velocity (42% of maximal swimming capacity), but decreased when the swimming capacity increased to 83% of maximal capacity (Antilla et al 2010).…”

Muscles Susceptibility to Ischemia-Reperfusion Injuries Depends on Fiber Type Specific Antioxidant Level

“…Further, the effects of exercise likely depend on muscle metabolic phenotype. For instance, exercise has a stronger influence on red muscle phenotype, as compared to white muscle in salmonids (Morash et al, 2014 ). Similarly, uphill-, as compared to down-hill training enhanced mitochondrial function specifically in both soleus and vastus intermedius skeletal muscle (Schlagowski et al, 2016 ).…”