Metabolic fuel kinetics in fish: swimming, hypoxia and muscle membranes

Abstract

Muscle performance depends on the supply of metabolic fuels and disposal of end-products. Using circulating metabolite concentrations to infer changes in fluxes is highly unreliable because the relationship between these parameters varies greatly with physiological state. Quantifying fuel kinetics directly is therefore crucial to the understanding of muscle metabolism. This review focuses on how carbohydrates, lipids and amino acids are provided to fish muscles during hypoxia and swimming. Both stresses force white muscle to produce lactate at higher rates than it can be processed by aerobic tissues. However, lactate accumulation is minimized because disposal is also strongly stimulated. Exogenous supply shows that trout have a much higher capacity to metabolize lactate than observed during hypoxia or intense swimming. The low density of monocarboxylate transporters and their lack of upregulation with exercise explain the phenomenon of white muscle lactate retention. This tissue operates as a quasi-closed system, where glycogen stores act as an 'energy spring' that alternates between explosive power release during swimming and slow recoil from lactate in situ during recovery. To cope with exogenous glucose, trout can completely suppress hepatic production and boost glucose disposal. Without these responses, glycemia would increase four times faster and reach dangerous levels. The capacity of salmonids for glucoregulation is therefore much better than presently described in the literature. Instead of albumin-bound fatty acids, fish use lipoproteins to shuttle energy from adipose tissue to working muscles during prolonged exercise. Proteins may play an important role in fueling muscle work in fish, but their exact contribution is yet to be established. The membrane pacemaker theory of metabolism accurately predicts general properties of muscle membranes such as unsaturation, but it does not explain allometric patterns of specific fatty acids. Investigations of metabolic fuel kinetics carried out in fish to date have demonstrated that these ectotherms use several unique strategies to orchestrate energy supply to working muscles and to survive hypoxia.

Protein changes as robust signatures of fish chronic stress: a proteomics approach in fish welfare research

“…When insufficient oxygen is available to maintain the aerobic ATP production, fish resort to anaerobic metabolism to meet cellular requirements. This shift consequently leads to lactate accumulation in the muscle (19,53). In this study, changes in circulating lactate are not in agreement with cortisol and glucose variations.…”

Metabolomics and fish nutrition: a review in the context of sustainable feed development

“…Chronic stress is also associated with higher lactate production (Karakach et al 2009). Furthermore, fish muscle retains lactate, especially in rainbow trout (Gleeson 1996;Weber et al 2016). The duration of post-mortem sampling time also affects lactate content through rapid depletion of glycogen stores.…”

Effects of dietary dehydrated lemon peel on some biochemical markers related to general metabolism, welfare and stress in gilthead seabream (Sparus aurataL.)

“…This lactate cannot be quickly processed, like glucose, from red muscle, heart, gills and brain. Some fish, like trout, use lactate as principal oxidative fuel (Weber, Choi, Gonzalez, & Omlin, 2016). Glucose and lactate are physiological indicators of non-specific stress (Chase, Flynn, & Todgham, 2016).…”