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

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.

Coping with an exogenous glucose overload: glucose kinetics of rainbow trout during graded swimming.

This study examines how chronically hyperglycemic rainbow trout modulate glucose kinetics in response to graded exercise up to critical swimming speed (Ucrit), with or without exogenous glucose supply. Our goals were 1) to quantify the rates of hepatic glucose production (Ra glucose) and disposal (Rd glucose) during graded swimming, 2) to determine how exogenous glucose affects the changes in glucose fluxes caused by exercise, and 3) to establish whether exogenous glucose modifies Ucrit or the cost of transport. Results show that graded swimming causes no change in Ra and Rd glucose at speeds below 2.5 body lengths per second (BL/s), but that glucose fluxes may be stimulated at the highest speeds. Excellent glucoregulation is also achieved at all exercise intensities. When exogenous glucose is supplied during exercise, trout suppress hepatic production from 16.4 ± 1.6 to 4.1 ± 1.7 µmol·kg(-1)·min(-1) and boost glucose disposal to 40.1 ± 13 µmol·kg(-1)·min(-1). These responses limit the effects of exogenous glucose to a 2.5-fold increase in glycemia, whereas fish showing no modulation of fluxes would reach dangerous levels of 114 mM of blood glucose. Exogenous glucose reduces metabolic rate by 16% and, therefore, causes total cost of transport to decrease accordingly. High glucose availability does not improve Ucrit because the fish are unable to take advantage of this extra fuel during maximal exercise and rely on tissue glycogen instead. In conclusion, trout have a remarkable ability to adjust glucose fluxes that allows them to cope with the cumulative stresses of a glucose overload and graded exercise.

Exogenous lactate supply affects lactate kinetics of rainbow trout, not swimming performance.

Intense swimming causes circulatory lactate accumulation in rainbow trout because lactate disposal (Rd) is not stimulated as strongly as lactate appearance (Ra). This mismatch suggests that maximal Rd is limited by tissue capacity to metabolize lactate. This study uses exogenous lactate to investigate what constrains maximal Rd and minimal Ra. Our goals were to determine how exogenous lactate affects: 1) Ra and Rd of lactate under baseline conditions or during graded swimming, and 2) exercise performance (critical swimming speed, Ucrit) and energetics (cost of transport, COT). Results show that exogenous lactate allows swimming trout to boost maximal Rd lactate by 40% and reach impressive rates of 56 µmol·kg(-1)·min(-1). This shows that the metabolic capacity of tissues for lactate disposal is not responsible for setting the highest Rd normally observed after intense swimming. Baseline endogenous Ra (resting in normoxic water) is not significantly reduced by exogenous lactate supply. Therefore, trout have an obligatory need to produce lactate, either as a fuel for oxidative tissues and/or from organs relying on glycolysis. Exogenous lactate does not affect Ucrit or COT, probably because it acts as a substitute for glucose and lipids rather than extra fuel. We conclude that the observed 40% increase in Rd lactate is made possible by accelerating lactate entry into oxidative tissues via monocarboxylate transporters (MCTs). This observation together with the weak expression of MCTs and the phenomenon of white muscle lactate retention show that lactate metabolism of rainbow trout is significantly constrained by transmembrane transport.

Lactate kinetics of rainbow trout during graded exercise: do catheters affect the cost of transport?

Changes in lactate kinetics as a function of exercise intensity have never been measured in an ectotherm. Continuous infusion of a tracer is necessary to quantify rates of lactate appearance (Ra) and disposal (Rd), but it requires double catheterization, which could interfere with swimming. Using rainbow trout, our goals were to: (1) determine the potential effects of catheters and blood sampling on metabolic rate (O2), total cost of transport (TCOT), net cost of transport (NCOT) and critical swimming speed (Ucrit), and (2) monitor changes in lactate fluxes during prolonged, steady-state swimming or graded swimming from rest to Ucrit. This athletic species maintains high baseline lactate fluxes of 24 µmol kg(-1) min(-1) that are only increased at intensities >2.4 body lengths (BL) s(-1) or 85% Ucrit. As the fish reaches Ucrit, Ra is more strongly stimulated (+67% to 40.4 µmol kg(-1) min(-1)) than Rd (+41% to 34.7 µmol kg(-1) min(-1)), causing a fourfold increase in blood lactate concentration. Without this stimulation of Rd during intense swimming, lactate accumulation would double. By contrast, steady-state exercise at 1.7 BL s(-1) increases lactate fluxes to ~30 µmol kg(-1) min(-1), with a trivial mismatch between Ra and Rd that only affects blood concentration minimally. Results also show that the catheterizations and blood sampling needed to measure metabolite kinetics in exercising fish have no significant impact on O2 or TCOT. However, these experimental procedures affect locomotion energetics by increasing NCOT at high speeds and by decreasing Ucrit.

Metabolic effects of exercise in the golden fish Salminus maxillosus "dourado" (Valenciennes, 1849)

Strenuous exercise in fish is usually a consequence of migration, reproduction, and spawning. Varying among fishes, this kind of stress is associated with blood glucose and lactate increase, in relation to which two major groups are distinguishable: the "lactate releasers" and "non-lactate releasers". Unlike strenuous exercise, sustained swimming imposes a variety of effort that results in distinct kinetic types of blood lactate and glucose. Compared to Platichthys stellatus and Oncorhynchus mikyiss, blood lactate of Salminus maxillosus (dourado) was lower after exercise, whereas recovery time was greater. Great demands were made of white muscle, and dourado is not a lactate releaser. Two different metabolic tendencies were observed in sustained and intense swimming. Gluconeogenesis was observed during recovery, as well as the alanine cycle which recomposes the lactate tissue pattern. Full recovery after intensive exertion required more than 24 hours.

Exercício intenso em peixes normalmente é conseqüência de migração, reprodução e desova. Esse tipo de esforço está associado ao aumento de glicose sangüínea e de lactato, o qual varia entre as diferentes espécies de peixes. Dois grupos são conhecidos, os "liberadores" e os "não liberadores" de lactato. Diferentemente do exercício intenso, o exercício contínuo impõe certo esforço que resulta em distintos tipos de cinética de lactato e glicose. A concentração de lactato plasmático em Salminus maxillosus é menor após o exercício quando comparada à Platichthys stellatus e Oncorhynchus mikyiss, mas o tempo de recuperação é maior. A musculatura branca é particularmente requisitada e o dourado apresenta-se como um "não liberador" de lactato. Duas tendências metabólicas distintas foram observadas para o exercício contínuo e intensivo. A gliconeogênese, que foi observada durante a recuperação, e o ciclo da alanina, que recompôs o padrão tissular de lactato. O período de completa recuperação do exercício intenso foi maior que 24 horas.