Lean, mean, lipolytic machines: lipid mobilization in rainbow trout during graded swimming

Abstract

The mobilization of mammalian lipid reserves is strongly stimulated during exercise to reach a maximum at moderate intensities, but the effects of swimming speed on fish lipolysis have never been quantified. Continuous infusion of 2-[H]glycerol was used to measure the rate of appearance of glycerol or lipolytic rate ( glycerol) in rainbow trout kept at rest, or during graded exercise in a swim tunnel up to critical swimming speed (). Results show that glycerol is 1.67±0.18 µmol kg min in control animals, and remains at a steady level of 1.24±0.10 µmol kg min in exercising fish at all swimming intensities. Baseline lipolytic rate provides more than enough fatty acids from lipid reserves to accommodate all the oxidative fuel requirements for swimming at up to 2 body lengths per second (BL s), and more than 50% of the energy needed at (3.4±0.1 BL s). Such 'excess lipolysis' also means that trout sustain high rates of fatty acid reesterification. Maintaining steady lipolysis at rest and throughout graded swimming is strikingly different from mammals that stimulate glycerol by twofold to fivefold to support exercise. Instead, trout act like 'lipolytic machines' that do not modulate glycerol even when their metabolic rate triples - a strategy that eliminates the need to increase lipolytic rate during exercise. This study also supports the notion that maintaining a high rate of reesterification (or triacylglycerol/fatty acid cycling) may be a mechanism widely used by ectotherms to achieve rapid membrane remodelling in variable environments.

On the Utilization of Dietary Glycerol in Carnivorous Fish—Part II: Insights Into Lipid Metabolism of Rainbow Trout (Oncorhynchus mykiss) and European Seabass (Dicentrarchus labrax)

“…This was confirmed and thoroughly discussed in Part I of the present study for hepatic glycogen synthesis in rainbow trout and blood glucose regulation in European seabass (Viegas et al, 2022). Moreover, high glycerol turnover allows for incredibly high rate of re-esterification (or TAG/FA cycling) in rainbow trout at rest (Magnoni et al, 2008;Turenne and Weber, 2018) which surprisingly remains unaltered when in exercise. This is a very different paradigm when compared with mammals that need to boost their lipolytic rates (measured as R a glycerol) by 2-5 fold (Turenne and Weber, 2018).…”

“…Moreover, high glycerol turnover allows for incredibly high rate of re-esterification (or TAG/FA cycling) in rainbow trout at rest (Magnoni et al, 2008;Turenne and Weber, 2018) which surprisingly remains unaltered when in exercise. This is a very different paradigm when compared with mammals that need to boost their lipolytic rates (measured as R a glycerol) by 2-5 fold (Turenne and Weber, 2018). This mechanism in fish has also been suggested as a means to achieve rapid membrane remodeling in variable environments.…”

Lactate signaling and fuel selection in rainbow trout: mobilization of energy reserves

“…These tracer methods have been thoroughly validated in fish (28) and specifically tested in rainbow trout to assess the effects of a variety of physiological stresses on R a glucose (14,19,20,29). The method to quantify R a glycerol is also well-established for rainbow trout (21)(22)(23). All infusates were freshly prepared immediately before each experiment by drying an aliquot of the tracer obtained from the supplier under N 2 and resuspending in Cortland's saline.…”

“…For glucose kinetics, a priming dose of tracer equivalent to 3 h of infusion was injected as a bolus at the start of each infusion to reach isotopic steady state in <45 min (28,30). A priming dose was not required to measure glycerol kinetics because the total glycerol pool is small and isotopic steady state is reached in <45 min without it (21,23,30). For each flux measurement, the infusate was administered continuously at ~1 ml h -1 (the exact infusion rate was determined for each fish to adjust for differences in body mass) using a calibrated syringe pump (Harvard Apparatus, South Natick, MA).…”

“…The mobilization of lipid reserves (lipolysis or rate of appearance of glycerol in the circulation: R a glycerol) is also increased by epinephrine, but contrary to its effect in mammals, it is inhibited by norepinephrine in fish (21). Surprisingly, fish lipolytic rate remains unaffected by endurance swimming (22) or graded exercise up to critical swimming speed (U crit ) (23). Whether lactate signaling or Hcar1 are involved in modulating fuel selection in fish is unknown.…”