Hepatic Glycerol Metabolism-Related Genes in Carnivorous Rainbow Trout (Oncorhynchus mykiss): Insights Into Molecular Characteristics, Ontogenesis, and Nutritional Regulation

Abstract

Glycerol metabolism in rainbow trout is poorly studied even though it is at the interface between lipid and glucose metabolism. Moreover, glycerol can be an important ingredient in new aquafeed formulation to decrease the catabolism of dietary amino acids. Thus, the present study aimed to characterize for the first time the different genes coding for key enzymes and proteins involved in hepatic glycerol metabolism. From the trout genomes, all the paralogous genes coding for glycerol transport (aqp9b), glycerol kinase (gk2a and gk5), glycerol-3-phosphate phosphatase (pgp), and glycerol-3phosphate dehydrogenase (gpd1a, gpd1b, and gpd1c) were identified. The ontogenesis determined that the capacity to metabolize glycerol begins with the apparition of the liver during the development (stage 22) and are more expressed at the endogenousexogenous feeding period (stage 35). The postprandial regulation of the expression of these genes in juvenile trout showed that the postprandial peak of expression is between 4 and 24 h after the last meal for many of the genes, demonstrating that glycerol metabolism could be nutritionally regulated at a molecular level. However, surprisingly, no regulation of the mRNA abundance for the glycerol metabolism-related genes by different levels of dietary glycerol (0, 2.5, and 5%) have been detected, showing that hepatic glycerol metabolism is poorly regulated at a molecular level by dietary glycerol in rainbow trout juveniles.

On the Utilization of Dietary Glycerol in Carnivorous Fish - Part I: Insights Into Hepatic Carbohydrate Metabolism of Juvenile Rainbow Trout (Oncorhynchus mykiss) and European Seabass (Dicentrarchus labrax)

“…The liver is the primary site for the de novo synthesis of glycerol so several metabolic pathways can mobilize and utilize its three carbons. The gene expressions for aqp9b during embryogenesis in trout does not appear along the setup of the primitive liver and hepatic portal vein, but rather at a later stage just before the first feeding (Panserat et al, 2020). Similar to that reported in trout, the present glycerol-supplemented diets had no effect on the mRNA levels of AQP9 in juvenile seabass liver at both 6 and 24 h (unpublished).…”

“…When compared with control diets, glycerol-supplemented diets in fish affect glycemia in a species-specific manner with often erratic, non-dose-dependent patterns (if compared at 24 h after last meal). In rainbow trout, while no alterations were reported in inclusions up to 5% glycerol (Panserat et al, 2020), 6% inclusions provoked a significant increase in glycemia (Menton et al, 1986). In channel catfish, glycemia increased at 5% inclusion but remained at control levels up to 20% inclusion (Li et al, 2010).…”

“…Similar to that reported in trout, the present glycerol-supplemented diets had no effect on the mRNA levels of AQP9 in juvenile seabass liver at both 6 and 24 h (unpublished). Short-term fasting (48 h) followed by refeeding also had no effect in hepatic AQP9 mRNA levels in juvenile trout (Panserat et al, 2020). On the other hand, the presence and distribution of AQP9 in the membrane of seabass hepatocytes increased in long-term (35 d) fasted fish followed by a decrease in refed fish (Gambardella et al, 2012).…”

“…Upon entrance in the liver, glycerol kinase catalyzes the initial phosphorylation of glycerol into G3P, which intersects with gluconeogenic/glycolityc pathways after being oxidized into dihydroxyacetone phosphate (DHAP) by G3P dehydrogenase. Both glycerol kinase and G3P dehydrogenase were poorly regulated by dietary glycerol levels in trout (Panserat et al, 2020) and Nile tilapia (Costa et al, 2015); even if G3P dehydrogenase and G3P phosphatase (reverse reaction of glycerol kinase) were deemed essential for cold adaptation in rainbow smelt (Driedzic et al, 2006). However, in trout the kinetics of postprandial regulation of glycerol-related enzymes (at first feeding stage and juvenile stage) when fed glycerolsupplemented diets (Panserat et al, 2020) was similar to the previously reported glycolytic and gluconeogenic genes when fed high-carbohydrate diets (Panserat et al, 2019).…”

“…Finally, inclusions up to 10% glycerol resulted in unaltered glycemia in Nile tilapia (Neu et al, 2013). To our knowledge, it is only recently that there has been some insight into the molecular and nutritional regulation of hepatic glycerol-related enzymes in fish (Panserat et al, 2020). However, the homeostatic mechanisms triggered in response to circulating dietary glycerol are yet to be addressed, namely the down-stream alterations into a metabolic rearrangement of the energetic substrates to regulate glycemia and store hepatic glycogen.…”