Dynamics of mitochondrial adaptation and energy metabolism in rainbow trout (Oncorhynchus mykiss) in response to sustainable diet and temperature.

Impacts of plant-based ingredients and temperatures on energy metabolism in rainbow trout was investigated. A total of 288 fish (mean body weight: 45.6 g) were fed four isocaloric, isolipidic, and isonitrogenous diets containing 40% protein and 20% lipid and formulated as 100% animal-based protein (AP) and a blend of 50% fish oil (FO) and 50% camelina oil (CO); 100% AP and100% CO; 100% plant-based protein (PP) and a blend of 50% FO and 50% CO or 100% PP and 100% CO at 14 or 18 °C for 150 d. Diet did not significantly affect weight gain (WG) (P = 0.1902), condition factor (CF) (P = 0.0833) or specific growth rate (SGR) (P = 0.1511), but diet significantly impacted both feed efficiency (FE) (P = 0.0076) and feed intake (FI) (P = 0.0076). Temperature did not significantly affect WG (P = 0.1231), FE (P = 0.0634), FI (P = 0.0879), CF (P = 0.8277), or SGR (P = 0.1232). The diet × temperature interaction did not significantly affect WG (P = 0.7203), FE (P = 0.4799), FI (P = 0.2783), CF (P = 0.5071), or SGR (P = 0.7429). Furthermore, temperature did not influence protein efficiency ratio (P = 0.0633), lipid efficiency ratio (P = 0.0630), protein productive value (P = 0.0756), energy productive value (P = 0.1048), and lipid productive value (P = 0.1386); however, diet had significant main effects on PER (P = 0.0076), LPV (P = 0.0075), and PPV (P = 0.0138). Temperature regimens induced increased activities of mitochondrial complexes I (P = 0.0120), II (P = 0.0008), III (P = 0.0010), IV (P < 0.0001), V (P < 0.0001), and citrate synthase (CS) (P < 0.0001) in the intestine; complexes I (P < 0.0001), II (P < 0.0001), and CS (P = 0.0122) in the muscle; and complexes I (P < 0.0001), II (P < 0.0001), and III (P < 0.0001) in the liver. Similarly, dietary composition significantly affected complexes I (P < 0.0001), II (P < 0.0001), IV (P < 0.0001), V (P < 0.0001), and CS (P < 0.0001) in the intestine; complexes I (P < 0.0001), II (P < 0.0001), III (P = 0.0002), IV (P < 0.0001), V (P = 0.0060), and CS (P < 0.0001) in the muscle; and complexes I (P < 0.0001), II (P < 0.0001), IV (P < 0.0001), V (P < 0.0001), and CS (P < 0.0001) in the liver activities except complex III activities in intestine (P = 0.0817) and liver (P = 0.4662). The diet × temperature interaction impacted CS activity in the intestine (P = 0.0010), complex II in the muscle (P = 0.0079), and complexes I (P = 0.0009) and II (P = 0.0348) in the liver. Overall, comparing partial to full dietary substitution of FO with CO, partial dietary replacement showed similar effects on complex activities.

Diets are one of the most important consideration in aquaculture production as more than 50% of production costs are incurred in raising cultured fish to market size. As the price of FM and FO continues to increase, it is necessary to seek alternative sources of proteins and oils for sustainable aquaculture development. Plant-based ingredient sources have appeared as sustainable alternatives; however, it is uncertain whether the uses of plant-based alternatives will be appropriate in securing the production of carnivorous aquaculture species in the context of global warming, with studies postulating on the potential effects of climate change on fish growth and health. A study was conducted to examine how the replacement of FM and FO with sustainable plant-based protein and camelina oil (CO) as ingredient sources at 14 or 18 °C would affect the growth performance, nutrient utilization efficiencies, and mitochondrial enzyme activity in rainbow trout. Based on the results, mitochondrial enzyme activities were generally higher at 18 °C and CO could replace 50% dietary FO without negative effects on rainbow trout. Overall, our study demonstrated that animal-based protein with CO is as good as animal-based with FO for growth and health, thus providing potentially sustainable diet options for aquaculture.

Combined effects of diets and temperature on mitochondrial function, growth and nutrient efficiency in rainbow trout (Oncorhynchus mykiss).

A 4×3 factorial experiment was conducted to evaluate the effects of two dietary protein sources (mixed fishmeal/plant protein-, and plant protein- based diet), two dietary lipid levels (10% and 20%) and three water temperatures (10°C, 14°C, and 18°C) on the growth performance, nutrient utilization efficiencies and mitochondrial enzyme complex activities in rainbow trout Oncorhynchus mykiss (average weight±SD, 39.5±5g) over a 180day rearing period. At the end of the experiment, weight gain (WG), condition factor (CF), and feed efficiency (FE) were significantly affected by diet×temperature interaction (P<0.05). Specific growth rate (SGR) was significantly affected by increasing temperature (P<0.05). The plant protein-based diets led to a higher CF than the mixed fishmeal/plant protein-based diets. The protein productive value (PPV), protein efficiency ratio (PER), lipid efficiency ratio, (LER) and lipid productive value (LPV) were all significantly affected by diet×temperature interaction (P<0.05). The diet×temperature interaction also had significant effects on mitochondrial enzyme complexes II, V and citrate synthase in the liver, complexes II and IV in the intestine, and complex IV in the muscle (P<0.05). Temperature had a significant main effect on the activity of the enzymatic complexes I and III in the liver, complex III and citrate synthase in the intestine, and complexes I, II, III, V and citrate synthase in the muscle (P<0.05). Diet had a significant main effect on complexes I and III in the liver, complexes II and III for the intestine and complexes I and II in the muscle (P<0.05). The significant temperature x diet interaction observed has practical ecological implications explicitly demonstrating how changes in temperature regimens as anticipated in the rising global temperature can influence organismal performance in relation to changes in dietary formulations (replacing fishmeal based diet with plant protein based ingredients). To illustrate the practical application of the observations from this study, the most economical and cost effective way to produce rainbow trout would be to use 40/10PP diet at 14°C because fish fed this treatment had a weight gain comparable to that of the fish fed the more expensive experimental diets (40/10 FM/PP, 40/20 FM/PP, and 40/20 PP).

Interactive effects of dietary lipid and phenotypic feed efficiency on the expression of nuclear and mitochondrial genes involved in the mitochondrial electron transport chain in rainbow trout.

A 2 × 3 factorial study was conducted to evaluate the effects of dietary lipid level on the expression of mitochondrial and nuclear genes involved in electron transport chain in all-female rainbow trout Oncorhynchus mykiss. Three practical diets with a fixed crude protein content of 40%, formulated to contain 10% (40/10), 20% (40/20) and 30% (40/30) dietary lipid, were fed to apparent satiety to triplicate groups of either low-feed efficient (F120; 217.66 ± 2.24 g initial average mass) or high-feed efficient (F136; 205.47 ± 1.27 g) full-sib families of fish, twice per day, for 90 days. At the end of the experiment, the results showed that there is an interactive effect of the dietary lipid levels and the phenotypic feed efficiency (growth rate and feed efficiency) on the expression of the mitochondrial genes nd1 (NADH dehydrogenase subunit 1), cytb (Cytochrome b), cox1 (Cytochrome c oxidase subunits 1), cox2 (Cytochrome c oxidase subunits 2) and atp6 (ATP synthase subunit 6) and nuclear genes ucp2α (uncoupling proteins 2 alpha), ucp2ß (uncoupling proteins 2 beta), pparα (peroxisome proliferator-activated receptor alpha), pparß (peroxisome proliferatoractivated receptor beta) and ppargc1α (proliferator-activated receptor gamma coactivator 1 alpha) in fish liver, intestine and muscle, except on ppargc1α in the muscle which was affected by the diet and the family separately. Also, the results revealed that the expression of mitochondrial genes is associated with that of nuclear genes involved in electron transport chain in fish liver, intestine and muscle. Furthermore, this work showed that the expression of mitochondrial genes parallels with the expression of genes encoding uncoupling proteins (UCP) in the liver and the intestine of rainbow trout. This study for the first time presents the molecular basis of the effects of dietary lipid level on mitochondrial and nuclear genes involved in mitochondrial electron transport chain in fish.

Genetic variation in feed consumption, growth, nutrient utilization efficiency and mitochondrial function within a farmed population of channel catfish (Ictalurus punctatus).

We evaluated the effects of diets (32/4 or 36/6 percent protein/fat) and six channel catfish families for growth performance characteristics. Two families with fast- (C) and slow- (D) growth rate and with low and high feed efficiency (FE) were selected for analyses of mitochondrial complex enzymatic activities (I, II, III, and IV) and gene expression (ND1, CYTB, COX1, COX2, ATP6) levels in liver, muscle, and intestine. There were significant differences in growth rate and nutrient retention among the families. Mitochondrial enzymatic complex activities (I-V) in the tissues were all lower in family C. Four of the five genes were down-regulated in the liver and up-regulated in the muscle for the fast growing family C. There were significant differences between diets for some mitochondrial respiratory chain enzyme activities and gene expression levels. Significant diet×family interactions were observed for some enzyme activities and gene expression levels. Changes in mitochondrial respiratory chain enzyme activities and gene expression levels provide insight into the cellular mechanisms of fish with differences in growth rate and feed efficiency. Results also suggest that genotype×diet interactions should be accounted for when considering strategies for using mitochondrial function as a criteria in channel catfish selection programs for improved growth performance characteristics.