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Muscle growth mechanisms in response to isoenergetic changes in dietary non-protein energy source at low and high protein levels in juvenile rainbow trout
Alami-Durante, Hélène ; Cluzeaud, Marianne ; Bazin, Didier ; Schrama, Johan W. ; Saravanan, Subramanian ; Geurden, Inge - \ 2019
Comparative Biochemistry and Physiology. A, Molecular and Integrative Physiology 230 (2019). - ISSN 1095-6433 - p. 91 - 99.
This study investigates muscle growth mechanisms in juvenile rainbow trout in response to isoenergetic changes in dietary non-protein energy (NPE) source (F, fat vs. C, carbohydrates) at two levels of digestible protein to digestible energy (DP/DE) ratio. Fish (initial weight 32.4 g) were fed four diets having similar DE levels (~18 kJ g−1) with a high (HP/E~26 mg kJ−1) vs. low (LP/E~14 mg kJ−1) DP/DE ratio using F or C as major NPE source (7 week-experiment). The lowering of dietary DP/DE ratio increased myoblast determination protein 1a (myod1a) and decreased myostatin 1b (mstn1b) and cathepsin D (ctsd) muscle mRNA levels. The isoenergetic change in dietary NPE from F to C decreased myod1a and proliferative cell nuclear antigen (pcna) muscle mRNA levels. An interaction between DP/DE ratio and NPE source was observed in muscle transcript levels of myogenic factor 6 (mrf4/myf6), fast myosin heavy chain (fmhc) and fast myosin light chain 2 (fmlc2). White muscle total cross-sectional area decreased at low dietary DP/DE ratio and also when NPE source changed from F to C, linked i) to a decreased total number of white muscle fibres, indicating that low dietary DP/DE restricted muscle hyperplasia and that dietary carbohydrate were less efficiently used than fat to sustain muscle hyperplasia, and ii) to decreased percentage of large muscle fibres, indicating limited fibre hypertrophy. Not only the DP level or the DP/DE ratio, but also the isoenergetic change in dietary NPE source (fat vs carbohydrates) thus appears as a potent regulator of muscle hyperplasia and hypertrophy.
Effects of dietary protein level and non-protein energy source on muscle growth mechanisms in rainbow trout (Oncorhynchus mykiss) juveniles
Alami-Durante, H. ; Cluzeaud, M. ; Bazin, D. ; Schrama, J.W. ; Subramanian, S. ; Geurden, Inge - \ 2018
- 1 p.
Feed intake and oxygen consumption in fish
Subramanian, S. - \ 2013
Wageningen University. Promotor(en): Johan Verreth, co-promotor(en): Johan Schrama; S.J. Kaushik; I. Geurden. - Wageningen : Wageningen UR - ISBN 9789461737571 - 163
vissen - voeropname - zuurstofconsumptie - energieopname - voer - samenstelling - energiemetabolisme - macronutriënten - visvoeding - visteelt - aquacultuur - voedingsfysiologie - fishes - feed intake - oxygen consumption - energy intake - feeds - composition - energy metabolism - macronutrients - fish feeding - fish culture - aquaculture - nutrition physiology

In fish, the voluntary feed intake is influenced by dietary, environmental and/or physiological factors. It is well known that under hypoxia the concentration of oxygen in the water (DO) determines the feed intake of fish. However at non-limiting water DO levels (normoxia), several other mechanisms might play a role in feed intake regulation. Under hypoxia feed intake and oxygen consumption are interrelated. In this thesis we proposed the ‘oxystatic’ concept of feed intake regulation, which states that even at normoxia and in the absence of other constraints, the long term (weeks) voluntary feed intake of fish can be constrained by a set-point value of oxygen consumption. Dietary macronutrient composition affects the ‘dietary oxygen demand’ (i.e., amount of O2 consumed per unit of feed). This oxystatic concept implies that fish fed to satiation with diets differing in ‘dietary oxygen demand’ (mg O2/ g or kJ feed) will have a different digestible energy intake but a similar oxygen consumption. The validity of the oxystatic concept was assessed in two species, Nile tilapia and rainbow trout. These fish were fed diets which had large contrasts in nutrient composition (i.e., protein to energy ratio; type of the non-protein energy source (starch vs. fat); amino acid composition) in order to create contrasts in dietary oxygen demand. In all conducted studies with both species, the digestible energy intake was affected by the diet composition. However, in some studies oxygen consumption was similar and in others it differed between the diets, which respectively supports and contradicts the oxystatic concept. In all studies with both species, the digestible energy intake of tilapia and trout was negatively related to dietary oxygen demand and positively related to efficiency of oxygen utilization for energy retention. Furthermore it was observed in tilapia that the within-day variation in feed intake was affected by dietary macronutrient composition. The variation in within-day feed intake was related to pre-feeding oxygen levels. Based on the combined results, it is suggested that even at normoxia voluntary feed intake in fish is limited/determined by oxygen consumption and/or the oxidative metabolism. Overall, the oxystatic concept appears to be valid for certain conditions, but its generic application remains questionable. Yet, the oxystatic concept enables the combination of dietary, environmental and fish factors into one concept. Further it provides a conceptual insight for better understanding of feed intake regulation in fish.

Voluntary Feed Intake in Rainbow Trout Is Regulated by Diet-Induced Differences in Oxygen Use
Subramanian, S. ; Geurden, I. ; Figueiredo-Silva, A.C. ; Kaushik, S.J. ; Verreth, J.A.J. ; Schrama, J.W. - \ 2013
The Journal of Nutrition 143 (2013)6. - ISSN 0022-3166 - p. 781 - 787.
tilapia oreochromis-niloticus - oncorhynchus-mykiss - food-intake - digestible energy - nile tilapia - induced thermogenesis - lipid level - dicentrarchus-labrax - growth-performance - self-feeders
This study investigated the hypothesis that the voluntary feed intake in fish is regulated by diet-induced differences in oxygen use. Four diets were prepared with a similar digestible protein:digestible energy ratio (18 mg/kJ), but which differed in the composition of nonprotein energy source. This replacement of fat (F) by starch (S) was intended to create a diet-induced difference in oxygen use (per unit of feed): diets F30-S70, F50-S50, F65-S35, and F80-S20 with digestible fat providing 28, 49, 65, and 81% of the nonprotein digestible energy (NPDE), respectively. Each diet was fed to satiation to triplicate groups of 20 rainbow trout for 6 wk. As expected, diet-induced oxygen use decreased linearly (R(2) = 0.89; P <0.001) with increasing NPDE as fat. The digestible and metabolizable energy intakes of trout slightly increased with increasing NPDE as fat (i.e., decreasing starch content) (R(2) = 0.30, P = 0.08; and R(2) = 0.34, P = 0.05, respectively). Oxygen consumption of trout fed to satiation declined with increasing dietary NPDE as fat (R(2) = 0.48; P = 0.01). The inverse relation between digestible energy intake of trout and the diet-induced oxygen use (R(2) = 0.33; P = 0.05) suggests a possible role of diet-induced oxygen use in feed intake regulation as shown by the replacement of dietary fat by starch.
Dietary electrolyte balance affects the nutrient digestibility and maintenance energy expenditure of Nile tilapia
Subramanian, S. ; Geurden, I. ; Orozco, Z.G.A. ; Kaushik, S.J. ; Verreth, J.A.J. ; Schrama, J.W. - \ 2013
The British journal of nutrition 110 (2013). - ISSN 0007-1145 - p. 1948 - 1957.
acid-base-balance - cation-anion difference - water rainbow-trout - juvenile african catfish - clarias-gariepinus burchell - fresh-water - alkaline tide - oreochromis-niloticus - gastrointestinal-tract - oncorhynchus-mykiss
Acid–base disturbances caused by environmental factors and physiological events including feeding have been well documented in several fish species, but little is known about the impact of dietary electrolyte balance (dEB). In the present study, we investigated the effect of feeding diets differing in dEB ( - 100, 200, 500 or 800 mEq/kg diet) on the growth, nutrient digestibility and energy balance of Nile tilapia. After 5 weeks on the test diet, the growth of the fish was linearly affected by the dEB levels (P<0·001), with the lowest growth being observed in the fish fed the 800 dEB diet. The apparent digestibility coefficient (ADC) of fat was unaffected by dEB, whereas the ADC of DM and protein were curvilinearly related to the dEB levels, being lowest and highest in the 200 and 800 dEB diets, respectively. Stomach chyme pH at 3 h after feeding was linearly related to the dEB levels (P<0·05). At the same time, blood pH of the heart (P<0·05) and caudal vein (P<0·01) was curvilinearly related to the dEB levels, suggesting the influence of dEB on postprandial metabolic alkalosis. Consequently, maintenance energy expenditure (MEm) was curvilinearly related to the dEB levels (P<0·001), being 54 % higher in the 800 dEB group (88 kJ/kg0·8 per d) than in the 200 dEB group (57 kJ/kg0·8 per d). These results suggest that varying dEB levels in a diet have both positive and negative effects on fish. On the one hand, they improve nutrient digestibility; on the other hand, they challenge the acid–base homeostasis (pH) of fish, causing an increase in MEm, and thereby reduce the energy required for growth.
Oxygen Consumption Constrains Food Intake in Fish Fed Diets Varying in Essential Amino Acid Composition
Subramanian, S. ; Geurden, I. ; Figueiredo-Silva, A.C. ; Nusantoro, S. ; Kaushik, S.J. ; Verreth, J.A.J. ; Schrama, J.W. - \ 2013
PLoS ONE 8 (2013)8. - ISSN 1932-6203 - 7 p.
trout oncorhynchus-mykiss - european sea bass - rainbow-trout - dissolved-oxygen - nile tilapia - feed-intake - oreochromis-niloticus - salmo-gairdneri - self-selection - protein
Compromisation of food intake when confronted with diets deficient in essential amino acids is a common response of fish and other animals, but the underlying physiological factors are poorly understood. We hypothesize that oxygen consumption of fish is a possible physiological factor constraining food intake. To verify, we assessed the food intake and oxygen consumption of rainbow trout fed to satiation with diets which differed in essential amino acid (methionine and lysine) compositions: a balanced vs. an imbalanced amino acid diet. Both diets were tested at two water oxygen levels: hypoxia vs. normoxia. Trout consumed 29% less food under hypoxia compared to normoxia (p0.05). This difference in food intake between diets under normoxia together with the identical oxygen consumption supports the hypothesis that food intake in fish can be constrained by a set-point value of oxygen consumption, as seen here on a six-week time scale.
A comparative study of the metabolic response in rainbow trout and Nile tilapia to changes in dietary macronutrient composition
Figueiredo-Silva, A.C. ; Subramanian, S. ; Schrama, J.W. ; Panserat, S. ; Kaushik, S.J. ; Geurden, I. - \ 2013
The British journal of nutrition 109 (2013)5. - ISSN 0007-1145 - p. 816 - 826.
x oreochromis-aureus - european sea-bass - oncorhynchus-mykiss - body-composition - lipid level - hepatic lipogenesis - growth-performance - enzyme-activities - glucose-6-phosphatase expression - glucose-metabolism
Metabolic mechanisms underlying the divergent response of rainbow trout (Oncorhynchus mykiss) and Nile tilapia (Oreochromis niloticus) to changes in dietary macronutrient composition were assessed. Fish were fed one of four isoenergetic diets having a digestible protein-to-digestible energy (DP:DE) ratio above or below the optimal DP:DE ratio for both species. At each DP:DE ratio, fat was substituted by an isoenergetic amount of digestible starch as the non-protein energy source (NPE). Dietary DP:DE ratio did not affect growth and only slightly lowered protein gains in tilapia. In rainbow trout fed diets with low DP:DE ratios, particularly with starch as the major NPE source, growth and protein utilisation were highly reduced, underlining the importance of NPE source in this species. We also observed species-specific responses of enzymes involved in amino acid catabolism, lipogenesis and gluconeogenesis to dietary factors. Amino acid transdeamination enzyme activities were reduced by a low dietary DP:DE ratio in both species and in tilapia also by the substitution of fat by starch as the NPE source. Such decreased amino acid catabolism at high starch intakes, however, did not lead to improved protein retention. Our data further suggest that a combination of increased lipogenic and decreased gluconeogenic enzyme activities accounts for the better use of carbohydrates and to the improved glycaemia control in tilapia compared with rainbow tront fed starch-enriched diets with low DP:DE ratio.
Dietary protein level and non-protein energy sources interact to regulate muscle cellularity in juvenile rainbow trout (Oncorhynchus mykiss)
Alami-Durante, H. ; Bazin, D. ; Cluzeaud, M. ; Subramanian, S. ; Schrama, J.W. ; Kaushik, S.J. ; Geurden, I. - \ 2012
Food intake and intermediary metabolism-related gene expression in rainbow trout fed at or below lysine and methionine requirements
Figueiredo-Silva, A.C. ; Kaushik, S.J. ; Subramanian, S. ; Schrama, J.W. ; Geurden, I. - \ 2012
Relation between essential amino acid deficiency, oxygen use, and feed intake in rainbow trout
Subramanian, S. ; Geurden, I. ; Figueiredo-Silva, A.C. ; Kaushik, S.J. ; Verreth, J.A.J. ; Schrama, J.W. - \ 2012
Relation between essential amino acid deficiency, oxygen use, and feed intake in rainbow trout
Subramanian, S. ; Geurden, I. ; Figueiredo-Silva, A.C. ; Kaushik, S.J. ; Verreth, J.A.J. ; Schrama, J.W. - \ 2012
Macronutrient-induced differences in food intake relate with hepatic oxidative metabolism and hypothalamic regulatory neuropeptides in rainbow trout (Oncorhynchus mykiss)
Figueiredo-Silva, A.C. ; Subramanian, S. ; Schrama, J.W. ; Kaushik, S.J. ; Geurden, I. - \ 2012
Physiology and Behavior 106 (2012)4. - ISSN 0031-9384 - p. 499 - 505.
fatty-acid oxidation - gene-expression - uncoupling protein-2 - glucose-oxidation - increases - goldfish - brain - fish - npy - stimulation
This study examines how dietary macronutrient-induced changes in voluntary food intake (FI) relate to changes in markers of hepatic oxidative metabolism and in the expression of FI regulatory neuropeptides in a teleost model, the rainbow trout. Rainbow trout were fed for 6 weeks with one of four iso-energetic diets (2 × 2 factorial design), containing either a high (HP, ~ 500 g·kg- 1 DM) or a low (LP, ~ 250 g·kg- 1 DM) protein level (PL) with, at each PL, fat (diets HP-F and LP-F) being substituted by an iso-energetic amount of gelatinized corn starch (diets HP-St and LP-St) as non-protein energy source (ES). Irrespective of the dietary PL, FI (g·kg- 0.8·d- 1) and digestible energy intake (DEI, kJ·kg- 0.8·d- 1) were significantly (P <0.05) reduced by the iso-energetic replacement of fat by starch as non-protein ES. Interestingly, trout fed these St-diets had higher gene expression of markers of hepatic oxidative phosphorylation (OxPhos), i.e. ubiquinol-cytochrome c reductase subunit 2 (UCR2) and cytochrome oxidase subunit 4 (COX4) and of aerobic oxidative capacity (CS, citrate synthase), which paralleled glucokinase (GK) transcription. This positive relation suggests that glucose phosphorylation and markers of mitochondrial OxPhos are linked at the hepatic level and possibly triggered the observed reduction in FI. Moreover, trout displaying the reduced FI had higher cocaine amphetamine regulator transcript (CART) mRNA in hypothalamus, whereas neuropeptide Y (NPY) mRNA did not follow the macronutrient-induced changes in FI. Further studies are needed to unravel the mechanisms by which diet-induced changes in hepatic metabolism inform central feeding centers involved in the regulation of FI in fish.
Eating more or eating less: Role of oxygen in fish
Subramanian, S. ; Geurden, I. ; Verreth, J.A.J. ; Schrama, J.W. - \ 2012
Dietary nutrient composition affects digestible energy utilisation for growth: a study on Nile tilapia (Oreochromis niloticus) and a literature comparison across fish species
Schrama, J.W. ; Subramanian, S. ; Geurden, I. ; Heinsbroek, L.T.N. ; Kaushik, S.J. ; Verreth, J.A.J. - \ 2012
The British journal of nutrition 108 (2012)2. - ISSN 0007-1145 - p. 277 - 289.
trout oncorhynchus-mykiss - ctenopharyngodon-idella val - bass dicentrarchus-labrax - rainbow-trout - feeding level - utilization efficiency - anguilla-anguilla - european eel - growing pigs - grass carp
The effect of the type of non-protein energy (NPE) on energy utilisation in Nile tilapia was studied, focusing on digestible energy utilisation for growth (kgDE). Furthermore, literature data on kgDE across fish species were analysed in order to evaluate the effect of dietary macronutrient composition. A total of twelve groups of fish were assigned in a 2 × 2 factorial design: two diets (‘fat’ v. ‘starch’) and two feeding levels (‘low’ v. ‘high’). In the ‘fat’-diet, 125 g fish oil and in the ‘starch’-diet 300 g maize starch were added to 875 g of an identical basal mixture. Fish were fed restrictively one of two ration levels (‘low’ or ‘high’) for estimating kgDE. Nutrient digestibility, N and energy balances were measured. For estimating kgDE, data of the present study were combined with previous data of Nile tilapia fed similar diets to satiation. The type of NPE affected kgDE (0·561 and 0·663 with the ‘starch’ and ‘fat’-diets, respectively; P <0·001). Across fish species, literature values of kgDE range from 0·31 to 0·82. Variability in kgDE was related to dietary macronutrient composition, the trophic level of the fish species and the composition of growth (fat:protein gain ratio). The across-species comparison suggested that the relationships of kgDE with trophic level and with growth composition were predominantly induced by dietary macronutrient composition. Reported kgDE values increased linearly with increasing dietary fat content and decreasing dietary carbohydrate content. In contrast, kgDE related curvilinearly to dietary crude protein content. In conclusion, energy utilisation for growth is influenced by dietary macronutrient composition.
Constraints on Energy Intake in Fish: The Link between Diet Composition, Energy Metabolism, and Energy Intake in Rainbow Trout
Subramanian, S. ; Schrama, J.W. ; Figueiredo-Silva, A.C. ; Kaushik, S.J. ; Verreth, J.A.J. ; Geurden, I. - \ 2012
PLoS ONE 7 (2012)4. - ISSN 1932-6203
european sea-bass - voluntary feed-intake - salmon salmo-salar - oncorhynchus-mykiss - food-intake - digestible energy - growing-pigs - utilization efficiency - oreochromis-niloticus - dicentrarchus-labrax
The hypothesis was tested that fish fed to satiation with iso-energetic diets differing in macronutrient composition will have different digestible energy intakes (DEI) but similar total heat production. Four iso-energetic diets (2×2 factorial design) were formulated having a contrast in i) the ratio of protein to energy (P/E): high (HP/E) vs. low (LP/E) and ii) the type of non-protein energy (NPE) source: fat vs. carbohydrate which were iso-energetically exchanged. Triplicate groups (35 fish/tank) of rainbow trout were hand-fed each diet twice daily to satiation for 6 weeks under non-limiting water oxygen conditions. Feed intake (FI), DEI (kJ kg-0.8 d-1) and growth (g kg-0.8 d-1) of trout were affected by the interaction between P/E ratio and NPE source of the diet (P0.05). Our data suggest that the control of DEI in trout might be a function of heat production, which in turn might reflect a physiological limit related with oxidative metabolism.
Control of voluntary feed intake in fish: a role for dietary oxygen demand in Nile tilapia (Oreochromis niloticus) fed diets with different macronutrient profiles
Subramanian, S. ; Geurden, I. ; Figueiredo-Silva, A.C. ; Kaushik, S.J. ; Haidar, M.N. ; Verreth, J.A.J. ; Schrama, J.W. - \ 2012
The British journal of nutrition 108 (2012)8. - ISSN 0007-1145 - p. 1519 - 1529.
trout oncorhynchus-mykiss - bass dicentrarchus-labrax - salmon salmo-salar - rainbow-trout - energy-utilization - food-intake - body-composition - dynamic action - gadus-morhua - lipid-levels
It has been hypothesised that, at non-limiting water oxygen conditions, voluntary feed intake (FI) in fish is limited by the maximal physiological capacity of oxygen use (i.e. an ‘oxystatic control of FI in fish’). This implies that fish will adjust FI when fed diets differing in oxygen demand, resulting in identical oxygen consumption. Therefore, FI, digestible energy (DE) intake, energy balance and oxygen consumption were monitored at non-limiting water oxygen conditions in Nile tilapia fed diets with contrasting macronutrient composition. Diets were formulated in a 2 × 2 factorial design in order to create contrasts in oxygen demand: two ratios of digestible protein (DP):DE (‘high’ v. ‘low’); and a contrast in the type of non-protein energy source (‘starch’ v. ‘fat’). Triplicate groups of tilapia were fed each diet twice daily to satiation for 48 d. FI (g DM/kg0·8 per d) was significantly lower (9·5 %) in tilapia fed the starch diets relative to the fat diets. The DP:DE ratio affected DE intakes (P <0·05), being 11 % lower with ‘high’ than with ‘low’ DP:DE ratio diets, which was in line with the 11·9 % higher oxygen demand of these diets. Indeed, DE intakes of fish showed an inverse linear relationship with dietary oxygen demand (DOD; R 2 0·81, P <0·001). As hypothesised (‘oxystatic’ theory), oxygen consumption of fish was identical among three out of the four diets. Altogether, these results demonstrate the involvement of metabolic oxygen use and DOD in the control of FI in tilapia.
Role of metabolic oxygen use in control of feed intake in fish, Nile tilapia
Subramanian, S. ; Geurden, I. ; Verreth, J.A.J. ; Schrama, J.W. - \ 2011
Different dietary energy-substrates affect food intake in rainbow trout through the regulation of hepatic oxidative metabolism and hypothalamic regulatory peptides
Figueiredo-Silva, A.C. ; Subramanian, S. ; Kaushik, S. ; Schrama, J.W. ; Geurden, I. - \ 2011
Metabolic response of rainbow trout and tilapia to changes in dietary non-protein source and protein levels
Figueiredo-Silva, A.C. ; Subramanian, S. ; Schrama, J.W. ; Kaushik, S. ; Geurden, I. - \ 2011
Dietary oxygen demand affects energy intake in rainbow trout
Subramanian, S. ; Geurden, I. ; Cláudia Figueiredo-Silva, A. ; Verreth, J.A.J. ; Kaushik, S.J. ; Schrama, J.W. - \ 2011
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