Aquaculture 488 (2018) 1–8

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Aquaculture

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Programming of the in rainbow trout juveniles after T chronic at hatching stage combined with a high dietary : Protein ratios intake at first-feeding

Huihua Hua,b,c,1, Jingwei Liua,1, Elisabeth Plagnes-Juana, Alexandre Hermana, Isabelle Leguend, ⁎ Lionel Goardone, Inge Geurdena, Stéphane Panserata, Lucie Marandela, a INRA, Univ Pau & Pays Adour, UMR 1419, Nutrition, Metabolism and Aquaculture, Saint Pée sur Nivelle, F-64310, France b State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, The Chinese Academy of Sciences, Wuhan 430072, China c Graduate University of the Chinese Academy of Sciences, Beijing 100049, China d INRA, UR1037 LPGP, Campus de Beaulieu, F-35000 Rennes, France e INRA, UE937 Pisciculture expérimentale des Monts d'Arrée, 29450 Sizun, France

ARTICLE INFO ABSTRACT

Keywords: It is well known that change in environmental parameters experienced during early life can have profound effect on the metabolism of individuals later in life. The purpose of the present study was to evaluate the impact of a expression −1 chronic hypoxic stimulus (15 days, 50% dissolved O2, 5.0 mg·L ) applied at hatching ( history) alone or Growth combined with a 60% high carbohydrate (HC) dietary stimulus (8 days) applied at first-feeding (dietary history) on Metabolic programming growth performance and glucose metabolism of juvenile trout. The effectiveness of the hypoxic and the HC dietary stimuli were verified by monitoring the modulation in mRNA levels of oxygen-sensitive and dietary carbohydrate- sensitive , respectively. At juvenile stage (28 weeks after first-feeding), neither dietary history nor oxygen history had long-term effect on growth performance. These juveniles were then subjected to a 5 days challenge test with a 30% carbohydrate . Our data showed that mRNA levels of some glucose transport-related genes in and muscle, and plasma were down-regulated in fish which were exposed to hypoxia during early life. Regarding to the effect of dietary history, the mRNA level of muscular pfkmaa was observably increased in fish previously subjected to the HC dietary stimulus. In summary, the present study indicated that a chronic hypoxic stimulus applied at hatching alone or combined with a high carbohydrate stimulus at first-feeding can affect plasma triglycerides level and glucose metabolism-related genes in juvenile trout.

1. Introduction and which may persist later in life in the absence of the environmental stimulus that initiated them (George et al., 2012; Kongsted et al., 2014; Environmental alterations (nutritional or non-nutritional) that are Lucas, 1998; Patel and Srinivasan, 2002). experienced during early life can lead to profound changes in meta- In aquaculture, the concept of metabolic programming has attracted bolism and of living organisms, which is termed metabolic more and more attention in recent years mostly in the context of the programming (when modifying metabolism) (Lucas, 1998). Long- replacement of fish meal by alternative ingredients (Fang et al., 2014; lasting modification in patterns is one of the most Geurden et al., 2007; Geurden et al., 2014; Gong et al., 2015; Rocha important biological mechanisms described in such case of adaptions et al., 2014, 2015) and more particularly by dietary carbohydrate.

Abbreviations: gck, glucokinase; , (muscle); , phosphofructokinase (liver); pkm, pyruvate (muscle); , (liver and red blood ); pck, phosphoenol pyruvate carboxykinases (cytosolic pck1 and mitochondrial pck2); fbp, 1, 6-bisphosphatase; g6pc, glucose 6-phosphatase; glut1/slc2a1, solute carrier family 2 (facilitated glucose transporter), member 1; glut2/slc2a2, solute carrier family 2 (facilitated glucose transporter), member 2; /slc2a4, solute carrier family 2 (facilitated glucose transporter), member 4; slc16a3, solute carrier family 16 (monocarboxylate transporter), member 3; egln3, egl-9 family hypoxia-inducible factor 3; hif1a, hypoxia inducible factor 1 alpha; pdk1, pyruvate dehydrogenase kinase 1; ldha, A; NEFA, non-esterified ⁎ Corresponding author. E-mail addresses: [email protected] (H. Hu), [email protected] (J. Liu), [email protected] (E. Plagnes-Juan), [email protected] (A. Herman), [email protected] (I. Leguen), [email protected] (L. Goardon), [email protected] (I. Geurden), [email protected] (S. Panserat), [email protected] (L. Marandel). 1 These authors contributed equally to this work. https://doi.org/10.1016/j.aquaculture.2018.01.015 Received 1 September 2017; Received in revised form 8 January 2018; Accepted 10 January 2018 Available online 12 January 2018 0044-8486/ © 2018 Elsevier B.V. All rights reserved. H. Hu et al. Aquaculture 488 (2018) 1–8

Indeed, dietary carbohydrates are promising candidates for partial re- the programming effect of a moderate chronic hypoxic stimulus (50% of −1 placement of fish meal due to their economical production in Europe O2, 5.0 mg·L , during 15 days) applied at hatching stage (312°D) alone and their “sparing effect” for protein through saving this precious nu- or combined with a 8-days high carbohydrate dietary stimulus applied trient for growth purpose instead of utilising as an energy source. at first-feeding (536°D) on growth performance, plasmatic metabolites However, carnivorous fish, such as the first species produced in Europe, and glucose metabolism in trout juveniles. the rainbow trout (Oncorhynchus mykiss), is considered as a “glucose- intolerant” species presenting a postprandial hyperglycaemia and 2. Materials and method growth retardation when fed, in the long term, a diet containing more than 20% carbohydrates (Polakof et al., 2012; Wilson, 1994). In this 2.1. Ethical issues and approval context, previous studies on rainbow trout have proved the possibility of using metabolic programming strategy to modify the glucose meta- Investigations were conducted according to the guiding principles for bolism in this fish (Geurden et al., 2007; Geurden et al., 2014; Liu et al., the use and care of laboratory animals and in compliance with French 2017a; Liu et al., 2017b) and tried to overcome the metabolic (nutri- and European regulations on animal welfare (Décret 2001–464, 29 May tional) bottlenecks of poor use of dietary glucose as an energy source. 2001 and Directive 2010/63/EU, respectively). This protocol and the First investigations were only based on a strict nutritional stimulus project as a whole were approved by the French National Consultative (Geurden et al., 2007; Geurden et al., 2014) which had no significant Ethics Committee (reference numbers 2,016,110,211,489,713, programming effect on the glucose metabolism of the most important 2,015,112,018,112,159 and 201,511,201,756,973). metabolic organ, the liver. The programming conditions were then re- viewed by Liu and collaborators (Liu et al., 2017a; Liu et al., 2017b) 2.2. Experimental design and sampling including an early non-nutritional stimulus based on an acute exposure ff to hypoxia, an environmental parameter known to a ect hepatic glu- were obtained from spawns in La Peima, INRA facilities, fi cose metabolism in aerobic organisms including sh (Osumek et al., France. The experiment design was shown in Fig. 1. From fertilisation 2014; Palmer and Clegg, 2014; Rissanen et al., 2006; Sappal et al., to just before first-feeding (536°D) fish were reared at 12 °C. After 2016; Zhong and Mostoslavsky, 2010). Indeed, under hypoxic condi- hatching (312°D), trout alevins were subjected to either a 15-days tions, Hif1a sub-unit integrity is maintained by the inhibition of prolyl −1 chronic hypoxic stimulus (50% of O2, between 4 and 5 mg·L Fig. 1)or − hydroxylase (which co-factor is O2), and able to form a com- kept under normoxic (between 10 and 11 mg·L 1, dissolved oxygen) plex with Hif1b which in turn act as a factor to regulate conditions (Fig. 1, Stimulus 1). Each condition was conducted in tri- glucose-metabolism related genes. Although some glucose metabolism plicate tanks. Hypoxia was obtained and maintained by supplied hy- related genes were affected in the long-term in these studies, the effect poxia tanks with N2-bubbled water. Oxygen levels were continuously of acute hypoxia remained however moderate and did not modify measured in 2 tanks (1 normoxia and 1 hypoxia) (Hach, Germany) and physiological parameters such as glycaemia or growth. In this latter check several times per day in all tanks. This first stimulus will be re- work, the selection for the stimulus focused on acute hypoxia because ferred as “oxygen history” thereafter. During the hypoxic stimulus, the rainbow trout is considered as an oxygen sensitive teleost species mortality of fish was noted every day to calculate the survival rate. (Gesser, 1977; Miller et al., 2008). However, under hypoxia, a complex Besides, 2 alevins per tank were sampled (anaesthetised in a − − of physiological and biochemical alterations take place and vary de- 0.024 mL·L 1 isoeugenol bath and then killed by a bath at 0.1 mL·L 1) pending on the hypoxia level and the duration of the exposure (Bristow at the last hour of this hypoxic stimulus to ensure the efficiency of the and Hill, 2008; Deldicque and Francaux, 2013; Liu et al., 2017b). Al- hypoxic stimulus (Fig. 1, Sampling 1). Just before first-feeding, alevins ff though there is limited information of long-term programming e ect of were transferred to the INRA experimental facilities of Lees-Athas, early chronic hypoxia exposure on glucose metabolism in rainbow France, and reared at 8 °C (with a period of adaptation). At the time of trout, a previous study in sea bass, an oxygen-sensitive teleost first-feeding (536°D), fish were fed with either a high carbohydrate (Pichavant et al., 2003; Terova et al., 2009), demonstrated that chronic (HC, 60%) diet or a no carbohydrate (NC) diet (Table 1) during 8 days hypoxic exposure induced lasting alterations in the mRNA level of (Fig. 1, Stimulus 2). This stimulus was referred as “dietary history” glucose metabolism-related genes in juveniles (Vanderplancke et al., thereafter. Each treatment was performed in triplicate of tanks and 2 2015). In this sense, it can be hypothesised that chronic hypoxia ex- fish per tank were sampled 3 h after last meal (Fig. 1, Sampling 2). After fi posure during early development may lead to long-term modi cation in this second stimulus, all fish were growth during 27 weeks (Fig. 1, glucose metabolism in trout juveniles. Growth trial) with a commercial diet (Skrettring, France). Nine weeks In this context, the present study was thus designed to investigate after first feeding, fish were transferred to INRA experimental facilities

After hatching First feeding Challenge Fig. 1. - Experimental design. Hypoxic stimulus (50% of −1 (Alevins 312 D) (Alevins 536 D) (Juveniles) O2, 5.0 mg·L ) was applied to rainbow trout for 15 days at the alevin stage (312°D) then the fish were fed either a high Stimulus1 Stimulus2 carbohydrate (HC) or a no carbohydrate (NC) diet at first- Oxygen Nutrition feeding (536°D). After a 27 weeks growth trial, fish were NC diet (0% CHO) subjected to a 5 days challenge test with 30% carbohydrate Normoxia diet. 1 10.0 mg·l O2 HC diet (60% CHO) Growth trial Challenge test Commercial diet 30% CHO

Hypoxia NC diet (0% CHO)

1 5 mg·l O2 (50%) HC diet (60% CHO)

15 days 8 days 27 weeks 5 days

Sampling 1 Sampling 2 Sampling 3 Last hour of hypoxia 3h after last meal 6 h after last meal

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