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Poster De Conférence Année : 2021

A parental low protein diet did not affect growth but modulate lipid metabolism in rainbow trout

Résumé

Introduction Toward a sustainable aquaculture, it is essential to continue to reduce the use of marine ingredients. Plant-derived carbohydrates are considered a promising substitute for protein contained in fishmeal because of their inexpensive price and most readily available amounts (Prabhu et al., 2017). Even though carbohydrates are considered to be poorly utilized by fish of high trophic levels such as rainbow trout (Oncorhynchus mykiss), recent studies have suggested that rainbow trout broodstock are able to grow and reproduce with a low protein/high carbohydrates diet (Callet et al., 2020). Besides, it is now recognized that nutritional insult received during the prenatal period could have a long-term effect on individual phenotype and metabolism. In mammals, both a paternal and a maternal low protein (LP) diets affect their offspring metabolism, growth and survival (Guo et al., 2020). However, such effects have not been widely studied in teleost fish. Before increasing the proportion of plant-derived carbohydrates in broodstock diet in farming condition, it is necessary to test the effects of such a parental diet on their offspring. As the effects of nutritional programming could be revealed during period of stress, we investigate the effects of such diet when their offspring were fed with a complete plant-based diet. Material and methods Two-year old male and female trout were fed either a control diet with a high protein content (NC, 63.89% protein and 0% carbohydrate) or a diet containing a lower proportion of protein but a higher carbohydrate content (LP-HC, 42,96% protein and 35% carbohydrate) for an entire reproductive cycle for females and 5 months for males. Crossed-fertilizations were carried out in order to obtain 4 groups of fish: NN fish from both males and females fed the control diet, HN fish from only females fed the LP-HC diet and males fed the control NC diet; NH fish from only males fed the LP-HC diet and females fed the NC diet; and HH fish from both parents were fed the LP-HC diet. After 6 month, fish were challenged during a 3 months trial with a complete plant-based diet. Growth parameters were monitored to reveal any effect on offspring phenotypes. Comparisons of hepatic global methylation and hepatic transcriptomes were performed to investigate the effect of a LP diet on offspring metabolism. Then, qPCR analyses were carried out to investigate specific pathways revealed by the transcriptomic analyses. Results and discussion At the end of the trial, no significant differences were observed on the final body weight (with the weight of NN 283.29 ± 6.25 g, NH 323.37 ± 20.05 g, HN 319.33 ± 4.91g, and HH 303.99 ± 11.28 g), regardless of the parental nutritional history. Even though fish phenotype were not affected, the parental LP-HC diet strongly altered their offspring hepatic metabolism. First, the global DNA methylation in liver was modified in HN and HH fish, revealing a strong effect of the maternal LP-HC diet; effect which were increased by the male LP-HC diet. Transcriptomic analyses did not detect differences between control fish (NN) and HN or NH fish. The paternal and the maternal LP-HC diet only did not highly alter hepatic metabolism. Hepatic transcriptomes of HH fish were however highly affected, suggesting the existence of the synergistic effect of the maternal and the paternal LP-HC diet. Of particular interest, expression of some genes related to lipid and cholesterol metabolism were affected by the paternal LP-HC diet. These results are consistent with result obtained in mammals (Carone et al., 2010). Interestingly, the cholesterol biosynthesis pathway known to be up-regulated when fish are fed with a complete plant-based diet (Zhu et al., 2020), was further enhanced by the paternal LP-HC diet. The de novo lipid lipogenesis pathways were also affected by the parental LP-HC diet (either maternal or paternal or both) and lead to an increased in triglycerides levels in plasma of HN and HH fish and an increased in whole body lipid content in NH and HH fish. Finally and more importantly, the biogenesis of polyunsaturated fatty acids (PUFA), pathway known to be enhanced when rainbow trout are fed a complete plant-based diet, were also increased by the parental LP-HC diet. Interestingly, similar effects of nutritional programming through broodstock have already been described in gilthead sea bream (Izquierdo et al., 2015). Together, the results suggest that plant-derived carbohydrates could replace fishmeal in trout broodstock diet as no strong adverse effects on their offspring phenotype were detected, in contrast to results typically observed in mammals. In aquaculture species, it has been suggested that nutritional programming could be used as a strategy to improve fish performances. Even though, a LP diet did not significantly improve growth in rainbow trout, such nutritional programming could modulate PUFA biogenesis which could be of particular interest to improve fish ability to use diets devoid of marine ingredients. References Callet, T.; Hu, H.; Larroquet, L.; Surget, A.; Liu, J.; Plagnes-Juan, E.; Maunas, P.; Turonnet, N.; Mennigen, J. A.; Bobe, J. & others. Exploring the impact of a low-protein high-carbohydrate diet in mature broodstock of a glucose-intolerant teleost, the rainbow trout. Frontiers in physiology, Frontiers, 2020, 11, 303 Carone, B. R.; Fauquier, L.; Habib, N.; Shea, J. M.; Hart, C. E.; Li, R.; Bock, C.; Li, C.; Gu, H.; Zamore, P. D. & others. Paternally induced transgenerational environmental reprogramming of metabolic gene expression in mammals. Cell, Elsevier, 2010, 143, 1084-1096 Guo, T.; Luo, F. & Lin, Q. You are affected by what your parents eat: Diet, epigenetics, transgeneration and intergeneration. Trends in Food Science & Technology, Elsevier, 2020, 100, 248-261 Izquierdo, M.; Turkmen, S.; Montero, D.; Zamorano, M.; Afonso, J.; Karalazos, V. & Fernández-Palacios, H. Nutritional programming through broodstock diets to improve utilization of very low fishmeal and fish oil diets in gilthead sea bream. Aquaculture, Elsevier, 2015, 449, 18-26 Prabu, E.; Felix, S.; Felix, N.; Ahilan, B. & Ruby, P. An overview on significance of fish nutrition in aquaculture industry. International Journal of Fisheries and Aquatic Studies, 2017, 5, 349-355 Zhu, T.; Corraze, G.; Plagnes-Juan, E. & Skiba-Cassy, S. Cholesterol metabolism regulation mediated by SREBP-2, LXRα and miR-33a in rainbow trout (Oncorhynchus mykiss) both in vivo and in vitro. Plos one, Public Library of Science San Francisco, CA USA, 2020, 15, e0223813
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Dates et versions

hal-03220591 , version 1 (07-05-2021)

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  • HAL Id : hal-03220591 , version 1

Citer

Thérèse Callet, H Li, Cécile Heraud, Laurence Larroquet, Anthony Lanuque, et al.. A parental low protein diet did not affect growth but modulate lipid metabolism in rainbow trout. Aquaculture Europe 2020, Apr 2021, online, France. , 2021. ⟨hal-03220591⟩
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