Modulation of Energy Metabolism and Epigenetic Landscape in Rainbow Trout Fry by a Parental Low Protein/High Carbohydrate Diet

Simple Summary While the effects of parental diets on their progeny have been highly described in mammals, such studies are lacking in fish. To explore such a question in a high trophic level teleost fish, two-year old male and female rainbow trout were fed either a control diet (0% carbohydrate and 63.89% protein) or a high-carbohydrate diet (35% carbohydrate and 42.96% protein), for a complete reproductive cycle for females and for a period of 5 months for males. Neither the maternal nor the paternal high-carbohydrate diet alone had induced significant effects on their progeny. Nevertheless, when both parents were fed the high-carbohydrate diet, the energy metabolism and mitochondrial dynamics of their progeny were altered. Moreover, the epigenetic landscape was also highly affected. Even though, offspring growth was only slightly affected at the early stage of life; the effect of parental high-carbohydrate diet should be explored over the long term. It is now recognized that parental diets could highly affect offspring metabolism and growth. Studies in fish are, however, lacking. In particular, the effect of a parental diet high in carbohydrate (HC) and low in protein (LP) on progeny has never been examined in higher trophic level teleost fish. Thus, two-year old male and female rainbow trout (Oncorhynchus mykiss) were fed either a control diet (0% carbohydrate and 63.89% protein) or a diet containing 35% carbohydrate and 42.96% protein (HC/LP) for a complete reproductive cycle for females and over a 5-month period for males. Cross-fertilizations were then carried out. To evaluate the effect of the parental diet on their offspring, different phenotypic and metabolic traits were recorded for offspring before their first feeding and again three weeks later. When considering the paternal and maternal HC/LP nutrition independently, fry phenotypes and transcriptomes were only slightly affected. The combination of the maternal and paternal HC/LP diets altered the energy metabolism and mitochondrial dynamics of their progeny, demonstrating the existence of a synergistic effect. The global DNA methylation of whole fry was also highly affected by the HC/LP parental diet, indicating that it could be one of the fundamental mechanisms responsible for the effects of nutritional programming.