Interactions between nutritional programming, genotype, and gut microbiota in Atlantic salmon: Long-term effects on gut microbiota, fish growth and feed efficiency

Abstract

Nutritional programming (NP) is a tool for developing adaptive changes that can be expressed in adulthood by exposing individuals to a stimulus early in life. This study investigated the interactions between nutritional programming (NP), genotype and gut microbiota in Atlantic salmon (Salmo salar) across the life cycle, to potentially improve feed efficiency and fish health. Approximately 5100 eggs from six families characterised by high (HP) or low pigment retention (LP) were incubated and divided into four groups (HPM, HPV, LPM, LPV) that received a stimulus diet based on marine (M) (61 % fishmeal and 8 % fish oil) or vegetable (V) (5 % fishmeal, plant proteins and rapeseed oil) ingredients. This stimulus phase lasted three weeks, followed by a 49-week freshwater intermediate phase with fish fed a commercial feed subsequent to seawater transfer. In seawater, the fish were initially fed a commercial feed for 13 weeks and then switched to a plant-based “challenge” diet with approximately 3 % EPA + DHA until the end of the experiment, at 101 weeks, at which point fish were 4 kg. During the study, survival rates, SGR, and FCR were monitored. Samples for microbiota analysis were collected at T0 (after the stimulus), T1 (before the challenge), T2 (challenge, after the feed change), and T3 (end of the feeding trial). Gut and feed microbiota were analysed by bacterial DNA extraction, Illumina NGS library preparation and raw sequencing data analysis using QIIME 2 and PICRUSt software. Gut microbiota composition changed with fish age, independent of NP and pigmentation genotype, emphasising the importance of developmental stage. Early diet influenced beta diversity and increased the number of specific bacteria, but these changes decreased with time. NP influenced the gut microbiota during the stimulus phase but not during the challenge phase, showing that the current diet has a greater influence than the earlier diet. Some microbial genera were associated with different genotypes and diets, suggesting interactions between genotype and stimulus diet. Differences in the metabolic potential of the gut microbiota due to the stimulus diet were observed but were not associated with differences in growth and feed utilisation. The study concludes that early nutritional programming with a plant-based diet has a transient effect on growth and gut microbiota, with long-term growth performance being more strongly influenced by pigmentation genotype. Further studies on the interactions between genotype, diet and microbiota are required.