Modulation of metabolic and immunoregulatory pathways in the gut transcriptome of Atlantic salmon (Salmo salar L.) after early nutritional programming during first feeding with plant-based diet

• Published in: Frontiers in Immunology
• Main Authors: Marwa Mamdouh Tawfik, Mónica B. Betancor, Stuart McMillan, Fernando Norambuena, Douglas R. Tocher, Alex Douglas, Samuel A. M. Martin
• Format: Article in Journal/Newspaper
• Language: English
• Published: Frontiers Media S.A. 2024
• Subjects: metabolic programming; first feeding; transcriptome; distal; midgut; mucosal immunity; Immunologic diseases. Allergy; RC581-607; Atlantic salmon; Salmo salar
• Online Access: https://doi.org/10.3389/fimmu.2024.1412821; https://doaj.org/article/d0a10a60f6eb4bb181bee6638020ecfe

IntroductionPlant-based nutritional programming is the concept of exposing fish at very early life stages to a plant-based diet for a short duration to improve physiological responses when exposed to a similar plant-rich diet at a later developmental stage. The mechanisms of action underlying nutritional programming have not been fully deciphered, and the responses may be controlled at multiple levels.MethodsThis 22-week study examines gut transcriptional changes after nutritional programming. Triplicate groups of Atlantic salmon were fed with a plant (V) vs. a marine-rich (M, control) diet for 2 weeks (stimulus phase) at the first exogenous feeding. Both stimulus fish groups (M and V fish) were then fed the M diet for 12 weeks (intermediate phase) and lastly fed the V diet (challenge phase) for 6 weeks, generating two dietary regimes (MMV and VMV) across phases. This study used a whole-transcriptome approach to analyse the effects of the V diet at the end of stimulus (short-term effects) and 22 weeks post-first feeding (long-term effects). After the stimulus, due to its developmental stage, the whole intestine was used, whereas, after the challenge, pyloric caeca and middle and distal intestines were examined.Results and discussionAt the stimulus end, genes with increased expression in V fish enriched pathways including regulatory epigenetic responses and lipid metabolism, and genes involved in innate immune response were downregulated. In the middle intestine at the end of the challenge, expression levels of genes of lipid, carbohydrate, and energy metabolism were increased in V fish, while M fish revealed increased expression of genes associated with autoimmune and acute adaptive immune response. The distal intestine of V fish showed increased expression of genes associated with immune response and potential immune tolerance. Conversely, the distal intestine of M fish at challenge revealed upregulation of lipid and carbohydrate metabolic pathways, tissue degeneration, and apoptotic responses. The present ...