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

Citation

Tawfik MM, Betancor MB, Mcmillan S, Norambuena F, Tocher DR, Douglas A & Martin SAM (2024) 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. Overland M (Editor) Frontiers in Immunology, 15. https://doi.org/10.3389/fimmu.2024.1412821

Abstract
Introduction: Plant-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. Methods: This 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 discussion: At 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 Frontiers in Immunology Tawfik MM, Betancor MB, McMillan S, Norambuena F, Tocher DR, Douglas A and Martin SAM (2024) 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. 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 study demonstrated nutritional programming-associated changes in the intestinal transcriptome, with altered expression of genes involved in both immune responses and different metabolic processes. While there were limited changes in growth between the groups, the results show that there were transcriptional differences, suggesting a programming response, although the mechanism of this response still requires to be fully elucidated.

Keywords
metabolic programming; first feeding; transcriptome; distal; midgut; mucosal immunity; epigenetic programming; hindgut

Journal
Frontiers in Immunology: Volume 15