Characterization of expression response in post-prandial situation of food sensing system in rainbow trout (Oncorhynchus mykiss) fed a plant-based diet: Focus on free fatty acid receptors and their signaling pathways

Recently identified and characterized in rainbow trout (Oncorhynchus mikyss), the main gustatory receptors for fatty acid, known as free fatty acids receptor (FFAR) 1 and 2, may play a crucial role in nutrient detection and regulation of feeding behavior. However, our understanding of their post-prandial roles remains limited. This study investigates the impact of a single meal (acute effect) with an alternative plant-based diet (vegetal diet, V diet devoid of fish meal and fish oil) on the food detection mechanisms in trout. After 30 days of feeding with commercial-like diet (C diet made up of a mix of fish meal, fish oil and plant ingredients) followed 5 days of fasting, we conducted a post-prandial kinetic experiment after single meal with C or V diet. We assessed the expression pattern of ffar genes, their associated signaling pathways (calcium and indolamine pathways) in the tongue along with the expression pattern of appetite-regulating neuropeptides in the hypothalamus. Additionally, we evaluated central activity through brain activity markers in the telencephalon of trout at various postmeal time points, including 20 min, 2, 6, 10 and 24 h. Our results revealed that the diet nature (C vs V) influences the expression of ffar genes, while some paralogs of ffar2 (ffar2a2 and ffar2b1.2) were early up-regulated by V diet, ffar2b1.1 and ffar1 were latter up-regulated by C diet. Differential regulations in the tongues of V diet fish were also observed on calcium signaling and an early alteration in serotonin turnover. The expression increase of neuropeptide npya from 6 to 10 h after meal, could suggest a greater sensation of hunger in fish fed the C diet. Finally, our findings suggest that rainbow trout exhibit a keen ability to detect a novel feed after a single meal with V diet at the brain level, particularly in areas associated with decision-making and behavior control. Altogether, results not only show that the integrative feeding response appears to be dysregulated by V diet, but also highlight the noteworthy sensitivity of nutrient detection mechanisms in rainbow trout to new food sources. FFARs may play a role in finely discerning diets with varying levels of omega-3 LC-PUFAs in rainbow trout. This heightened detection sensitivity holds the potential to significantly influence the regulation of feeding behavior and food detection in farmed fish.