Specific Blood Plasma Circulating miRs Are Associated with the Physiological Impact of Total Fish Meal Replacement with Soybean Meal in Diets for Rainbow Trout (Oncorhynchus mykiss)

SIMPLE SUMMARY: To warrant food security and nutrition, more sustainable aquafeeds should be used in fish farming, and the content of fish meal (FM) in fish diets should be reduced. Soybean meal (SBM) is one of the most commonly used alternative raw materials to replace FM in commercial diets, although a high SBM dietary content can affect fish growth, physiology, and wellbeing. Although these effects are known to be produced by several antinutritional factors (ANFs), the underlying mechanisms are still not fully understood. Deeper characterization of how SBM dietary content alters fish physiology will allow the development of more integrative fish physiology monitoring. In the present work, the expression of six microRNAs (miRs) in blood plasma was associated with a high SBM dietary content and related physiological consequences. Circulating miRs can be used as a less invasive procedure to monitor fish physiology without the need of animal sacrifice, allowing the development of more sustainable aquafeeds with the use of fewer animals in experimentation. ABSTRACT: High dietary SBM content is known to induce important physiological alterations, hampering its use as a major FM alternative. Rainbow trout (Oncorhynchus mykiss) juveniles were fed two experimental diets during 9 weeks: (i) a FM diet containing 12% FM; and (ii) a vegetable meal (VM) diet totally devoid of FM and based on SBM (26%). Fish fed the VM diet did not show reduced growth performance when compared with fish fed the FM diet. Nevertheless, fish fed the VM diet had an increased viscerosomatic index, lower apparent fat digestibility, higher aminopeptidase enzyme activity and number of villi fusions, and lower α-amylase enzyme activity and brush border integrity. Small RNA-Seq analysis identified six miRs (omy-miR-730a-5p, omy-miR-135c-5p, omy-miR-93a-3p, omy-miR-152-5p, omy-miR-133a-5p, and omy-miR-196a-3p) with higher expression in blood plasma from fish fed the VM diet. Bioinformatic prediction of target mRNAs identified several overrepresented biological processes known to be associated with high dietary SBM content (e.g., lipid metabolism, epithelial integrity disruption, and bile acid status). The present research work increases our understanding of how SBM dietary content has a physiological impact in farmed fish and suggests circulating miRs might be suitable, integrative, and less invasive biomarkers in fish.