Partial fishmeal replacement by soybean meal induces fish growth retardation and gut inflammation via gut mucosal barrier dysfunction and dysbiosis in largemouth bass

Abstract

The study aimed to investigate the effect of partial fishmeal replacement by soybean meal on fish growth, gut histology, oxidative stress, gut microbiota, and gene expression of inflammatory cytokines and tight junction proteins in largemouth bass (Micropterus salmoides). Four isonitrogenous and isolipidic diets were formulated: the FM diet contained 45% fishmeal (FM diet) and did not contain soybean meal; diets SM25, SM50, and SM75 replaced 25%, 50%, and 75% fishmeal protein in the FM group with soybean meal, respectively. Experimental fish (4.3 ± 0.1g) were fed to apparent satiation for eight weeks. The results showed that replacing 25% or more fishmeal decreased villus height, villus width, total superoxide dismutase (T-SOD) and catalase (CAT) activity levels, reduced glutathione contents, and Aurantimicrobium abundance; increased malonaldehyde contents and tumor necrosis factor α (TNF-α) and interleukin 1β (IL-1β) expression; downregulated nuclear factor E2‐related factor 2 (Nrf2), occludin, and zona occluding-1 (ZO-1), lysozyme (LYS) and hypoxia-inducible factor-1α (HIF-1α) expression, compared with FM (P < 0.05). Moreover, SBM50 and SBM75 decreased final body weight, weight gain rate, and specific growth rate, and increased the lamina propria width than FM (P < 0.05). Furthermore, SBM25 dramatically reduced Actinobacteriota, Enterococcus, Lactococcus, Leuconostoc, and Streptococcus abundance (P < 0.05). Compared to SM25, SM75 dramatically increased Brucella abundance (P < 0.05). Pearson correlation analysis indicated that tight junction proteins (ZO-1 and Occludin) and gut microbiota (Aurantimicrobium and Brucella) have a significant association with gut inflammation and fish growth (P < 0.05). These results showed that gut dysbiosis and intestinal mucosal barrier dysfunction are major contributors to the soybean meal-induced growth retardation and gut inflammation in fish.