Mechanism of fumonisin B1 on growth performance and intestinal structural integrity of juvenile grass carp (Ctenopharyngodon idella).

Abstract

Fumonisin B1 (FB1) is a prevalent mycotoxin found in plant-based feed ingredients, and it negatively impacts the performance of aquatic animals. However, the mechanism of this toxicity remains unclear. This study aims to investigate the effect and underlying mechanism of dietary FB1 on the growth performance of juvenile grass carp (Ctenopharyngodon idella). A total of 720 juvenile grass carp (10.92 ± 0.02 g) were fed with four different levels of FB1 diets (0, 2.06, 3.94, and 8.05 mg/kg) for 30 d and each group had 3 replicates of 60 fish. Our data indicated that when the FB1 concentration in the diet exceeded 3.94 mg/kg, there was a significant decline in growth performance (e.g., final body weight, percent weight gain, and body length) (P < 0.05), as well as reductions in the activities of digestive enzymes (e.g., chymotrypsin and trypsin), alkaline phosphatase, and creatine kinase in juvenile grass carp (P < 0.05). Furthermore, increased levels of intestinal sphinganine (Sa), sphingosine (So), and FB1 residues were observed, along with disruptions in intestinal tissue structure and elevated serum D-lactic acid levels (P < 0.05). Additionally, FB1 inhibited the Kelch-like ECH-associated protein 1a/NF-E2-related factor-2 signaling pathway, resulting in decreased gene expression of intestinal copper-zinc superoxide dismutase, glutathione peroxidase 4b, and glutathione peroxidase 1a (P < 0.05). These alterations were accompanied by a reduction in glutathione levels, total superoxide dismutase activity, and total antioxidant capacity (P < 0.05), as well as an increase in levels of reactive oxygen species and malondialdehyde in the intestine (P < 0.05). FB1 induced intestinal apoptosis by downregulating the gene expression of B-cell lymphoma 2 (P = 0.009), while simultaneously upregulating the expression of Bcl-2-associated X protein, apoptotic protease activating factor-1, caspase-9, and caspase-3 (P < 0.05). Additionally, FB1 decreased the gene expression of apical junction complex-related molecules (e.g., zonula occluden-1, occludin, and nectin) (P < 0.05), while increasing the expression of claudin-15b, myosin light chain kinase, Rho family GTPases, and Rho-associated protein kinase (P < 0.05). These findings indicated that dietary FB1 negatively impacts the growth performance of juvenile grass carp, likely due to reduced digestive and absorptive capacities, elevated intestinal Sa and So levels, and disruption of intestinal structure integrity. This study filled the study gap on the toxicity of FB1 to the intestines of aquatic animals.