Dietary bile acids have a differential role in preventing enteritis in juvenile grass carp, Ctenopharyngodon idella

Abstract

Enteritis often limits intensive aquaculture, where bile acids (BAs), a group of steroid molecules, are used to prevent intestinal diseases. However, the functions of certain BAs are poorly understood. In this study, grass carp with enteritis (EGC) and healthy grass carp (HGC) were sampled, and the BAs' composition was analyzed. Results showed distinct differences in the BA profiles: EGC exhibited significantly elevated levels of taurodeoxycholic acid (TDCA), lithocholic acid (LCA), glycoursodeoxycholic acid (GUDCA), and glycohyocholic acid (GHCA) (P < 0.05), and decreased levels of TCDCA, taurocholic acid (TCA), and cholic acid (CA) in the intestine compared with their levels in HGC. Subsequently, five diets containing four typical BAs (CA, chenodeoxycholic acid [CDCA], deoxycholic acid [DCA], and LCA) at the same concentration (0.1 %) were formulated to feed the juvenile grass carps (6.29 ± 0.05 g) for 8 weeks. DCA alone increased body weight, reduced the feed conversion ratio (FCR), and ameliorated histological intestinal inflammatory hallmarks. Conversely, individual supplementation with CDCA, LCA, or CA decreased body weight and increased FCR and exacerbated the histological hallmarks of enteritis. Furthermore, DCA markedly reduced the mRNA expression levels of endoplasmic reticulum stress (ERS)-related genes in the intestine, including glucose-regulated protein 78 (GPR78), activating transcription factor 6 (ATF6), inositol-requiring enzyme 1, and protein kinase RNA-like ER kinase, as well as genes encoding proinflammatory cytokines, such as interleukin (IL)-1 beta, IL-8, and tumor necrosis factor α (TNF-α). Supplementation with CDCA, LCA, or CA promoted the expression of ERS- and proinflammatory-cytokine-related genes. Additionally, Actinobacteriota abundance negatively correlated with intestinal mRNA expression levels of TNF-α, ATF6, IL-1β, GPR78, and IL-8, and Candidatus-Arthromitus abundance positively correlated with these inflammatory markers (P < 0.05). In conclusion, our results demonstrated that BAs play differential roles in modulating the enteritis process and that DCA may have a specific anti-inflammatory role in grass carp.

Keywords

• enteritis
• bile acids
• endoplasmic reticulum stress
• microbiota
• grass carp