Rosemary-derived triterpene acids improve growth and lipid metabolism in juvenile grass carp (Ctenopharyngodon idella) through the gut–liver axis by tissue-specifically regulating the farnesoid X receptor

TL;DR

Rosemary-derived triterpene acids improve growth and lipid metabolism in juvenile grass carp by regulating the gut–liver axis and specific metabolic pathways.

Contribution

This study reveals the tissue-specific regulation of the farnesoid X receptor by triterpene acids in improving lipid metabolism in grass carp.

Findings

TAs increased growth rate and protein retention while reducing body fat in juvenile grass carp.

TAs enhanced intestinal enzyme activity and improved digestive and absorptive functions.

TAs inhibited hepatic lipid synthesis and activated the FXR pathway, promoting lipid utilization.

Abstract

Rosemary-derived triterpene acids (TAs), primarily composed of ursolic acid, oleanolic acid, and betulinic acid, exhibit multiple bioactive properties. However, their effects on lipid metabolism and the underlying regulatory pathways remain unclear. This study investigated the effects of dietary supplementation with TAs on the growth performance, digestive and absorptive function, and hepatic lipid metabolism in juvenile grass carp (Ctenopharyngodon idella).

In this trial, 2,160 juvenile grass carp (average weight 13.04 ± 0.02 g) were randomly allocated to six dietary treatments, each comprising six replicates with 60 fish per replicate. Fish were fed diets supplemented with increasing concentrations of TAs (0, 58.80, 179.30, 261.90, 312.00, and 390.00 mg/kg) for 70 d. At the end of the trial, relevant samples were collected for subsequent analyses.

The results demonstrated that dietary supplementation with TAs significantly increased specific growth rate (SGR), whole-body crude protein (CP) levels, and protein retention value (PRV) in juvenile grass carp, while reducing whole-body ether extract (EE) levels. Moreover, dietary supplementation with TAs significantly enhanced the activities of intestinal digestive enzymes and brush-border enzymes, thereby improving the digestive and absorptive capacity of juvenile grass carp. In the liver, dietary supplementation with TAs markedly inhibited lipid synthesis while promoting lipid utilization. The effects of TAs on lipid metabolism were associated with activation of the hepatic farnesoid X receptor (FXR) pathway, involving peroxisome proliferator-activated receptor alpha (PPARα) and sterol regulatory element-binding protein 1 (SREBP-1). Furthermore, TAs modulated the gut–liver axis by inhibiting the intestinal FXR–sphingomyelin phosphodiesterase 3 (SMPD3)–ceramide pathway, which may contribute to reduced hepatic lipid deposition. Quadratic regression analysis showed that the optimal dietary TAs supplementation levels were 245.00 mg/kg (SGR), 218.33 mg/kg (intestinal lipase activity), and 267.64 mg/kg (hepatic hormone-sensitive lipase activity).

The addition of TAs to the diet improved growth performance, digestive and absorptive capacity, and liver lipid utilization in juvenile grass carp. This work reveals the potential application of TAs in aquaculture and provides a theoretical basis for the development of functional feed additives.

The online version contains supplementary material available at 10.1186/s40104-025-01351-1.

Figures