Dietary sodium acetate and sodium butyrate improve high-carbohydrate diet utilization by regulating gut microbiota, liver lipid metabolism, oxidative stress, and inflammation in largemouth bass (Micropterus salmoides)

Qiao Liu; Liangshun Cheng; Maozhu Wang; Lianfeng Shen; Chengxian Zhang; Jin Mu; Yifan Hu; Yihui Yang; Kuo He; Haoxiao Yan; Liulan Zhao; Song Yang

doi:10.1186/s40104-024-01009-4

Dietary sodium acetate and sodium butyrate improve high-carbohydrate diet utilization by regulating gut microbiota, liver lipid metabolism, oxidative stress, and inflammation in largemouth bass (Micropterus salmoides)

J Anim Sci Biotechnol. 2024 Apr 3;15(1):50. doi: 10.1186/s40104-024-01009-4.

Authors

Qiao Liu^#¹, Liangshun Cheng^#¹, Maozhu Wang¹, Lianfeng Shen¹, Chengxian Zhang¹, Jin Mu¹, Yifan Hu¹, Yihui Yang¹, Kuo He¹, Haoxiao Yan¹, Liulan Zhao², Song Yang³

Affiliations

¹ College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, 611130, Sichuan, China.
² College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, 611130, Sichuan, China. zhaoliulan2007@163.com.
³ College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, 611130, Sichuan, China. ysys210@hotmail.com.

^# Contributed equally.

Abstract

Background: Adequate level of carbohydrates in aquafeeds help to conserve protein and reduce cost. However, studies have indicated that high-carbohydrate (HC) diet disrupt the homeostasis of the gut-liver axis in largemouth bass, resulting in decreased intestinal acetate and butyrate level.

Method: Herein, we had concepted a set of feeding experiment to assess the effects of dietary sodium acetate (SA) and sodium butyrate (SB) on liver health and the intestinal microbiota in largemouth bass fed an HC diet. The experimental design comprised 5 isonitrogenous and isolipidic diets, including LC (9% starch), HC (18% starch), HCSA (18% starch; 2 g/kg SA), HCSB (18% starch; 2 g/kg SB), and HCSASB (18% starch; 1 g/kg SA + 1 g/kg SB). Juvenile largemouth bass with an initial body weight of 7.00 ± 0.20 g were fed on these diets for 56 d.

Results: We found that dietary SA and SB reduced hepatic triglyceride accumulation by activating autophagy (ATG101, LC3B and TFEB), promoting lipolysis (CPT1α, HSL and AMPKα), and inhibiting adipogenesis (FAS, ACCA, SCD1 and PPARγ). In addition, SA and SB decreased oxidative stress in the liver (CAT, GPX1α and SOD1) by activating the Keap1-Nrf2 pathway. Meanwhile, SA and SB alleviated HC-induced inflammation by downregulating the expression of pro-inflammatory factors (IL-1β, COX2 and Hepcidin1) through the NF-κB pathway. Importantly, SA and SB increased the abundance of bacteria that produced acetic acid and butyrate (Clostridium_sensu_stricto_1). Combined with the KEGG analysis, the results showed that SA and SB enriched carbohydrate metabolism and amino acid metabolism pathways, thereby improving the utilization of carbohydrates. Pearson correlation analysis indicated that growth performance was closely related to hepatic lipid deposition, autophagy, antioxidant capacity, inflammation, and intestinal microbial composition.

Conclusions: In conclusion, dietary SA and SB can reduce hepatic lipid deposition; and alleviate oxidative stress and inflammation in largemouth bass fed on HC diet. These beneficial effects may be due to the altered composition of the gut microbiota caused by SA and SB. The improvement effects of SB were stronger than those associated with SA.

Keywords: High carbohydrate diet; Intestinal microbiota; Largemouth bass; Lipid deposition; Sodium acetate; Sodium butyrate.