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)

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....

Full description

Bibliographic Details
Main Authors: Qiao Liu, Liangshun Cheng, Maozhu Wang, Lianfeng Shen, Chengxian Zhang, Jin Mu, Yifan Hu, Yihui Yang, Kuo He, Haoxiao Yan, Liulan Zhao, Song Yang
Format: Article
Language:English
Published: BMC 2024-04-01
Series:Journal of Animal Science and Biotechnology
Subjects:
Online Access:https://doi.org/10.1186/s40104-024-01009-4
_version_ 1797219653941985280
author Qiao Liu
Liangshun Cheng
Maozhu Wang
Lianfeng Shen
Chengxian Zhang
Jin Mu
Yifan Hu
Yihui Yang
Kuo He
Haoxiao Yan
Liulan Zhao
Song Yang
author_facet Qiao Liu
Liangshun Cheng
Maozhu Wang
Lianfeng Shen
Chengxian Zhang
Jin Mu
Yifan Hu
Yihui Yang
Kuo He
Haoxiao Yan
Liulan Zhao
Song Yang
author_sort Qiao Liu
collection DOAJ
description 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.
first_indexed 2024-04-24T12:37:04Z
format Article
id doaj.art-381a00718f644511aea8ddf64c1275c6
institution Directory Open Access Journal
issn 2049-1891
language English
last_indexed 2024-04-24T12:37:04Z
publishDate 2024-04-01
publisher BMC
record_format Article
series Journal of Animal Science and Biotechnology
spelling doaj.art-381a00718f644511aea8ddf64c1275c62024-04-07T11:26:32ZengBMCJournal of Animal Science and Biotechnology2049-18912024-04-0115111910.1186/s40104-024-01009-4Dietary 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 Liu0Liangshun Cheng1Maozhu Wang2Lianfeng Shen3Chengxian Zhang4Jin Mu5Yifan Hu6Yihui Yang7Kuo He8Haoxiao Yan9Liulan Zhao10Song Yang11College of Animal Science and Technology, Sichuan Agricultural UniversityCollege of Animal Science and Technology, Sichuan Agricultural UniversityCollege of Animal Science and Technology, Sichuan Agricultural UniversityCollege of Animal Science and Technology, Sichuan Agricultural UniversityCollege of Animal Science and Technology, Sichuan Agricultural UniversityCollege of Animal Science and Technology, Sichuan Agricultural UniversityCollege of Animal Science and Technology, Sichuan Agricultural UniversityCollege of Animal Science and Technology, Sichuan Agricultural UniversityCollege of Animal Science and Technology, Sichuan Agricultural UniversityCollege of Animal Science and Technology, Sichuan Agricultural UniversityCollege of Animal Science and Technology, Sichuan Agricultural UniversityCollege of Animal Science and Technology, Sichuan Agricultural UniversityAbstract 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.https://doi.org/10.1186/s40104-024-01009-4High carbohydrate dietIntestinal microbiotaLargemouth bassLipid depositionSodium acetateSodium butyrate
spellingShingle Qiao Liu
Liangshun Cheng
Maozhu Wang
Lianfeng Shen
Chengxian Zhang
Jin Mu
Yifan Hu
Yihui Yang
Kuo He
Haoxiao Yan
Liulan Zhao
Song Yang
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)
Journal of Animal Science and Biotechnology
High carbohydrate diet
Intestinal microbiota
Largemouth bass
Lipid deposition
Sodium acetate
Sodium butyrate
title 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)
title_full 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)
title_fullStr 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)
title_full_unstemmed 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)
title_short 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)
title_sort 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
topic High carbohydrate diet
Intestinal microbiota
Largemouth bass
Lipid deposition
Sodium acetate
Sodium butyrate
url https://doi.org/10.1186/s40104-024-01009-4
work_keys_str_mv AT qiaoliu dietarysodiumacetateandsodiumbutyrateimprovehighcarbohydratedietutilizationbyregulatinggutmicrobiotaliverlipidmetabolismoxidativestressandinflammationinlargemouthbassmicropterussalmoides
AT liangshuncheng dietarysodiumacetateandsodiumbutyrateimprovehighcarbohydratedietutilizationbyregulatinggutmicrobiotaliverlipidmetabolismoxidativestressandinflammationinlargemouthbassmicropterussalmoides
AT maozhuwang dietarysodiumacetateandsodiumbutyrateimprovehighcarbohydratedietutilizationbyregulatinggutmicrobiotaliverlipidmetabolismoxidativestressandinflammationinlargemouthbassmicropterussalmoides
AT lianfengshen dietarysodiumacetateandsodiumbutyrateimprovehighcarbohydratedietutilizationbyregulatinggutmicrobiotaliverlipidmetabolismoxidativestressandinflammationinlargemouthbassmicropterussalmoides
AT chengxianzhang dietarysodiumacetateandsodiumbutyrateimprovehighcarbohydratedietutilizationbyregulatinggutmicrobiotaliverlipidmetabolismoxidativestressandinflammationinlargemouthbassmicropterussalmoides
AT jinmu dietarysodiumacetateandsodiumbutyrateimprovehighcarbohydratedietutilizationbyregulatinggutmicrobiotaliverlipidmetabolismoxidativestressandinflammationinlargemouthbassmicropterussalmoides
AT yifanhu dietarysodiumacetateandsodiumbutyrateimprovehighcarbohydratedietutilizationbyregulatinggutmicrobiotaliverlipidmetabolismoxidativestressandinflammationinlargemouthbassmicropterussalmoides
AT yihuiyang dietarysodiumacetateandsodiumbutyrateimprovehighcarbohydratedietutilizationbyregulatinggutmicrobiotaliverlipidmetabolismoxidativestressandinflammationinlargemouthbassmicropterussalmoides
AT kuohe dietarysodiumacetateandsodiumbutyrateimprovehighcarbohydratedietutilizationbyregulatinggutmicrobiotaliverlipidmetabolismoxidativestressandinflammationinlargemouthbassmicropterussalmoides
AT haoxiaoyan dietarysodiumacetateandsodiumbutyrateimprovehighcarbohydratedietutilizationbyregulatinggutmicrobiotaliverlipidmetabolismoxidativestressandinflammationinlargemouthbassmicropterussalmoides
AT liulanzhao dietarysodiumacetateandsodiumbutyrateimprovehighcarbohydratedietutilizationbyregulatinggutmicrobiotaliverlipidmetabolismoxidativestressandinflammationinlargemouthbassmicropterussalmoides
AT songyang dietarysodiumacetateandsodiumbutyrateimprovehighcarbohydratedietutilizationbyregulatinggutmicrobiotaliverlipidmetabolismoxidativestressandinflammationinlargemouthbassmicropterussalmoides