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....
Main Authors: | , , , , , , , , , , , |
---|---|
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 |