Dietary high lipid and high plant-protein affected growth performance, liver health, bile acid metabolism and gut microbiota in groupers

High lipid diets (HLD) and high plant-protein diets (HPD) exhibit potential fishmeal-saving effects but negatively impact liver health and growth performance in fish. We hypothesized that HLD and HPD impair liver health in pearl gentian groupers (Epinephelus fuscoguttatus♂ × Epinephelus lanceolatus♀...

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Main Authors: Jia Xu, Fan Wang, Chaoqun Hu, Junxiang Lai, Shiwei Xie, Kefu Yu, Fajun Jiang
Format: Article
Language:English
Published: KeAi Communications Co., Ltd. 2024-12-01
Series:Animal Nutrition
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Online Access:http://www.sciencedirect.com/science/article/pii/S2405654524001331
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author Jia Xu
Fan Wang
Chaoqun Hu
Junxiang Lai
Shiwei Xie
Kefu Yu
Fajun Jiang
author_facet Jia Xu
Fan Wang
Chaoqun Hu
Junxiang Lai
Shiwei Xie
Kefu Yu
Fajun Jiang
author_sort Jia Xu
collection DOAJ
description High lipid diets (HLD) and high plant-protein diets (HPD) exhibit potential fishmeal-saving effects but negatively impact liver health and growth performance in fish. We hypothesized that HLD and HPD impair liver health in pearl gentian groupers (Epinephelus fuscoguttatus♂ × Epinephelus lanceolatus♀) through the modulation of intestinal microbiota and bile acid (BA) metabolism. Four diet groups were tested: control diet (CD, 46.21% crude protein, 9.48% crude lipid), HLD (46.37% crude protein, 16.70% crude lipid), HPD (46.50% crude protein, 9.38% crude lipid), and high lipid-high plant-protein diet (HLPD, 46.54% crude protein, 16.67% crude lipid). A total of 300 fish (average body weight = 15.22 ± 0.03 g) were randomly divided into 4 diet treatments (ensuring 3 tanks replicates of each diet treatment, each tank containing 25 fish). After an eight-week feeding period, the HLD and HPD significantly decreased the final body weight (FBW), weight gain rate (WGR), specific growth rate (SGR) and feed intake (FI) in comparison to CD group, with HLPD exacerbating these indicators (P < 0.05). Compared to CD group, the content of total cholesterol (T-CHO) and triglyceride (TG) in liver and serum were significantly increased in HLD group (P < 0.05). Compared to HPD group, the content of T-CHO in liver was significantly decreased, the content of TG in liver and serum were significantly increased in HLPD group (P < 0.05). HLD, HPD, and HLPD impaired liver health by inducing histological damage, inflammation, and oxidative stress. Compared to CD group, the mRNA relative expression of bile salt export pump (bsep) and multidrug resistance protein 3 (mdr3) were significantly increased in HLD group, whereas the mRNA relative expression of sterol-27-hydroxylase (cyp27a1), microsomal epoxide hydrolase (meh), apical sodium-dependent bile acid transporter (asbt), multidrug resistance-associated protein 3 (mrp3), farnesoid X receptor (fxr) and G protein-coupled bile acid receptor 5 (tgr5) were significantly decreased (P < 0.05). Compared to CD group, the mRNA relative expression of mdr3, asbt, mrp3, organic anion transporters 1 (oatp1), meh, fxr and tgr5 were significantly decreased in HPD group (P < 0.05). In summary, HLD affects intestinal microbiota, BA metabolism, and lipid metabolism, leading to lipid deposition and liver damage. HPD regulates gut microbiota, BA metabolism, inflammatory responses, and BA receptor expression, impairing grouper liver health. HLPD synergistically combines the adverse effects of HLD and HPD on grouper liver health.
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spelling doaj-art-338ea003fb004db0bfaaa9c048eb826d2025-08-20T02:40:04ZengKeAi Communications Co., Ltd.Animal Nutrition2405-65452024-12-011937038510.1016/j.aninu.2024.08.005Dietary high lipid and high plant-protein affected growth performance, liver health, bile acid metabolism and gut microbiota in groupersJia Xu0Fan Wang1Chaoqun Hu2Junxiang Lai3Shiwei Xie4Kefu Yu5Fajun Jiang6Guangxi Key Laboratory of Marine Environmental Science, Guangxi Academy of Marine Sciences, Guangxi Academy of Sciences, Nanning 530007, China; Guangxi Laboratory on the Study of Coral Reefs in the South China Sea, School of Marine Sciences, Guangxi University, Nanning 530004, ChinaGuangxi Key Laboratory of Marine Environmental Science, Guangxi Academy of Marine Sciences, Guangxi Academy of Sciences, Nanning 530007, China; Guangxi Laboratory on the Study of Coral Reefs in the South China Sea, School of Marine Sciences, Guangxi University, Nanning 530004, ChinaGuangxi Key Laboratory of Marine Environmental Science, Guangxi Academy of Marine Sciences, Guangxi Academy of Sciences, Nanning 530007, China; Key Laboratory of Tropical Marine Bio-Resources and Ecology, Guangdong Provincial Key Laboratory of Applied Marine Biology, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou 510301, China; Corresponding authors.Guangxi Key Laboratory of Marine Environmental Science, Guangxi Academy of Marine Sciences, Guangxi Academy of Sciences, Nanning 530007, ChinaLaboratory of Aquatic Animal Nutrition and Feed, Fisheries College, Guangdong Ocean University, Zhanjiang 524088, ChinaGuangxi Laboratory on the Study of Coral Reefs in the South China Sea, School of Marine Sciences, Guangxi University, Nanning 530004, ChinaGuangxi Key Laboratory of Marine Environmental Science, Guangxi Academy of Marine Sciences, Guangxi Academy of Sciences, Nanning 530007, China; Corresponding authors.High lipid diets (HLD) and high plant-protein diets (HPD) exhibit potential fishmeal-saving effects but negatively impact liver health and growth performance in fish. We hypothesized that HLD and HPD impair liver health in pearl gentian groupers (Epinephelus fuscoguttatus♂ × Epinephelus lanceolatus♀) through the modulation of intestinal microbiota and bile acid (BA) metabolism. Four diet groups were tested: control diet (CD, 46.21% crude protein, 9.48% crude lipid), HLD (46.37% crude protein, 16.70% crude lipid), HPD (46.50% crude protein, 9.38% crude lipid), and high lipid-high plant-protein diet (HLPD, 46.54% crude protein, 16.67% crude lipid). A total of 300 fish (average body weight = 15.22 ± 0.03 g) were randomly divided into 4 diet treatments (ensuring 3 tanks replicates of each diet treatment, each tank containing 25 fish). After an eight-week feeding period, the HLD and HPD significantly decreased the final body weight (FBW), weight gain rate (WGR), specific growth rate (SGR) and feed intake (FI) in comparison to CD group, with HLPD exacerbating these indicators (P < 0.05). Compared to CD group, the content of total cholesterol (T-CHO) and triglyceride (TG) in liver and serum were significantly increased in HLD group (P < 0.05). Compared to HPD group, the content of T-CHO in liver was significantly decreased, the content of TG in liver and serum were significantly increased in HLPD group (P < 0.05). HLD, HPD, and HLPD impaired liver health by inducing histological damage, inflammation, and oxidative stress. Compared to CD group, the mRNA relative expression of bile salt export pump (bsep) and multidrug resistance protein 3 (mdr3) were significantly increased in HLD group, whereas the mRNA relative expression of sterol-27-hydroxylase (cyp27a1), microsomal epoxide hydrolase (meh), apical sodium-dependent bile acid transporter (asbt), multidrug resistance-associated protein 3 (mrp3), farnesoid X receptor (fxr) and G protein-coupled bile acid receptor 5 (tgr5) were significantly decreased (P < 0.05). Compared to CD group, the mRNA relative expression of mdr3, asbt, mrp3, organic anion transporters 1 (oatp1), meh, fxr and tgr5 were significantly decreased in HPD group (P < 0.05). In summary, HLD affects intestinal microbiota, BA metabolism, and lipid metabolism, leading to lipid deposition and liver damage. HPD regulates gut microbiota, BA metabolism, inflammatory responses, and BA receptor expression, impairing grouper liver health. HLPD synergistically combines the adverse effects of HLD and HPD on grouper liver health.http://www.sciencedirect.com/science/article/pii/S2405654524001331Liver damageLipid metabolismBile acid metabolismMicrobiotaGrouper
spellingShingle Jia Xu
Fan Wang
Chaoqun Hu
Junxiang Lai
Shiwei Xie
Kefu Yu
Fajun Jiang
Dietary high lipid and high plant-protein affected growth performance, liver health, bile acid metabolism and gut microbiota in groupers
Animal Nutrition
Liver damage
Lipid metabolism
Bile acid metabolism
Microbiota
Grouper
title Dietary high lipid and high plant-protein affected growth performance, liver health, bile acid metabolism and gut microbiota in groupers
title_full Dietary high lipid and high plant-protein affected growth performance, liver health, bile acid metabolism and gut microbiota in groupers
title_fullStr Dietary high lipid and high plant-protein affected growth performance, liver health, bile acid metabolism and gut microbiota in groupers
title_full_unstemmed Dietary high lipid and high plant-protein affected growth performance, liver health, bile acid metabolism and gut microbiota in groupers
title_short Dietary high lipid and high plant-protein affected growth performance, liver health, bile acid metabolism and gut microbiota in groupers
title_sort dietary high lipid and high plant protein affected growth performance liver health bile acid metabolism and gut microbiota in groupers
topic Liver damage
Lipid metabolism
Bile acid metabolism
Microbiota
Grouper
url http://www.sciencedirect.com/science/article/pii/S2405654524001331
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