Cargando…

The direct and gut microbiota-mediated effects of dietary bile acids on the improvement of gut barriers in largemouth bass (Micropterus salmoides)

Fish gut barrier damage under intensive culture model is a significant concern for aquaculture industry. This study aimed to investigate the effects of bile acids (BAs) on gut barriers in Micropterus salmoides. A germ-free (GF) zebrafish model was employed to elucidate the effects of the direct stimu...

Descripción completa

Detalles Bibliográficos
Autores principales: Xia, Rui, Zhang, Qingshuang, Xia, Dongmei, Hao, Qiang, Ding, Qianwen, Ran, Chao, Yang, Yalin, Cao, Aizhi, Zhang, Zhen, Zhou, Zhigang
Formato: Online Artículo Texto
Lenguaje:English
Publicado: KeAi Publishing 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10208797/
https://www.ncbi.nlm.nih.gov/pubmed/37234949
http://dx.doi.org/10.1016/j.aninu.2023.03.008
_version_ 1785046746579075072
author Xia, Rui
Zhang, Qingshuang
Xia, Dongmei
Hao, Qiang
Ding, Qianwen
Ran, Chao
Yang, Yalin
Cao, Aizhi
Zhang, Zhen
Zhou, Zhigang
author_facet Xia, Rui
Zhang, Qingshuang
Xia, Dongmei
Hao, Qiang
Ding, Qianwen
Ran, Chao
Yang, Yalin
Cao, Aizhi
Zhang, Zhen
Zhou, Zhigang
author_sort Xia, Rui
collection PubMed
description Fish gut barrier damage under intensive culture model is a significant concern for aquaculture industry. This study aimed to investigate the effects of bile acids (BAs) on gut barriers in Micropterus salmoides. A germ-free (GF) zebrafish model was employed to elucidate the effects of the direct stimulation of BAs and the indirect regulations mediated by the gut microbiota on gut barrier functions. Four diets were formulated with BAs supplemented at 0, 150, 300 and 450 mg/kg, and these 4 diets were defined as control, BA150, BA300 and BA450, respectively. After 5 weeks of feeding experiment, the survival rate of fish fed with BA300 diet was increased (P < 0.05). Histological analysis revealed an improvement of gut structural integrity in the BA150 and BA300 groups. Compared with the control group, the expression of genes related to chemical barrier (mucin, lysozyme and complement 1) and physical barrier (occludin and claudin-4) was increased in the BA150 and BA300 groups (P < 0.05), and the expression of genes related to immunological barrier (interleukin [IL]-6, tumor growth factor β, IL-10, macrophage galactose-type lectin and immunoglobulin M [IgM]) was significantly increased in the BA300 group (P < 0.05), but the expression of genes related to chemical barrier (hepcidin) and immunological barrier (IL-1β, tumor necrosis factor-α, IL-6 and arginase) was significantly decreased in the BA450 group (P < 0.05). Gut microbiota composition analysis revealed that the abundance of Firmicutes was augmented prominently in the BA150 and BA300 groups (P < 0.05), while that of Actinobacteriota and Proteobacteria showed a downward trend in the BA150 and BA300 groups (P > 0.05). The results of the gut microbiota transferring experiment demonstrated an upregulation of gut barrier-related genes, including immunoglobulin Z/T (IgZ/T), IL-6, IL-1β and IL-10, by the gut microbiota transferred from the BA300 group compared with the control (P < 0.05). Feeding the BA300 diet directly to GF zebrafish resulted in enhanced expression of IgM, IgZ/T, lysozyme, occludin-2, IL-6 and IL-10 (P < 0.05). In conclusion, BAs can improve the gut barriers of fish through both direct and indirect effects mediated by the gut microbiota.
format Online
Article
Text
id pubmed-10208797
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher KeAi Publishing
record_format MEDLINE/PubMed
spelling pubmed-102087972023-05-25 The direct and gut microbiota-mediated effects of dietary bile acids on the improvement of gut barriers in largemouth bass (Micropterus salmoides) Xia, Rui Zhang, Qingshuang Xia, Dongmei Hao, Qiang Ding, Qianwen Ran, Chao Yang, Yalin Cao, Aizhi Zhang, Zhen Zhou, Zhigang Anim Nutr Original Research Article Fish gut barrier damage under intensive culture model is a significant concern for aquaculture industry. This study aimed to investigate the effects of bile acids (BAs) on gut barriers in Micropterus salmoides. A germ-free (GF) zebrafish model was employed to elucidate the effects of the direct stimulation of BAs and the indirect regulations mediated by the gut microbiota on gut barrier functions. Four diets were formulated with BAs supplemented at 0, 150, 300 and 450 mg/kg, and these 4 diets were defined as control, BA150, BA300 and BA450, respectively. After 5 weeks of feeding experiment, the survival rate of fish fed with BA300 diet was increased (P < 0.05). Histological analysis revealed an improvement of gut structural integrity in the BA150 and BA300 groups. Compared with the control group, the expression of genes related to chemical barrier (mucin, lysozyme and complement 1) and physical barrier (occludin and claudin-4) was increased in the BA150 and BA300 groups (P < 0.05), and the expression of genes related to immunological barrier (interleukin [IL]-6, tumor growth factor β, IL-10, macrophage galactose-type lectin and immunoglobulin M [IgM]) was significantly increased in the BA300 group (P < 0.05), but the expression of genes related to chemical barrier (hepcidin) and immunological barrier (IL-1β, tumor necrosis factor-α, IL-6 and arginase) was significantly decreased in the BA450 group (P < 0.05). Gut microbiota composition analysis revealed that the abundance of Firmicutes was augmented prominently in the BA150 and BA300 groups (P < 0.05), while that of Actinobacteriota and Proteobacteria showed a downward trend in the BA150 and BA300 groups (P > 0.05). The results of the gut microbiota transferring experiment demonstrated an upregulation of gut barrier-related genes, including immunoglobulin Z/T (IgZ/T), IL-6, IL-1β and IL-10, by the gut microbiota transferred from the BA300 group compared with the control (P < 0.05). Feeding the BA300 diet directly to GF zebrafish resulted in enhanced expression of IgM, IgZ/T, lysozyme, occludin-2, IL-6 and IL-10 (P < 0.05). In conclusion, BAs can improve the gut barriers of fish through both direct and indirect effects mediated by the gut microbiota. KeAi Publishing 2023-04-20 /pmc/articles/PMC10208797/ /pubmed/37234949 http://dx.doi.org/10.1016/j.aninu.2023.03.008 Text en © 2023 The Authors. Publishing services by Elsevier B.V. on behalf of KeAi Communications Co. Ltd. https://creativecommons.org/licenses/by-nc-nd/4.0/This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
spellingShingle Original Research Article
Xia, Rui
Zhang, Qingshuang
Xia, Dongmei
Hao, Qiang
Ding, Qianwen
Ran, Chao
Yang, Yalin
Cao, Aizhi
Zhang, Zhen
Zhou, Zhigang
The direct and gut microbiota-mediated effects of dietary bile acids on the improvement of gut barriers in largemouth bass (Micropterus salmoides)
title The direct and gut microbiota-mediated effects of dietary bile acids on the improvement of gut barriers in largemouth bass (Micropterus salmoides)
title_full The direct and gut microbiota-mediated effects of dietary bile acids on the improvement of gut barriers in largemouth bass (Micropterus salmoides)
title_fullStr The direct and gut microbiota-mediated effects of dietary bile acids on the improvement of gut barriers in largemouth bass (Micropterus salmoides)
title_full_unstemmed The direct and gut microbiota-mediated effects of dietary bile acids on the improvement of gut barriers in largemouth bass (Micropterus salmoides)
title_short The direct and gut microbiota-mediated effects of dietary bile acids on the improvement of gut barriers in largemouth bass (Micropterus salmoides)
title_sort direct and gut microbiota-mediated effects of dietary bile acids on the improvement of gut barriers in largemouth bass (micropterus salmoides)
topic Original Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10208797/
https://www.ncbi.nlm.nih.gov/pubmed/37234949
http://dx.doi.org/10.1016/j.aninu.2023.03.008
work_keys_str_mv AT xiarui thedirectandgutmicrobiotamediatedeffectsofdietarybileacidsontheimprovementofgutbarriersinlargemouthbassmicropterussalmoides
AT zhangqingshuang thedirectandgutmicrobiotamediatedeffectsofdietarybileacidsontheimprovementofgutbarriersinlargemouthbassmicropterussalmoides
AT xiadongmei thedirectandgutmicrobiotamediatedeffectsofdietarybileacidsontheimprovementofgutbarriersinlargemouthbassmicropterussalmoides
AT haoqiang thedirectandgutmicrobiotamediatedeffectsofdietarybileacidsontheimprovementofgutbarriersinlargemouthbassmicropterussalmoides
AT dingqianwen thedirectandgutmicrobiotamediatedeffectsofdietarybileacidsontheimprovementofgutbarriersinlargemouthbassmicropterussalmoides
AT ranchao thedirectandgutmicrobiotamediatedeffectsofdietarybileacidsontheimprovementofgutbarriersinlargemouthbassmicropterussalmoides
AT yangyalin thedirectandgutmicrobiotamediatedeffectsofdietarybileacidsontheimprovementofgutbarriersinlargemouthbassmicropterussalmoides
AT caoaizhi thedirectandgutmicrobiotamediatedeffectsofdietarybileacidsontheimprovementofgutbarriersinlargemouthbassmicropterussalmoides
AT zhangzhen thedirectandgutmicrobiotamediatedeffectsofdietarybileacidsontheimprovementofgutbarriersinlargemouthbassmicropterussalmoides
AT zhouzhigang thedirectandgutmicrobiotamediatedeffectsofdietarybileacidsontheimprovementofgutbarriersinlargemouthbassmicropterussalmoides
AT xiarui directandgutmicrobiotamediatedeffectsofdietarybileacidsontheimprovementofgutbarriersinlargemouthbassmicropterussalmoides
AT zhangqingshuang directandgutmicrobiotamediatedeffectsofdietarybileacidsontheimprovementofgutbarriersinlargemouthbassmicropterussalmoides
AT xiadongmei directandgutmicrobiotamediatedeffectsofdietarybileacidsontheimprovementofgutbarriersinlargemouthbassmicropterussalmoides
AT haoqiang directandgutmicrobiotamediatedeffectsofdietarybileacidsontheimprovementofgutbarriersinlargemouthbassmicropterussalmoides
AT dingqianwen directandgutmicrobiotamediatedeffectsofdietarybileacidsontheimprovementofgutbarriersinlargemouthbassmicropterussalmoides
AT ranchao directandgutmicrobiotamediatedeffectsofdietarybileacidsontheimprovementofgutbarriersinlargemouthbassmicropterussalmoides
AT yangyalin directandgutmicrobiotamediatedeffectsofdietarybileacidsontheimprovementofgutbarriersinlargemouthbassmicropterussalmoides
AT caoaizhi directandgutmicrobiotamediatedeffectsofdietarybileacidsontheimprovementofgutbarriersinlargemouthbassmicropterussalmoides
AT zhangzhen directandgutmicrobiotamediatedeffectsofdietarybileacidsontheimprovementofgutbarriersinlargemouthbassmicropterussalmoides
AT zhouzhigang directandgutmicrobiotamediatedeffectsofdietarybileacidsontheimprovementofgutbarriersinlargemouthbassmicropterussalmoides