Broad Bean (Vicia faba L.) Induces Intestinal Inflammation in Grass Carp (Ctenopharyngodon idellus C. et V) by Increasing Relative Abundances of Intestinal Gram-Negative and Flagellated Bacteria

Constant consumption of broad bean (Vicia faba L.) induces intestinal inflammation and reduces growth rate in grass carp (Ctenopharyngodon idellus C. et V). However, the mechanisms underlying these effects are unclear. In mammalian models of inflammatory bowel disease (IBD), endotoxin and flagellin...

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Main Authors: Zhifei Li, Ermeng Yu, Guangjun Wang, Deguang Yu, Kai Zhang, Wangbao Gong, Jun Xie
Format: Article
Language:English
Published: Frontiers Media S.A. 2018-08-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fmicb.2018.01913/full
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author Zhifei Li
Zhifei Li
Ermeng Yu
Ermeng Yu
Guangjun Wang
Guangjun Wang
Deguang Yu
Deguang Yu
Kai Zhang
Kai Zhang
Wangbao Gong
Wangbao Gong
Jun Xie
Jun Xie
author_facet Zhifei Li
Zhifei Li
Ermeng Yu
Ermeng Yu
Guangjun Wang
Guangjun Wang
Deguang Yu
Deguang Yu
Kai Zhang
Kai Zhang
Wangbao Gong
Wangbao Gong
Jun Xie
Jun Xie
author_sort Zhifei Li
collection DOAJ
description Constant consumption of broad bean (Vicia faba L.) induces intestinal inflammation and reduces growth rate in grass carp (Ctenopharyngodon idellus C. et V). However, the mechanisms underlying these effects are unclear. In mammalian models of inflammatory bowel disease (IBD), endotoxin and flagellin cause intestinal inflammation through upregulation of tumor necrosis factor (TNF)-α expression. We therefore speculated that broad bean consumption alters intestinal microbiota composition, thereby increasing the relative abundance of endotoxin-producing Gram-negative and flagellated bacteria and resulting in upregulation of TNF-α and intestinal inflammation in grass carp. We tested this hypothesis by comparing intestinal microbiota compositions of grass carp fed broad bean (GCBB), hybrid giant napier (Pennisetum sinese Roxb, GCHG), or formula feed (GCFF) by 16S rRNA gene sequencing. We also performed a histological analysis of the intestinal inner wall by scanning electron microscopy and measured intestinal wall and serum concentrations of TNF-α. Our results revealed epithelial cell damage including microvillus effacement and synechia along with increased TNF-α levels in the intestinal wall in the GCBB group as compared to the GCHG and GCFF groups. The relative abundances of Gram-negative and flagellated bacteria were also higher in the GCBB group than in the GCHG and GCFF groups; this was accompanied by upregulation of genes expressing endotoxin and flagellin in intestinal microbiota. Thus, broad bean-induced intestinal inflammation in grass carp shares features with IBD. Our findings demonstrate that the microbiome in fish is directly influenced by diet and provide a reference for deconstructing host–intestinal microbiota interactions.
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spelling doaj.art-8ad7fd4329a941618f5e32b7f08260982022-12-22T00:29:33ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2018-08-01910.3389/fmicb.2018.01913386894Broad Bean (Vicia faba L.) Induces Intestinal Inflammation in Grass Carp (Ctenopharyngodon idellus C. et V) by Increasing Relative Abundances of Intestinal Gram-Negative and Flagellated BacteriaZhifei Li0Zhifei Li1Ermeng Yu2Ermeng Yu3Guangjun Wang4Guangjun Wang5Deguang Yu6Deguang Yu7Kai Zhang8Kai Zhang9Wangbao Gong10Wangbao Gong11Jun Xie12Jun Xie13Key Laboratory of Tropical and Subtropical Fishery Resource Application and Cultivation, Pearl River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Guangzhou, ChinaGuangdong Ecological Remediation of Aquaculture Pollution Research Center, Guangzhou, ChinaKey Laboratory of Tropical and Subtropical Fishery Resource Application and Cultivation, Pearl River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Guangzhou, ChinaGuangdong Ecological Remediation of Aquaculture Pollution Research Center, Guangzhou, ChinaKey Laboratory of Tropical and Subtropical Fishery Resource Application and Cultivation, Pearl River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Guangzhou, ChinaGuangdong Ecological Remediation of Aquaculture Pollution Research Center, Guangzhou, ChinaKey Laboratory of Tropical and Subtropical Fishery Resource Application and Cultivation, Pearl River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Guangzhou, ChinaGuangdong Ecological Remediation of Aquaculture Pollution Research Center, Guangzhou, ChinaKey Laboratory of Tropical and Subtropical Fishery Resource Application and Cultivation, Pearl River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Guangzhou, ChinaGuangdong Ecological Remediation of Aquaculture Pollution Research Center, Guangzhou, ChinaKey Laboratory of Tropical and Subtropical Fishery Resource Application and Cultivation, Pearl River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Guangzhou, ChinaGuangdong Ecological Remediation of Aquaculture Pollution Research Center, Guangzhou, ChinaKey Laboratory of Tropical and Subtropical Fishery Resource Application and Cultivation, Pearl River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Guangzhou, ChinaGuangdong Ecological Remediation of Aquaculture Pollution Research Center, Guangzhou, ChinaConstant consumption of broad bean (Vicia faba L.) induces intestinal inflammation and reduces growth rate in grass carp (Ctenopharyngodon idellus C. et V). However, the mechanisms underlying these effects are unclear. In mammalian models of inflammatory bowel disease (IBD), endotoxin and flagellin cause intestinal inflammation through upregulation of tumor necrosis factor (TNF)-α expression. We therefore speculated that broad bean consumption alters intestinal microbiota composition, thereby increasing the relative abundance of endotoxin-producing Gram-negative and flagellated bacteria and resulting in upregulation of TNF-α and intestinal inflammation in grass carp. We tested this hypothesis by comparing intestinal microbiota compositions of grass carp fed broad bean (GCBB), hybrid giant napier (Pennisetum sinese Roxb, GCHG), or formula feed (GCFF) by 16S rRNA gene sequencing. We also performed a histological analysis of the intestinal inner wall by scanning electron microscopy and measured intestinal wall and serum concentrations of TNF-α. Our results revealed epithelial cell damage including microvillus effacement and synechia along with increased TNF-α levels in the intestinal wall in the GCBB group as compared to the GCHG and GCFF groups. The relative abundances of Gram-negative and flagellated bacteria were also higher in the GCBB group than in the GCHG and GCFF groups; this was accompanied by upregulation of genes expressing endotoxin and flagellin in intestinal microbiota. Thus, broad bean-induced intestinal inflammation in grass carp shares features with IBD. Our findings demonstrate that the microbiome in fish is directly influenced by diet and provide a reference for deconstructing host–intestinal microbiota interactions.https://www.frontiersin.org/article/10.3389/fmicb.2018.01913/fullgut inflammationflagellingram-negative bacteriagrass carpbroad bean
spellingShingle Zhifei Li
Zhifei Li
Ermeng Yu
Ermeng Yu
Guangjun Wang
Guangjun Wang
Deguang Yu
Deguang Yu
Kai Zhang
Kai Zhang
Wangbao Gong
Wangbao Gong
Jun Xie
Jun Xie
Broad Bean (Vicia faba L.) Induces Intestinal Inflammation in Grass Carp (Ctenopharyngodon idellus C. et V) by Increasing Relative Abundances of Intestinal Gram-Negative and Flagellated Bacteria
Frontiers in Microbiology
gut inflammation
flagellin
gram-negative bacteria
grass carp
broad bean
title Broad Bean (Vicia faba L.) Induces Intestinal Inflammation in Grass Carp (Ctenopharyngodon idellus C. et V) by Increasing Relative Abundances of Intestinal Gram-Negative and Flagellated Bacteria
title_full Broad Bean (Vicia faba L.) Induces Intestinal Inflammation in Grass Carp (Ctenopharyngodon idellus C. et V) by Increasing Relative Abundances of Intestinal Gram-Negative and Flagellated Bacteria
title_fullStr Broad Bean (Vicia faba L.) Induces Intestinal Inflammation in Grass Carp (Ctenopharyngodon idellus C. et V) by Increasing Relative Abundances of Intestinal Gram-Negative and Flagellated Bacteria
title_full_unstemmed Broad Bean (Vicia faba L.) Induces Intestinal Inflammation in Grass Carp (Ctenopharyngodon idellus C. et V) by Increasing Relative Abundances of Intestinal Gram-Negative and Flagellated Bacteria
title_short Broad Bean (Vicia faba L.) Induces Intestinal Inflammation in Grass Carp (Ctenopharyngodon idellus C. et V) by Increasing Relative Abundances of Intestinal Gram-Negative and Flagellated Bacteria
title_sort broad bean vicia faba l induces intestinal inflammation in grass carp ctenopharyngodon idellus c et v by increasing relative abundances of intestinal gram negative and flagellated bacteria
topic gut inflammation
flagellin
gram-negative bacteria
grass carp
broad bean
url https://www.frontiersin.org/article/10.3389/fmicb.2018.01913/full
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