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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Frontiers Media S.A.
2018-08-01
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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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language | English |
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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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