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Supplemental Xylooligosaccharide Modulates Intestinal Mucosal Barrier and Cecal Microbiota in Laying Hens Fed Oxidized Fish Oil

Our previous study indicated that dietary xylooligosaccharide (XOS) supplementation improved feed efficiency, ileal morphology, and nutrient digestibility in laying hens. The objective of this study was to evaluate the mitigative effects of XOS on intestinal mucosal barrier impairment and microbiota...

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Autores principales: Zhou, Jian-min, Zhang, Hai-jun, Wu, Shu-geng, Qiu, Kai, Fu, Yu, Qi, Guang-hai, Wang, Jing
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7937631/
https://www.ncbi.nlm.nih.gov/pubmed/33692770
http://dx.doi.org/10.3389/fmicb.2021.635333
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author Zhou, Jian-min
Zhang, Hai-jun
Wu, Shu-geng
Qiu, Kai
Fu, Yu
Qi, Guang-hai
Wang, Jing
author_facet Zhou, Jian-min
Zhang, Hai-jun
Wu, Shu-geng
Qiu, Kai
Fu, Yu
Qi, Guang-hai
Wang, Jing
author_sort Zhou, Jian-min
collection PubMed
description Our previous study indicated that dietary xylooligosaccharide (XOS) supplementation improved feed efficiency, ileal morphology, and nutrient digestibility in laying hens. The objective of this study was to evaluate the mitigative effects of XOS on intestinal mucosal barrier impairment and microbiota dysbiosis induced by oxidized fish oil (OFO) in laying hens. A total of 384 Hy-Line Brown layers at 50 weeks of age were randomly divided into four dietary treatments, including the diets supplemented with 20 g/kg of fresh fish oil (FFO group) or 20 g/kg of oxidized fish oil (OFO group), and the OFO diets with XOS addition at 200 mg/kg (OFO/XOS(200) group) or 400 mg/kg (OFO/XOS(400) group). Each treatment had eight replicates with 12 birds each. The OFO treatment decreased (P < 0.05) the production performance of birds from 7 to 12 weeks of the experiment, reduced (P < 0.05) ileal mucosal secretory immunoglobulin A (sIgA) content, and increased (P < 0.05) serum endotoxin concentration, as well as downregulated (P < 0.05) mRNA expression of claudin-1 (CLDN1) and claudin-5 (CLDN5) in the ileal mucosa at the end of the experiment. Dietary XOS addition (400 mg/kg) recovered (P < 0.05) these changes and further improved (P < 0.05) ileal villus height (VH) and the villus height-to-crypt depth ratio (VCR). In addition, OFO treatment altered cecal microbial composition of layers, and these alterations were probably involved in OFO-induced ileal mucosal impairment as causes or consequences. Supplemental XOS remodeled cecal microbiota of layers fed the OFO diet, characterized by an elevation in microbial richness and changes in microbial composition, including increases in Firmicutes, Ruminococcaceae, Verrucomicrobia (Akkermansia), Paraprevotella, Prevotella_9, and Oscillospira, along with a decrease in Erysipelatoclostridium. The increased abundance of Verrucomicrobia (Akkermansia) had positive correlations with the improved ileal VH and ileal mucosal expression of CLDN1. The abundance of Erysipelatoclostridium decreased by XOS addition was negatively associated with ileal VH, VCR, ileal mucosal sIgA content, and the relative expression of zonula occludens-2, CLDN1, and CLDN5. Collectively, supplemental XOS alleviated OFO-induced intestinal mucosal barrier dysfunction and performance impairment in laying hens, which could be at least partially attributed to the modulation of gut microbiota.
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spelling pubmed-79376312021-03-09 Supplemental Xylooligosaccharide Modulates Intestinal Mucosal Barrier and Cecal Microbiota in Laying Hens Fed Oxidized Fish Oil Zhou, Jian-min Zhang, Hai-jun Wu, Shu-geng Qiu, Kai Fu, Yu Qi, Guang-hai Wang, Jing Front Microbiol Microbiology Our previous study indicated that dietary xylooligosaccharide (XOS) supplementation improved feed efficiency, ileal morphology, and nutrient digestibility in laying hens. The objective of this study was to evaluate the mitigative effects of XOS on intestinal mucosal barrier impairment and microbiota dysbiosis induced by oxidized fish oil (OFO) in laying hens. A total of 384 Hy-Line Brown layers at 50 weeks of age were randomly divided into four dietary treatments, including the diets supplemented with 20 g/kg of fresh fish oil (FFO group) or 20 g/kg of oxidized fish oil (OFO group), and the OFO diets with XOS addition at 200 mg/kg (OFO/XOS(200) group) or 400 mg/kg (OFO/XOS(400) group). Each treatment had eight replicates with 12 birds each. The OFO treatment decreased (P < 0.05) the production performance of birds from 7 to 12 weeks of the experiment, reduced (P < 0.05) ileal mucosal secretory immunoglobulin A (sIgA) content, and increased (P < 0.05) serum endotoxin concentration, as well as downregulated (P < 0.05) mRNA expression of claudin-1 (CLDN1) and claudin-5 (CLDN5) in the ileal mucosa at the end of the experiment. Dietary XOS addition (400 mg/kg) recovered (P < 0.05) these changes and further improved (P < 0.05) ileal villus height (VH) and the villus height-to-crypt depth ratio (VCR). In addition, OFO treatment altered cecal microbial composition of layers, and these alterations were probably involved in OFO-induced ileal mucosal impairment as causes or consequences. Supplemental XOS remodeled cecal microbiota of layers fed the OFO diet, characterized by an elevation in microbial richness and changes in microbial composition, including increases in Firmicutes, Ruminococcaceae, Verrucomicrobia (Akkermansia), Paraprevotella, Prevotella_9, and Oscillospira, along with a decrease in Erysipelatoclostridium. The increased abundance of Verrucomicrobia (Akkermansia) had positive correlations with the improved ileal VH and ileal mucosal expression of CLDN1. The abundance of Erysipelatoclostridium decreased by XOS addition was negatively associated with ileal VH, VCR, ileal mucosal sIgA content, and the relative expression of zonula occludens-2, CLDN1, and CLDN5. Collectively, supplemental XOS alleviated OFO-induced intestinal mucosal barrier dysfunction and performance impairment in laying hens, which could be at least partially attributed to the modulation of gut microbiota. Frontiers Media S.A. 2021-02-22 /pmc/articles/PMC7937631/ /pubmed/33692770 http://dx.doi.org/10.3389/fmicb.2021.635333 Text en Copyright © 2021 Zhou, Zhang, Wu, Qiu, Fu, Qi and Wang. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Zhou, Jian-min
Zhang, Hai-jun
Wu, Shu-geng
Qiu, Kai
Fu, Yu
Qi, Guang-hai
Wang, Jing
Supplemental Xylooligosaccharide Modulates Intestinal Mucosal Barrier and Cecal Microbiota in Laying Hens Fed Oxidized Fish Oil
title Supplemental Xylooligosaccharide Modulates Intestinal Mucosal Barrier and Cecal Microbiota in Laying Hens Fed Oxidized Fish Oil
title_full Supplemental Xylooligosaccharide Modulates Intestinal Mucosal Barrier and Cecal Microbiota in Laying Hens Fed Oxidized Fish Oil
title_fullStr Supplemental Xylooligosaccharide Modulates Intestinal Mucosal Barrier and Cecal Microbiota in Laying Hens Fed Oxidized Fish Oil
title_full_unstemmed Supplemental Xylooligosaccharide Modulates Intestinal Mucosal Barrier and Cecal Microbiota in Laying Hens Fed Oxidized Fish Oil
title_short Supplemental Xylooligosaccharide Modulates Intestinal Mucosal Barrier and Cecal Microbiota in Laying Hens Fed Oxidized Fish Oil
title_sort supplemental xylooligosaccharide modulates intestinal mucosal barrier and cecal microbiota in laying hens fed oxidized fish oil
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7937631/
https://www.ncbi.nlm.nih.gov/pubmed/33692770
http://dx.doi.org/10.3389/fmicb.2021.635333
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