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The Regulation of Ruminal Short-Chain Fatty Acids on the Functions of Rumen Barriers

The rumen barriers, constituted by the microbial, physical and immune barrier, prevent the transmission of pathogens and toxins to the host tissue in the maintenance of host-microbe homeostasis. Ruminal short-chain fatty acids (SCFAs), which are the important signaling molecules derived from the rum...

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Autores principales: Shen, Hong, Xu, Zhihui, Shen, Zanming, Lu, Zhongyan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6842973/
https://www.ncbi.nlm.nih.gov/pubmed/31749707
http://dx.doi.org/10.3389/fphys.2019.01305
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author Shen, Hong
Xu, Zhihui
Shen, Zanming
Lu, Zhongyan
author_facet Shen, Hong
Xu, Zhihui
Shen, Zanming
Lu, Zhongyan
author_sort Shen, Hong
collection PubMed
description The rumen barriers, constituted by the microbial, physical and immune barrier, prevent the transmission of pathogens and toxins to the host tissue in the maintenance of host-microbe homeostasis. Ruminal short-chain fatty acids (SCFAs), which are the important signaling molecules derived from the rumen microbiota, regulate a variety of physiological functions of the rumen. So far, how the ruminal SCFAs regulate the function of rumen barriers is unclear. By the combined methods of transcriptome sequencing, 16S rRNA gene sequencing, and metagenome shotgun sequencing, we have investigated the regulatory effects of ruminal SCFAs on the functions of rumen barriers, by determining the composition and functions of epimural microbiota and on the structure and immunity of the rumen epithelium in goats receiving a 10% (LC group), 35% (MC group), or 65% concentrate diet (HC group). We found that, when the dietary concentrate shifted from 10 to 35%, the increase of total SCFA is associated with the diversification of epimural microbiota and the diversity of its gene pool. Within the microbial community, the relative abundance of genera Sphingobium, Acinetobacter, and Streptococcus increase mostly. Meantime, the signals on pathways concerning the mechanical connections and growth homeostasis in the rumen epithelium were upregulated. Under these conditions, the responses of immune components in the rumen epithelium decrease. However, when the dietary concentrate shifted from 35 to 65%, the increase of acetate and reduction of pH decrease the diversity of epimural microbiota and the diversity of its gene pool. Within the microbial community, the relative abundance of genera Sphingobium, Acinetobacter, and Streptococcus significantly decrease. Concomitantly, the signals on pathways concerning the cell growth and tight junction disruption were upregulated, while the signals on pathways concerning paracellular permeability were downregulated. Under these conditions, the signals on the pathways relating to the immune components increase. Our data thus indicates that diet-SCFA axis maintains the host-microbe homeostasis via promoting the diversification of epimural microbiota and maintaining the integrity of rumen epithelium in healthy animals, while via enhancing the activities of immune barrier in animal with lower rumen pH.
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spelling pubmed-68429732019-11-20 The Regulation of Ruminal Short-Chain Fatty Acids on the Functions of Rumen Barriers Shen, Hong Xu, Zhihui Shen, Zanming Lu, Zhongyan Front Physiol Physiology The rumen barriers, constituted by the microbial, physical and immune barrier, prevent the transmission of pathogens and toxins to the host tissue in the maintenance of host-microbe homeostasis. Ruminal short-chain fatty acids (SCFAs), which are the important signaling molecules derived from the rumen microbiota, regulate a variety of physiological functions of the rumen. So far, how the ruminal SCFAs regulate the function of rumen barriers is unclear. By the combined methods of transcriptome sequencing, 16S rRNA gene sequencing, and metagenome shotgun sequencing, we have investigated the regulatory effects of ruminal SCFAs on the functions of rumen barriers, by determining the composition and functions of epimural microbiota and on the structure and immunity of the rumen epithelium in goats receiving a 10% (LC group), 35% (MC group), or 65% concentrate diet (HC group). We found that, when the dietary concentrate shifted from 10 to 35%, the increase of total SCFA is associated with the diversification of epimural microbiota and the diversity of its gene pool. Within the microbial community, the relative abundance of genera Sphingobium, Acinetobacter, and Streptococcus increase mostly. Meantime, the signals on pathways concerning the mechanical connections and growth homeostasis in the rumen epithelium were upregulated. Under these conditions, the responses of immune components in the rumen epithelium decrease. However, when the dietary concentrate shifted from 35 to 65%, the increase of acetate and reduction of pH decrease the diversity of epimural microbiota and the diversity of its gene pool. Within the microbial community, the relative abundance of genera Sphingobium, Acinetobacter, and Streptococcus significantly decrease. Concomitantly, the signals on pathways concerning the cell growth and tight junction disruption were upregulated, while the signals on pathways concerning paracellular permeability were downregulated. Under these conditions, the signals on the pathways relating to the immune components increase. Our data thus indicates that diet-SCFA axis maintains the host-microbe homeostasis via promoting the diversification of epimural microbiota and maintaining the integrity of rumen epithelium in healthy animals, while via enhancing the activities of immune barrier in animal with lower rumen pH. Frontiers Media S.A. 2019-10-25 /pmc/articles/PMC6842973/ /pubmed/31749707 http://dx.doi.org/10.3389/fphys.2019.01305 Text en Copyright © 2019 Shen, Xu, Shen and Lu. https://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 Physiology
Shen, Hong
Xu, Zhihui
Shen, Zanming
Lu, Zhongyan
The Regulation of Ruminal Short-Chain Fatty Acids on the Functions of Rumen Barriers
title The Regulation of Ruminal Short-Chain Fatty Acids on the Functions of Rumen Barriers
title_full The Regulation of Ruminal Short-Chain Fatty Acids on the Functions of Rumen Barriers
title_fullStr The Regulation of Ruminal Short-Chain Fatty Acids on the Functions of Rumen Barriers
title_full_unstemmed The Regulation of Ruminal Short-Chain Fatty Acids on the Functions of Rumen Barriers
title_short The Regulation of Ruminal Short-Chain Fatty Acids on the Functions of Rumen Barriers
title_sort regulation of ruminal short-chain fatty acids on the functions of rumen barriers
topic Physiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6842973/
https://www.ncbi.nlm.nih.gov/pubmed/31749707
http://dx.doi.org/10.3389/fphys.2019.01305
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