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Microbiome–host co-oscillation patterns in remodeling of colonic homeostasis during adaptation to a high-grain diet in a sheep model

BACKGROUND: Ruminant gastrointestinal tract homeostasis deploys interactive microbiome–host metabolic communication and signaling axes to underpin the fitness of the host. After this stable niche is destroyed by environmental triggers, remodeling of homeostasis can occur as a spontaneous physiologic...

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Autores principales: Lin, Limei, Wang, Yue, Xu, Lei, Liu, Junhua, Zhu, Weiyun, Mao, Shengyong
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7807687/
https://www.ncbi.nlm.nih.gov/pubmed/33499965
http://dx.doi.org/10.1186/s42523-020-00041-9
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author Lin, Limei
Wang, Yue
Xu, Lei
Liu, Junhua
Zhu, Weiyun
Mao, Shengyong
author_facet Lin, Limei
Wang, Yue
Xu, Lei
Liu, Junhua
Zhu, Weiyun
Mao, Shengyong
author_sort Lin, Limei
collection PubMed
description BACKGROUND: Ruminant gastrointestinal tract homeostasis deploys interactive microbiome–host metabolic communication and signaling axes to underpin the fitness of the host. After this stable niche is destroyed by environmental triggers, remodeling of homeostasis can occur as a spontaneous physiological compensatory actor. RESULTS: In this study, 20 sheep were randomly divided into four groups: a hay-fed control (CON) group and a high-grain (HG) diet group for 7, 14, or 28 days. Then, we examined 16S rRNA gene sequences and transcriptome sequences to outline the microbiome–host co-oscillation patterns in remodeling of colonic homeostasis in a sheep model during adaptation to a HG diet. Our data revealed that with durations of an HG diet, the higher starch levels directly affected the colonic lumen environment (lower pH and higher fermentation parameters), which in turn filtered lumen-specific functional taxonomic groups (HG-sensitive and HG-tolerant taxa). The colonic epithelium then gave rise to a new niche that triggered endoplasmic reticulum stress to activate unfolded protein response, if the duration of endoplasmic reticulum stress was overlong, this process would regulate cell apoptosis (Caspase-3, Caspase-8, and TNFRSF21) to achieve a functional transformation. CONCLUSIONS: Our results provide a holistic view of the colonic microbial assemblages and epithelium functional profile co-oscillation patterns in remodeling of colonic homeostasis during adaptation to an HG diet in a sheep model. These findings also provide a proof of concept that the microbe–host collaboration is vital for maintaining hindgut homeostasis to adapt to dietary dichotomies.
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spelling pubmed-78076872021-01-19 Microbiome–host co-oscillation patterns in remodeling of colonic homeostasis during adaptation to a high-grain diet in a sheep model Lin, Limei Wang, Yue Xu, Lei Liu, Junhua Zhu, Weiyun Mao, Shengyong Anim Microbiome Research Article BACKGROUND: Ruminant gastrointestinal tract homeostasis deploys interactive microbiome–host metabolic communication and signaling axes to underpin the fitness of the host. After this stable niche is destroyed by environmental triggers, remodeling of homeostasis can occur as a spontaneous physiological compensatory actor. RESULTS: In this study, 20 sheep were randomly divided into four groups: a hay-fed control (CON) group and a high-grain (HG) diet group for 7, 14, or 28 days. Then, we examined 16S rRNA gene sequences and transcriptome sequences to outline the microbiome–host co-oscillation patterns in remodeling of colonic homeostasis in a sheep model during adaptation to a HG diet. Our data revealed that with durations of an HG diet, the higher starch levels directly affected the colonic lumen environment (lower pH and higher fermentation parameters), which in turn filtered lumen-specific functional taxonomic groups (HG-sensitive and HG-tolerant taxa). The colonic epithelium then gave rise to a new niche that triggered endoplasmic reticulum stress to activate unfolded protein response, if the duration of endoplasmic reticulum stress was overlong, this process would regulate cell apoptosis (Caspase-3, Caspase-8, and TNFRSF21) to achieve a functional transformation. CONCLUSIONS: Our results provide a holistic view of the colonic microbial assemblages and epithelium functional profile co-oscillation patterns in remodeling of colonic homeostasis during adaptation to an HG diet in a sheep model. These findings also provide a proof of concept that the microbe–host collaboration is vital for maintaining hindgut homeostasis to adapt to dietary dichotomies. BioMed Central 2020-07-09 /pmc/articles/PMC7807687/ /pubmed/33499965 http://dx.doi.org/10.1186/s42523-020-00041-9 Text en © The Author(s) 2020 Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Research Article
Lin, Limei
Wang, Yue
Xu, Lei
Liu, Junhua
Zhu, Weiyun
Mao, Shengyong
Microbiome–host co-oscillation patterns in remodeling of colonic homeostasis during adaptation to a high-grain diet in a sheep model
title Microbiome–host co-oscillation patterns in remodeling of colonic homeostasis during adaptation to a high-grain diet in a sheep model
title_full Microbiome–host co-oscillation patterns in remodeling of colonic homeostasis during adaptation to a high-grain diet in a sheep model
title_fullStr Microbiome–host co-oscillation patterns in remodeling of colonic homeostasis during adaptation to a high-grain diet in a sheep model
title_full_unstemmed Microbiome–host co-oscillation patterns in remodeling of colonic homeostasis during adaptation to a high-grain diet in a sheep model
title_short Microbiome–host co-oscillation patterns in remodeling of colonic homeostasis during adaptation to a high-grain diet in a sheep model
title_sort microbiome–host co-oscillation patterns in remodeling of colonic homeostasis during adaptation to a high-grain diet in a sheep model
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7807687/
https://www.ncbi.nlm.nih.gov/pubmed/33499965
http://dx.doi.org/10.1186/s42523-020-00041-9
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