The epithelial transcriptome and mucosal microbiota are altered for goats fed with a low-protein diet

IntroductionFeeding low protein (LP) diet to animals impose severe challenge to animals' immune homeostasis. However, limited knowledge about the underlying adaption mechanism of host and ruminal microbiota responding to LP diet were well understood. Herein, this study was performed to examine...

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Main Authors: Jian Wu, Changxin Tian, Jinzhen Jiao, Qiongxian Yan, Chuanshe Zhou, Zhiliang Tan
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-09-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2023.1237955/full
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author Jian Wu
Jian Wu
Jian Wu
Changxin Tian
Changxin Tian
Changxin Tian
Changxin Tian
Jinzhen Jiao
Jinzhen Jiao
Jinzhen Jiao
Qiongxian Yan
Qiongxian Yan
Qiongxian Yan
Chuanshe Zhou
Chuanshe Zhou
Chuanshe Zhou
Zhiliang Tan
Zhiliang Tan
Zhiliang Tan
author_facet Jian Wu
Jian Wu
Jian Wu
Changxin Tian
Changxin Tian
Changxin Tian
Changxin Tian
Jinzhen Jiao
Jinzhen Jiao
Jinzhen Jiao
Qiongxian Yan
Qiongxian Yan
Qiongxian Yan
Chuanshe Zhou
Chuanshe Zhou
Chuanshe Zhou
Zhiliang Tan
Zhiliang Tan
Zhiliang Tan
author_sort Jian Wu
collection DOAJ
description IntroductionFeeding low protein (LP) diet to animals impose severe challenge to animals' immune homeostasis. However, limited knowledge about the underlying adaption mechanism of host and ruminal microbiota responding to LP diet were well understood. Herein, this study was performed to examine the changes in relative abundance of ruminal microbiota and host ruminal mucosal transcriptome profiles in response to a LP diet.MethodsA total of twenty-four female Xiangdong balck goats with similar weight (20.64 ± 2.40 kg) and age (8 ± 0.3 months) were randomly assigned into two groups, LP (5.52% crude protein containing diet) and CON (10.77% crude protein containing diet) groups. Upon completion of the trial, all goats were slaughtered after a 16-hour fasting period in LiuYang city (N 28°15′, E 113°63′) in China. HE staining, free amino acids measurement, transcriptome analysis and microbiome analysis were applied to detect the morphology alterations, free amino acids profile alterations and the shift in host ruminal mucosal transcriptome and ruminal microbiota communities.ResultsFirstly, the results showed that feeding LP diet to goats decreased the rumen papilla width (P = 0.043), surface area (P = 0.013) and total ruminal free amino acids concentration (P = 0.016). Secondly, microbiome analysis indicated that 9 microbial genera, including Eubacterium and Prevotella, were enriched in LP group while 11 microbial genera, including Butyrivibrio and Ruminococcus, were enriched in CON group. Finally, in terms of immune-related genes, the expression levels of genes involved in tight junction categories (e.g., MYH11, PPP2R2C, and MYL9) and acquired immunity (e.g., PCP4 and CXCL13) were observed to be upregulated in the LP group when compared to the CON group.ConclusionUnder the LP diet, the rumen exhibited increased relative abundance of pathogenic microbiota and VFA-degrading microbiota, leading to disruptions in immune homeostasis within the host's ruminal mucosa. These findings indicate that the ruminal microbiota interacts with host results in the disruption in animals' immune homeostasis under LP diet challenge.
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spelling doaj.art-5e4ce02ec33d4486bddb2bc73190efea2023-09-04T09:22:38ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-09-011410.3389/fmicb.2023.12379551237955The epithelial transcriptome and mucosal microbiota are altered for goats fed with a low-protein dietJian Wu0Jian Wu1Jian Wu2Changxin Tian3Changxin Tian4Changxin Tian5Changxin Tian6Jinzhen Jiao7Jinzhen Jiao8Jinzhen Jiao9Qiongxian Yan10Qiongxian Yan11Qiongxian Yan12Chuanshe Zhou13Chuanshe Zhou14Chuanshe Zhou15Zhiliang Tan16Zhiliang Tan17Zhiliang Tan18CAS Key Laboratory of Agro-ecological Processes in Subtropical Region, Institute of Subtropical Agriculture, Chinese Academy of Sciences, Changsha, Hunan, ChinaNational Engineering Laboratory for Pollution Control and Waste Utilization in Livestock and Poultry Production, Institute of Subtropical Agriculture, Chinese Academy of Sciences, Changsha, Hunan, ChinaHunan Provincial Key Laboratory of Animal Nutritional Physiology and Metabolic Process, Institute of Subtropical Agriculture, Chinese Academy of Sciences, Changsha, Hunan, ChinaCAS Key Laboratory of Agro-ecological Processes in Subtropical Region, Institute of Subtropical Agriculture, Chinese Academy of Sciences, Changsha, Hunan, ChinaNational Engineering Laboratory for Pollution Control and Waste Utilization in Livestock and Poultry Production, Institute of Subtropical Agriculture, Chinese Academy of Sciences, Changsha, Hunan, ChinaHunan Provincial Key Laboratory of Animal Nutritional Physiology and Metabolic Process, Institute of Subtropical Agriculture, Chinese Academy of Sciences, Changsha, Hunan, ChinaUniversity of Chinese Academy of Sciences, Beijing, ChinaCAS Key Laboratory of Agro-ecological Processes in Subtropical Region, Institute of Subtropical Agriculture, Chinese Academy of Sciences, Changsha, Hunan, ChinaNational Engineering Laboratory for Pollution Control and Waste Utilization in Livestock and Poultry Production, Institute of Subtropical Agriculture, Chinese Academy of Sciences, Changsha, Hunan, ChinaHunan Provincial Key Laboratory of Animal Nutritional Physiology and Metabolic Process, Institute of Subtropical Agriculture, Chinese Academy of Sciences, Changsha, Hunan, ChinaCAS Key Laboratory of Agro-ecological Processes in Subtropical Region, Institute of Subtropical Agriculture, Chinese Academy of Sciences, Changsha, Hunan, ChinaNational Engineering Laboratory for Pollution Control and Waste Utilization in Livestock and Poultry Production, Institute of Subtropical Agriculture, Chinese Academy of Sciences, Changsha, Hunan, ChinaHunan Provincial Key Laboratory of Animal Nutritional Physiology and Metabolic Process, Institute of Subtropical Agriculture, Chinese Academy of Sciences, Changsha, Hunan, ChinaCAS Key Laboratory of Agro-ecological Processes in Subtropical Region, Institute of Subtropical Agriculture, Chinese Academy of Sciences, Changsha, Hunan, ChinaNational Engineering Laboratory for Pollution Control and Waste Utilization in Livestock and Poultry Production, Institute of Subtropical Agriculture, Chinese Academy of Sciences, Changsha, Hunan, ChinaHunan Provincial Key Laboratory of Animal Nutritional Physiology and Metabolic Process, Institute of Subtropical Agriculture, Chinese Academy of Sciences, Changsha, Hunan, ChinaCAS Key Laboratory of Agro-ecological Processes in Subtropical Region, Institute of Subtropical Agriculture, Chinese Academy of Sciences, Changsha, Hunan, ChinaNational Engineering Laboratory for Pollution Control and Waste Utilization in Livestock and Poultry Production, Institute of Subtropical Agriculture, Chinese Academy of Sciences, Changsha, Hunan, ChinaHunan Provincial Key Laboratory of Animal Nutritional Physiology and Metabolic Process, Institute of Subtropical Agriculture, Chinese Academy of Sciences, Changsha, Hunan, ChinaIntroductionFeeding low protein (LP) diet to animals impose severe challenge to animals' immune homeostasis. However, limited knowledge about the underlying adaption mechanism of host and ruminal microbiota responding to LP diet were well understood. Herein, this study was performed to examine the changes in relative abundance of ruminal microbiota and host ruminal mucosal transcriptome profiles in response to a LP diet.MethodsA total of twenty-four female Xiangdong balck goats with similar weight (20.64 ± 2.40 kg) and age (8 ± 0.3 months) were randomly assigned into two groups, LP (5.52% crude protein containing diet) and CON (10.77% crude protein containing diet) groups. Upon completion of the trial, all goats were slaughtered after a 16-hour fasting period in LiuYang city (N 28°15′, E 113°63′) in China. HE staining, free amino acids measurement, transcriptome analysis and microbiome analysis were applied to detect the morphology alterations, free amino acids profile alterations and the shift in host ruminal mucosal transcriptome and ruminal microbiota communities.ResultsFirstly, the results showed that feeding LP diet to goats decreased the rumen papilla width (P = 0.043), surface area (P = 0.013) and total ruminal free amino acids concentration (P = 0.016). Secondly, microbiome analysis indicated that 9 microbial genera, including Eubacterium and Prevotella, were enriched in LP group while 11 microbial genera, including Butyrivibrio and Ruminococcus, were enriched in CON group. Finally, in terms of immune-related genes, the expression levels of genes involved in tight junction categories (e.g., MYH11, PPP2R2C, and MYL9) and acquired immunity (e.g., PCP4 and CXCL13) were observed to be upregulated in the LP group when compared to the CON group.ConclusionUnder the LP diet, the rumen exhibited increased relative abundance of pathogenic microbiota and VFA-degrading microbiota, leading to disruptions in immune homeostasis within the host's ruminal mucosa. These findings indicate that the ruminal microbiota interacts with host results in the disruption in animals' immune homeostasis under LP diet challenge.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1237955/fullimmune homeostasislow protein dietmicrobiometranscriptomegoat
spellingShingle Jian Wu
Jian Wu
Jian Wu
Changxin Tian
Changxin Tian
Changxin Tian
Changxin Tian
Jinzhen Jiao
Jinzhen Jiao
Jinzhen Jiao
Qiongxian Yan
Qiongxian Yan
Qiongxian Yan
Chuanshe Zhou
Chuanshe Zhou
Chuanshe Zhou
Zhiliang Tan
Zhiliang Tan
Zhiliang Tan
The epithelial transcriptome and mucosal microbiota are altered for goats fed with a low-protein diet
Frontiers in Microbiology
immune homeostasis
low protein diet
microbiome
transcriptome
goat
title The epithelial transcriptome and mucosal microbiota are altered for goats fed with a low-protein diet
title_full The epithelial transcriptome and mucosal microbiota are altered for goats fed with a low-protein diet
title_fullStr The epithelial transcriptome and mucosal microbiota are altered for goats fed with a low-protein diet
title_full_unstemmed The epithelial transcriptome and mucosal microbiota are altered for goats fed with a low-protein diet
title_short The epithelial transcriptome and mucosal microbiota are altered for goats fed with a low-protein diet
title_sort epithelial transcriptome and mucosal microbiota are altered for goats fed with a low protein diet
topic immune homeostasis
low protein diet
microbiome
transcriptome
goat
url https://www.frontiersin.org/articles/10.3389/fmicb.2023.1237955/full
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