Multi-Omics Reveals That the Rumen Transcriptome, Microbiome, and Its Metabolome Co-regulate Cold Season Adaptability of Tibetan Sheep

Tibetan sheep can maintain a normal life and reproduce in harsh environments under extreme cold and lack of nutrition. However, the molecular and metabolic mechanisms underlying the adaptability of Tibetan sheep during the cold season are still unclear. Hence, we conducted a comprehensive analysis o...

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Main Authors: Xiu Liu, Yuzhu Sha, Weibing Lv, Guizhong Cao, Xinyu Guo, Xiaoning Pu, Jiqing Wang, Shaobin Li, Jiang Hu, Yuzhu Luo
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-04-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2022.859601/full
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author Xiu Liu
Yuzhu Sha
Weibing Lv
Guizhong Cao
Xinyu Guo
Xiaoning Pu
Jiqing Wang
Shaobin Li
Jiang Hu
Yuzhu Luo
author_facet Xiu Liu
Yuzhu Sha
Weibing Lv
Guizhong Cao
Xinyu Guo
Xiaoning Pu
Jiqing Wang
Shaobin Li
Jiang Hu
Yuzhu Luo
author_sort Xiu Liu
collection DOAJ
description Tibetan sheep can maintain a normal life and reproduce in harsh environments under extreme cold and lack of nutrition. However, the molecular and metabolic mechanisms underlying the adaptability of Tibetan sheep during the cold season are still unclear. Hence, we conducted a comprehensive analysis of rumen epithelial morphology, epithelial transcriptomics, microbiology and metabolomics in a Tibetan sheep model. The results showed that morphological structure of rumen epithelium of Tibetan sheep in cold season had adaptive changes. Transcriptomics analysis showed that the differential genes were primarily enriched in the PPAR signaling pathway (ko03320), legionellosis (ko05134), phagosome (ko04145), arginine and proline metabolism (ko00330), and metabolism of xenobiotics by cytochrome P450 (ko00980). Unique differential metabolites were identified in cold season, such as cynaroside A, sanguisorbin B and tryptophyl-valine, which were mainly enriched in arachidonic acid metabolism, arachidonic acid metabolism and linolenic acid metabolism pathways, and had certain correlation with microorganisms. Integrated transcriptome-metabolome-microbiome analysis showed that epithelial gene-GSTM3 expression was upregulated in the metabolism of xenobiotics by the cytochrome P450 pathway during the cold season, leading to the downregulation of some harmful metabolites; TLR5 gene expression was upregulated and CD14 gene expression was downregulated in the legionellosis pathway during the cold season. This study comprehensively described the interaction mechanism between the rumen host and microbes and their metabolites in grazing Tibetan sheep during the cold season. Rumen epithelial genes, microbiota and metabolites act together in some key pathways related to cold season adaptation.
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spelling doaj.art-1d3d8992c55f4fd6870874e2afb9fc9f2022-12-22T02:06:54ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2022-04-011310.3389/fmicb.2022.859601859601Multi-Omics Reveals That the Rumen Transcriptome, Microbiome, and Its Metabolome Co-regulate Cold Season Adaptability of Tibetan SheepXiu Liu0Yuzhu Sha1Weibing Lv2Guizhong Cao3Xinyu Guo4Xiaoning Pu5Jiqing Wang6Shaobin Li7Jiang Hu8Yuzhu Luo9Gansu Key Laboratory of Herbivorous Animal Biotechnology, College of Animal Science and Technology, Gansu Agricultural University, Lanzhou, ChinaGansu Key Laboratory of Herbivorous Animal Biotechnology, College of Animal Science and Technology, Gansu Agricultural University, Lanzhou, ChinaGansu Key Laboratory of Herbivorous Animal Biotechnology, College of Animal Science and Technology, Gansu Agricultural University, Lanzhou, ChinaAnimal Husbandry and Veterinary Station in Huangyuan County, Xining, ChinaGansu Key Laboratory of Herbivorous Animal Biotechnology, College of Animal Science and Technology, Gansu Agricultural University, Lanzhou, ChinaGansu Key Laboratory of Herbivorous Animal Biotechnology, College of Animal Science and Technology, Gansu Agricultural University, Lanzhou, ChinaGansu Key Laboratory of Herbivorous Animal Biotechnology, College of Animal Science and Technology, Gansu Agricultural University, Lanzhou, ChinaGansu Key Laboratory of Herbivorous Animal Biotechnology, College of Animal Science and Technology, Gansu Agricultural University, Lanzhou, ChinaGansu Key Laboratory of Herbivorous Animal Biotechnology, College of Animal Science and Technology, Gansu Agricultural University, Lanzhou, ChinaGansu Key Laboratory of Herbivorous Animal Biotechnology, College of Animal Science and Technology, Gansu Agricultural University, Lanzhou, ChinaTibetan sheep can maintain a normal life and reproduce in harsh environments under extreme cold and lack of nutrition. However, the molecular and metabolic mechanisms underlying the adaptability of Tibetan sheep during the cold season are still unclear. Hence, we conducted a comprehensive analysis of rumen epithelial morphology, epithelial transcriptomics, microbiology and metabolomics in a Tibetan sheep model. The results showed that morphological structure of rumen epithelium of Tibetan sheep in cold season had adaptive changes. Transcriptomics analysis showed that the differential genes were primarily enriched in the PPAR signaling pathway (ko03320), legionellosis (ko05134), phagosome (ko04145), arginine and proline metabolism (ko00330), and metabolism of xenobiotics by cytochrome P450 (ko00980). Unique differential metabolites were identified in cold season, such as cynaroside A, sanguisorbin B and tryptophyl-valine, which were mainly enriched in arachidonic acid metabolism, arachidonic acid metabolism and linolenic acid metabolism pathways, and had certain correlation with microorganisms. Integrated transcriptome-metabolome-microbiome analysis showed that epithelial gene-GSTM3 expression was upregulated in the metabolism of xenobiotics by the cytochrome P450 pathway during the cold season, leading to the downregulation of some harmful metabolites; TLR5 gene expression was upregulated and CD14 gene expression was downregulated in the legionellosis pathway during the cold season. This study comprehensively described the interaction mechanism between the rumen host and microbes and their metabolites in grazing Tibetan sheep during the cold season. Rumen epithelial genes, microbiota and metabolites act together in some key pathways related to cold season adaptation.https://www.frontiersin.org/articles/10.3389/fmicb.2022.859601/fullTibetan sheeprumentranscriptomemicroorganismmetabolomecold season
spellingShingle Xiu Liu
Yuzhu Sha
Weibing Lv
Guizhong Cao
Xinyu Guo
Xiaoning Pu
Jiqing Wang
Shaobin Li
Jiang Hu
Yuzhu Luo
Multi-Omics Reveals That the Rumen Transcriptome, Microbiome, and Its Metabolome Co-regulate Cold Season Adaptability of Tibetan Sheep
Frontiers in Microbiology
Tibetan sheep
rumen
transcriptome
microorganism
metabolome
cold season
title Multi-Omics Reveals That the Rumen Transcriptome, Microbiome, and Its Metabolome Co-regulate Cold Season Adaptability of Tibetan Sheep
title_full Multi-Omics Reveals That the Rumen Transcriptome, Microbiome, and Its Metabolome Co-regulate Cold Season Adaptability of Tibetan Sheep
title_fullStr Multi-Omics Reveals That the Rumen Transcriptome, Microbiome, and Its Metabolome Co-regulate Cold Season Adaptability of Tibetan Sheep
title_full_unstemmed Multi-Omics Reveals That the Rumen Transcriptome, Microbiome, and Its Metabolome Co-regulate Cold Season Adaptability of Tibetan Sheep
title_short Multi-Omics Reveals That the Rumen Transcriptome, Microbiome, and Its Metabolome Co-regulate Cold Season Adaptability of Tibetan Sheep
title_sort multi omics reveals that the rumen transcriptome microbiome and its metabolome co regulate cold season adaptability of tibetan sheep
topic Tibetan sheep
rumen
transcriptome
microorganism
metabolome
cold season
url https://www.frontiersin.org/articles/10.3389/fmicb.2022.859601/full
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