Large-scale metagenomic assembly provide new insights into the genetic evolution of gut microbiomes in plateau ungulates

Abstract Trillions of microbes colonize the ungulate gastrointestinal tract, playing a pivotal role in enhancing host nutrient utilization by breaking down cellulose and hemicellulose present in plants. Here, through large-scale metagenomic assembly, we established a catalog of 131,416 metagenome-as...

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Main Authors: Bo Xu, Pengfei Song, Feng Jiang, Zhenyuan Cai, Haifeng Gu, Hongmei Gao, Bin Li, Chengbo Liang, Wen Qin, Jingjie Zhang, Jingyan Yan, Daoxin Liu, Guo Sun, Tongzuo Zhang
Format: Article
Language:English
Published: Nature Portfolio 2024-11-01
Series:npj Biofilms and Microbiomes
Online Access:https://doi.org/10.1038/s41522-024-00597-3
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author Bo Xu
Pengfei Song
Feng Jiang
Zhenyuan Cai
Haifeng Gu
Hongmei Gao
Bin Li
Chengbo Liang
Wen Qin
Jingjie Zhang
Jingyan Yan
Daoxin Liu
Guo Sun
Tongzuo Zhang
author_facet Bo Xu
Pengfei Song
Feng Jiang
Zhenyuan Cai
Haifeng Gu
Hongmei Gao
Bin Li
Chengbo Liang
Wen Qin
Jingjie Zhang
Jingyan Yan
Daoxin Liu
Guo Sun
Tongzuo Zhang
author_sort Bo Xu
collection DOAJ
description Abstract Trillions of microbes colonize the ungulate gastrointestinal tract, playing a pivotal role in enhancing host nutrient utilization by breaking down cellulose and hemicellulose present in plants. Here, through large-scale metagenomic assembly, we established a catalog of 131,416 metagenome-assembled genomes (MAGs) and 11,175 high-quality species-level genome bins (SGBs) from 17 species of ungulates in China. Our study revealed the convergent evolution of high relative abundances of carbohydrate-active enzymes (CAZymes) in the gut microbiomes of plateau-dwelling ungulates. Notably, two significant factors contribute to this phenotype: structural variations in their gut microbiome genomes, which contain more CAZymes, and the presence of novel gut microbiota species, particularly those in the genus Cryptobacteroides, which are undergoing independent rapid evolution and speciation and have higher gene densities of CAZymes. Furthermore, these enrichment CAZymes in the gut microbiomes are highly enrichment in known metabolic pathways for short-chain fatty acid (SCFA) production. Our findings not only provide a valuable genomic resource for understanding the gut microbiomes of ungulates but also offer fresh insights into the interaction between gut microbiomes and their hosts, as well as the co-adaptation of hosts and their gut microbiomes to their environments.
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spelling doaj-art-732bbbdfba7e42d8b6236f544686756e2025-08-20T02:13:31ZengNature Portfolionpj Biofilms and Microbiomes2055-50082024-11-0110111310.1038/s41522-024-00597-3Large-scale metagenomic assembly provide new insights into the genetic evolution of gut microbiomes in plateau ungulatesBo Xu0Pengfei Song1Feng Jiang2Zhenyuan Cai3Haifeng Gu4Hongmei Gao5Bin Li6Chengbo Liang7Wen Qin8Jingjie Zhang9Jingyan Yan10Daoxin Liu11Guo Sun12Tongzuo Zhang13Key Laboratory of Adaptation and Evolution of Plateau Biota, Northwest Institute of Plateau Biology, Chinese Academy of SciencesKey Laboratory of Adaptation and Evolution of Plateau Biota, Northwest Institute of Plateau Biology, Chinese Academy of SciencesKey Laboratory of Adaptation and Evolution of Plateau Biota, Northwest Institute of Plateau Biology, Chinese Academy of SciencesKey Laboratory of Adaptation and Evolution of Plateau Biota, Northwest Institute of Plateau Biology, Chinese Academy of SciencesKey Laboratory of Adaptation and Evolution of Plateau Biota, Northwest Institute of Plateau Biology, Chinese Academy of SciencesKey Laboratory of Adaptation and Evolution of Plateau Biota, Northwest Institute of Plateau Biology, Chinese Academy of SciencesKey Laboratory of Adaptation and Evolution of Plateau Biota, Northwest Institute of Plateau Biology, Chinese Academy of SciencesKey Laboratory of Adaptation and Evolution of Plateau Biota, Northwest Institute of Plateau Biology, Chinese Academy of SciencesState Key Laboratory of Plateau Ecology and Agriculture, Qinghai University 10743State Key Laboratory of Plateau Ecology and Agriculture, Qinghai University 10743College of Agriculture and Animal Husbandry, Qinghai University 10743College of Agriculture and Animal Husbandry, Qinghai University 10743College of Agriculture and Animal Husbandry, Qinghai University 10743Key Laboratory of Adaptation and Evolution of Plateau Biota, Northwest Institute of Plateau Biology, Chinese Academy of SciencesAbstract Trillions of microbes colonize the ungulate gastrointestinal tract, playing a pivotal role in enhancing host nutrient utilization by breaking down cellulose and hemicellulose present in plants. Here, through large-scale metagenomic assembly, we established a catalog of 131,416 metagenome-assembled genomes (MAGs) and 11,175 high-quality species-level genome bins (SGBs) from 17 species of ungulates in China. Our study revealed the convergent evolution of high relative abundances of carbohydrate-active enzymes (CAZymes) in the gut microbiomes of plateau-dwelling ungulates. Notably, two significant factors contribute to this phenotype: structural variations in their gut microbiome genomes, which contain more CAZymes, and the presence of novel gut microbiota species, particularly those in the genus Cryptobacteroides, which are undergoing independent rapid evolution and speciation and have higher gene densities of CAZymes. Furthermore, these enrichment CAZymes in the gut microbiomes are highly enrichment in known metabolic pathways for short-chain fatty acid (SCFA) production. Our findings not only provide a valuable genomic resource for understanding the gut microbiomes of ungulates but also offer fresh insights into the interaction between gut microbiomes and their hosts, as well as the co-adaptation of hosts and their gut microbiomes to their environments.https://doi.org/10.1038/s41522-024-00597-3
spellingShingle Bo Xu
Pengfei Song
Feng Jiang
Zhenyuan Cai
Haifeng Gu
Hongmei Gao
Bin Li
Chengbo Liang
Wen Qin
Jingjie Zhang
Jingyan Yan
Daoxin Liu
Guo Sun
Tongzuo Zhang
Large-scale metagenomic assembly provide new insights into the genetic evolution of gut microbiomes in plateau ungulates
npj Biofilms and Microbiomes
title Large-scale metagenomic assembly provide new insights into the genetic evolution of gut microbiomes in plateau ungulates
title_full Large-scale metagenomic assembly provide new insights into the genetic evolution of gut microbiomes in plateau ungulates
title_fullStr Large-scale metagenomic assembly provide new insights into the genetic evolution of gut microbiomes in plateau ungulates
title_full_unstemmed Large-scale metagenomic assembly provide new insights into the genetic evolution of gut microbiomes in plateau ungulates
title_short Large-scale metagenomic assembly provide new insights into the genetic evolution of gut microbiomes in plateau ungulates
title_sort large scale metagenomic assembly provide new insights into the genetic evolution of gut microbiomes in plateau ungulates
url https://doi.org/10.1038/s41522-024-00597-3
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