Dynamic changes in the gastrointestinal microbial communities of Gangba sheep and analysis of their functions in plant biomass degradation at high altitude

Abstract Background While Gangba sheep being well known for their unique flavour and nutritional value, harsh environmental factors negatively affect their growth and development, leading to poor productivity. The gastrointestinal tract microbiota plays an important role in host nutrient absorption...

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Main Authors: Xiaozhen Liu, He Ding, Xiaoxue Zhang, Na Ta, Jinmei Zhao, Qian Zhang, Huiyun Liu, Mengjiao Sun, Xiaoqing Zhang
Format: Article
Language:English
Published: BMC 2025-01-01
Series:Microbiome
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Online Access:https://doi.org/10.1186/s40168-024-02022-5
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author Xiaozhen Liu
He Ding
Xiaoxue Zhang
Na Ta
Jinmei Zhao
Qian Zhang
Huiyun Liu
Mengjiao Sun
Xiaoqing Zhang
author_facet Xiaozhen Liu
He Ding
Xiaoxue Zhang
Na Ta
Jinmei Zhao
Qian Zhang
Huiyun Liu
Mengjiao Sun
Xiaoqing Zhang
author_sort Xiaozhen Liu
collection DOAJ
description Abstract Background While Gangba sheep being well known for their unique flavour and nutritional value, harsh environmental factors negatively affect their growth and development, leading to poor productivity. The gastrointestinal tract microbiota plays an important role in host nutrient absorption and metabolism. The identification of dynamic changes in the gastrointestinal microbial communities and their functions is an important step towards improving animal production performance and health. Results A comprehensive multi-omics survey of the microbial communities of the Gangba sheep gastrointestinal tract was performed under three distinct feeding strategies: natural grazing, semi-grazing with supplementation, and barn feeding. The dynamic changes, cross-kingdom partnerships and functional potential profiles were analysed and the results revealed that the feeding strategies had a greater impact on the microbial communities than the site of the gastrointestinal tract. The different microbial associations among the groups were revealed by co-occurrence networks based on the amplicon sequence variants (ASVs). Moreover, a Gangba sheep gastrointestinal microbial genomic catalogue was constructed for the first time, including 1146 metagenome-assembled genomes (MAGs) with completeness > 50% and contamination < 10%, among which, 504 bacterial and 15 archaeal MAGs were of high quality with completeness > 80% and contamination < 10%. About 40% of the high-quality MAGs displaying enzyme activity were related to the microbial species that contribute to plant biomass degradation. Most of these enzymes were expressed in rumen metatranscriptome datasets, especially in Prevotella spp. and Ruminococcus spp., suggesting that gastrointestinal microbial communities in ruminants play major roles in the digestion of plant biomass to provide nutrition and energy for the host. Conclusions These findings suggest that feeding strategies are the primary cause of changes in the gastrointestinal microbiome. Diversification of livestock feed might be an effective strategy to maintain the diversity and ecological multifunctionality of microbial communities in the gastrointestinal tract. Additionally, the catalogue of microbial genomes and the encoded biomass-degrading enzymes identified here provide insights into the potential microbial functions of the gastrointestinal tract of Gangba sheep at high altitudes. This paves the way for microbial interventions to improve the growth performance, productivity and product quality of ruminant livestock. Video Abstract
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series Microbiome
spelling doaj-art-86198ffed22d4f1d8d1bf7f46d8e6a912025-01-26T12:43:07ZengBMCMicrobiome2049-26182025-01-0113111510.1186/s40168-024-02022-5Dynamic changes in the gastrointestinal microbial communities of Gangba sheep and analysis of their functions in plant biomass degradation at high altitudeXiaozhen Liu0He Ding1Xiaoxue Zhang2Na Ta3Jinmei Zhao4Qian Zhang5Huiyun Liu6Mengjiao Sun7Xiaoqing Zhang8Institute of Grassland Research, Chinese Academy of Agricultural SciencesInstitute of Grassland Research, Chinese Academy of Agricultural SciencesInstitute of Grassland Research, Chinese Academy of Agricultural SciencesInstitute of Grassland Research, Chinese Academy of Agricultural SciencesInstitute of Grassland Research, Chinese Academy of Agricultural SciencesInstitute of Grassland Research, Chinese Academy of Agricultural SciencesInstitute of Grassland Research, Chinese Academy of Agricultural SciencesInstitute of Grassland Research, Chinese Academy of Agricultural SciencesInstitute of Grassland Research, Chinese Academy of Agricultural SciencesAbstract Background While Gangba sheep being well known for their unique flavour and nutritional value, harsh environmental factors negatively affect their growth and development, leading to poor productivity. The gastrointestinal tract microbiota plays an important role in host nutrient absorption and metabolism. The identification of dynamic changes in the gastrointestinal microbial communities and their functions is an important step towards improving animal production performance and health. Results A comprehensive multi-omics survey of the microbial communities of the Gangba sheep gastrointestinal tract was performed under three distinct feeding strategies: natural grazing, semi-grazing with supplementation, and barn feeding. The dynamic changes, cross-kingdom partnerships and functional potential profiles were analysed and the results revealed that the feeding strategies had a greater impact on the microbial communities than the site of the gastrointestinal tract. The different microbial associations among the groups were revealed by co-occurrence networks based on the amplicon sequence variants (ASVs). Moreover, a Gangba sheep gastrointestinal microbial genomic catalogue was constructed for the first time, including 1146 metagenome-assembled genomes (MAGs) with completeness > 50% and contamination < 10%, among which, 504 bacterial and 15 archaeal MAGs were of high quality with completeness > 80% and contamination < 10%. About 40% of the high-quality MAGs displaying enzyme activity were related to the microbial species that contribute to plant biomass degradation. Most of these enzymes were expressed in rumen metatranscriptome datasets, especially in Prevotella spp. and Ruminococcus spp., suggesting that gastrointestinal microbial communities in ruminants play major roles in the digestion of plant biomass to provide nutrition and energy for the host. Conclusions These findings suggest that feeding strategies are the primary cause of changes in the gastrointestinal microbiome. Diversification of livestock feed might be an effective strategy to maintain the diversity and ecological multifunctionality of microbial communities in the gastrointestinal tract. Additionally, the catalogue of microbial genomes and the encoded biomass-degrading enzymes identified here provide insights into the potential microbial functions of the gastrointestinal tract of Gangba sheep at high altitudes. This paves the way for microbial interventions to improve the growth performance, productivity and product quality of ruminant livestock. Video Abstracthttps://doi.org/10.1186/s40168-024-02022-5High altitudeGangba sheepFeeding strategiesGastrointestinal tractBiomass-degrading enzymes
spellingShingle Xiaozhen Liu
He Ding
Xiaoxue Zhang
Na Ta
Jinmei Zhao
Qian Zhang
Huiyun Liu
Mengjiao Sun
Xiaoqing Zhang
Dynamic changes in the gastrointestinal microbial communities of Gangba sheep and analysis of their functions in plant biomass degradation at high altitude
Microbiome
High altitude
Gangba sheep
Feeding strategies
Gastrointestinal tract
Biomass-degrading enzymes
title Dynamic changes in the gastrointestinal microbial communities of Gangba sheep and analysis of their functions in plant biomass degradation at high altitude
title_full Dynamic changes in the gastrointestinal microbial communities of Gangba sheep and analysis of their functions in plant biomass degradation at high altitude
title_fullStr Dynamic changes in the gastrointestinal microbial communities of Gangba sheep and analysis of their functions in plant biomass degradation at high altitude
title_full_unstemmed Dynamic changes in the gastrointestinal microbial communities of Gangba sheep and analysis of their functions in plant biomass degradation at high altitude
title_short Dynamic changes in the gastrointestinal microbial communities of Gangba sheep and analysis of their functions in plant biomass degradation at high altitude
title_sort dynamic changes in the gastrointestinal microbial communities of gangba sheep and analysis of their functions in plant biomass degradation at high altitude
topic High altitude
Gangba sheep
Feeding strategies
Gastrointestinal tract
Biomass-degrading enzymes
url https://doi.org/10.1186/s40168-024-02022-5
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