The gastrointestinal microbiome in dairy cattle is constrained by the deterministic driver of the region and the modified effect of diet
Abstract Background Dairy cattle (Bos taurus), especially Holstein cows, which are the highest-producing dairy animals and are widely bred to provide milk products to humans, rely critically on their associated gastrointestinal tract (GIT) microbiota to digest plant feed. However, the region-specifi...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2023-01-01
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| Series: | Microbiome |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s40168-022-01453-2 |
| _version_ | 1797945849455575040 |
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| author | Limei Lin Zheng Lai Jiyou Zhang Weiyun Zhu Shengyong Mao |
| author_facet | Limei Lin Zheng Lai Jiyou Zhang Weiyun Zhu Shengyong Mao |
| author_sort | Limei Lin |
| collection | DOAJ |
| description | Abstract Background Dairy cattle (Bos taurus), especially Holstein cows, which are the highest-producing dairy animals and are widely bred to provide milk products to humans, rely critically on their associated gastrointestinal tract (GIT) microbiota to digest plant feed. However, the region-specific taxonomic composition and function of the GIT microbiome in dairy cattle and the mechanistic basis for the diet-induced effects remain to be elucidated. Results We collected 120 digesta samples from 10 GIT regions of 12 Holstein cows fed forage- and grain-based diets and characterized their GIT microbiome via functional shotgun metagenomics and the resolution of metagenome-assembled genomes. Our results demonstrated that the GIT microbiome was mainly partitioned into three distinct clusters, four-chambered stomach, small intestine, and large intestine. Moreover, we found that the four-chambered stomach microbiome with the highest diversity had a strong ability to degrade recalcitrant polysaccharide substrates, underpinned by the prevalence of potential cellulosome-producing and plant-derived polysaccharide utilization loci-encoding consortia. In contrast, the post-gastric intestinal microbiome orchestrated alternative fermentation pathways to adapt to nutrient availability and energy acquisition. Diet shifts selectively modified the metabolic cascades of the microbiome in specific GIT regions, evidenced by the loss of fiber-degrading taxa and increased hydrogen sinks in propionate after grain introduction. Conclusions Our findings provide new insights into GIT microbial organization and function in dairy cattle by GIT regions and diet regimes, which offers clues for improving animal production and health in the future. Video Abstract |
| first_indexed | 2024-04-10T21:01:38Z |
| format | Article |
| id | doaj.art-fd27103ed8b64ef492ec95dcaf297f19 |
| institution | Directory Open Access Journal |
| issn | 2049-2618 |
| language | English |
| last_indexed | 2024-04-10T21:01:38Z |
| publishDate | 2023-01-01 |
| publisher | BMC |
| record_format | Article |
| series | Microbiome |
| spelling | doaj.art-fd27103ed8b64ef492ec95dcaf297f192023-01-22T12:19:47ZengBMCMicrobiome2049-26182023-01-0111112110.1186/s40168-022-01453-2The gastrointestinal microbiome in dairy cattle is constrained by the deterministic driver of the region and the modified effect of dietLimei Lin0Zheng Lai1Jiyou Zhang2Weiyun Zhu3Shengyong Mao4Laboratory of Gastrointestinal Microbiology, Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, National Center for International Research On Animal Gut Nutrition, College of Animal Science and Technology, Nanjing Agricultural UniversityLaboratory of Gastrointestinal Microbiology, Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, National Center for International Research On Animal Gut Nutrition, College of Animal Science and Technology, Nanjing Agricultural UniversityLaboratory of Gastrointestinal Microbiology, Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, National Center for International Research On Animal Gut Nutrition, College of Animal Science and Technology, Nanjing Agricultural UniversityLaboratory of Gastrointestinal Microbiology, Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, National Center for International Research On Animal Gut Nutrition, College of Animal Science and Technology, Nanjing Agricultural UniversityLaboratory of Gastrointestinal Microbiology, Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, National Center for International Research On Animal Gut Nutrition, College of Animal Science and Technology, Nanjing Agricultural UniversityAbstract Background Dairy cattle (Bos taurus), especially Holstein cows, which are the highest-producing dairy animals and are widely bred to provide milk products to humans, rely critically on their associated gastrointestinal tract (GIT) microbiota to digest plant feed. However, the region-specific taxonomic composition and function of the GIT microbiome in dairy cattle and the mechanistic basis for the diet-induced effects remain to be elucidated. Results We collected 120 digesta samples from 10 GIT regions of 12 Holstein cows fed forage- and grain-based diets and characterized their GIT microbiome via functional shotgun metagenomics and the resolution of metagenome-assembled genomes. Our results demonstrated that the GIT microbiome was mainly partitioned into three distinct clusters, four-chambered stomach, small intestine, and large intestine. Moreover, we found that the four-chambered stomach microbiome with the highest diversity had a strong ability to degrade recalcitrant polysaccharide substrates, underpinned by the prevalence of potential cellulosome-producing and plant-derived polysaccharide utilization loci-encoding consortia. In contrast, the post-gastric intestinal microbiome orchestrated alternative fermentation pathways to adapt to nutrient availability and energy acquisition. Diet shifts selectively modified the metabolic cascades of the microbiome in specific GIT regions, evidenced by the loss of fiber-degrading taxa and increased hydrogen sinks in propionate after grain introduction. Conclusions Our findings provide new insights into GIT microbial organization and function in dairy cattle by GIT regions and diet regimes, which offers clues for improving animal production and health in the future. Video Abstracthttps://doi.org/10.1186/s40168-022-01453-2Dairy cattleGastrointestinal microbiomeSegmental heterogeneityDietary regimesCarbon handoffsInterspecies hydrogen transfer |
| spellingShingle | Limei Lin Zheng Lai Jiyou Zhang Weiyun Zhu Shengyong Mao The gastrointestinal microbiome in dairy cattle is constrained by the deterministic driver of the region and the modified effect of diet Microbiome Dairy cattle Gastrointestinal microbiome Segmental heterogeneity Dietary regimes Carbon handoffs Interspecies hydrogen transfer |
| title | The gastrointestinal microbiome in dairy cattle is constrained by the deterministic driver of the region and the modified effect of diet |
| title_full | The gastrointestinal microbiome in dairy cattle is constrained by the deterministic driver of the region and the modified effect of diet |
| title_fullStr | The gastrointestinal microbiome in dairy cattle is constrained by the deterministic driver of the region and the modified effect of diet |
| title_full_unstemmed | The gastrointestinal microbiome in dairy cattle is constrained by the deterministic driver of the region and the modified effect of diet |
| title_short | The gastrointestinal microbiome in dairy cattle is constrained by the deterministic driver of the region and the modified effect of diet |
| title_sort | gastrointestinal microbiome in dairy cattle is constrained by the deterministic driver of the region and the modified effect of diet |
| topic | Dairy cattle Gastrointestinal microbiome Segmental heterogeneity Dietary regimes Carbon handoffs Interspecies hydrogen transfer |
| url | https://doi.org/10.1186/s40168-022-01453-2 |
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