The hindgut microbiome contributes to host oxidative stress in postpartum dairy cows by affecting glutathione synthesis process
Abstract Background Dairy cows are susceptible to postpartum systemic oxidative stress (OS), which leads to significant production loss and metabolic disorders. The gut microbiota has been linked to host health and stress levels. However, to what extent the gut microbiota is associated with postpart...
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BMC
2023-04-01
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| Series: | Microbiome |
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| Online Access: | https://doi.org/10.1186/s40168-023-01535-9 |
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| author | Fengfei Gu Senlin Zhu Jinxiu Hou Yifan Tang Jian-Xin Liu Qingbiao Xu Hui-Zeng Sun |
| author_facet | Fengfei Gu Senlin Zhu Jinxiu Hou Yifan Tang Jian-Xin Liu Qingbiao Xu Hui-Zeng Sun |
| author_sort | Fengfei Gu |
| collection | DOAJ |
| description | Abstract Background Dairy cows are susceptible to postpartum systemic oxidative stress (OS), which leads to significant production loss and metabolic disorders. The gut microbiota has been linked to host health and stress levels. However, to what extent the gut microbiota is associated with postpartum OS remains unknown. In this study, the contribution of the fecal microbiota to postpartum systemic OS and its underlying mechanisms were investigated by integrating 16S rRNA gene sequencing, metagenomics, and metabolomics in postpartum dairy cattle and by transplanting fecal microbiota from cattle to mice. Results A strong link was found between fecal microbial composition and postpartum OS, with an explainability of 43.1%. A total of 17 significantly differential bacterial genera and 19 species were identified between cows with high (HOS) and low OS (LOS). Among them, 9 genera and 16 species showed significant negative correlations with OS, and Marasmitruncus and Ruminococcus_sp._CAG:724 had the strongest correlations. The microbial functional analysis showed that the fecal microbial metabolism of glutamine, glutamate, glycine, and cysteine involved in glutathione synthesis was lower in HOS cows. Moreover, 58 significantly different metabolites were identified between HOS and LOS cows, and of these metabolites, 19 were produced from microbiota or cometabolism of microbiota and host. Furthermore, these microbial metabolites were enriched in the metabolism of glutamine, glutamate, glycine, and cysteine. The mice gavaged with HOS fecal microbiota had significantly higher OS and lower plasma glutathione peroxidase and glutathione content than those orally administered saline or LOS fecal microbiota. Conclusions Integrated results suggest that the fecal microbiota is responsible for OS and that lower glutathione production plays a causative role in HOS. These findings provide novel insights into the mechanisms of postpartum OS and potential regulatory strategies to alleviate OS in dairy cows. Video Abstract |
| first_indexed | 2024-04-09T16:22:43Z |
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| language | English |
| last_indexed | 2024-04-09T16:22:43Z |
| publishDate | 2023-04-01 |
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| series | Microbiome |
| spelling | doaj.art-50b7353778264c50a4f951939cfb3a622023-04-23T11:23:38ZengBMCMicrobiome2049-26182023-04-0111111610.1186/s40168-023-01535-9The hindgut microbiome contributes to host oxidative stress in postpartum dairy cows by affecting glutathione synthesis processFengfei Gu0Senlin Zhu1Jinxiu Hou2Yifan Tang3Jian-Xin Liu4Qingbiao Xu5Hui-Zeng Sun6Institute of Dairy Science, College of Animal Sciences, Zhejiang UniversityInstitute of Dairy Science, College of Animal Sciences, Zhejiang UniversityCollege of Animal Sciences and Technology, Huazhong Agricultural UniversityInstitute of Dairy Science, College of Animal Sciences, Zhejiang UniversityInstitute of Dairy Science, College of Animal Sciences, Zhejiang UniversityCollege of Animal Sciences and Technology, Huazhong Agricultural UniversityInstitute of Dairy Science, College of Animal Sciences, Zhejiang UniversityAbstract Background Dairy cows are susceptible to postpartum systemic oxidative stress (OS), which leads to significant production loss and metabolic disorders. The gut microbiota has been linked to host health and stress levels. However, to what extent the gut microbiota is associated with postpartum OS remains unknown. In this study, the contribution of the fecal microbiota to postpartum systemic OS and its underlying mechanisms were investigated by integrating 16S rRNA gene sequencing, metagenomics, and metabolomics in postpartum dairy cattle and by transplanting fecal microbiota from cattle to mice. Results A strong link was found between fecal microbial composition and postpartum OS, with an explainability of 43.1%. A total of 17 significantly differential bacterial genera and 19 species were identified between cows with high (HOS) and low OS (LOS). Among them, 9 genera and 16 species showed significant negative correlations with OS, and Marasmitruncus and Ruminococcus_sp._CAG:724 had the strongest correlations. The microbial functional analysis showed that the fecal microbial metabolism of glutamine, glutamate, glycine, and cysteine involved in glutathione synthesis was lower in HOS cows. Moreover, 58 significantly different metabolites were identified between HOS and LOS cows, and of these metabolites, 19 were produced from microbiota or cometabolism of microbiota and host. Furthermore, these microbial metabolites were enriched in the metabolism of glutamine, glutamate, glycine, and cysteine. The mice gavaged with HOS fecal microbiota had significantly higher OS and lower plasma glutathione peroxidase and glutathione content than those orally administered saline or LOS fecal microbiota. Conclusions Integrated results suggest that the fecal microbiota is responsible for OS and that lower glutathione production plays a causative role in HOS. These findings provide novel insights into the mechanisms of postpartum OS and potential regulatory strategies to alleviate OS in dairy cows. Video Abstracthttps://doi.org/10.1186/s40168-023-01535-9Dairy cowsFecal microbiota transplantationGlutathione synthesisMultiomicsOxidative stressTransition period |
| spellingShingle | Fengfei Gu Senlin Zhu Jinxiu Hou Yifan Tang Jian-Xin Liu Qingbiao Xu Hui-Zeng Sun The hindgut microbiome contributes to host oxidative stress in postpartum dairy cows by affecting glutathione synthesis process Microbiome Dairy cows Fecal microbiota transplantation Glutathione synthesis Multiomics Oxidative stress Transition period |
| title | The hindgut microbiome contributes to host oxidative stress in postpartum dairy cows by affecting glutathione synthesis process |
| title_full | The hindgut microbiome contributes to host oxidative stress in postpartum dairy cows by affecting glutathione synthesis process |
| title_fullStr | The hindgut microbiome contributes to host oxidative stress in postpartum dairy cows by affecting glutathione synthesis process |
| title_full_unstemmed | The hindgut microbiome contributes to host oxidative stress in postpartum dairy cows by affecting glutathione synthesis process |
| title_short | The hindgut microbiome contributes to host oxidative stress in postpartum dairy cows by affecting glutathione synthesis process |
| title_sort | hindgut microbiome contributes to host oxidative stress in postpartum dairy cows by affecting glutathione synthesis process |
| topic | Dairy cows Fecal microbiota transplantation Glutathione synthesis Multiomics Oxidative stress Transition period |
| url | https://doi.org/10.1186/s40168-023-01535-9 |
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