Lactobacillus reuteri improves the development and maturation of fecal microbiota in piglets through mother-to-infant microbe and metabolite vertical transmission
Abstract Background The immature neonatal fecal microbiota substantially impacts the development of gut health and greatly increases the risk of disease. Developing effective strategies to modulate the development of neonatal fecal microbiota has great significance. Herein, we investigated whether t...
| Main Authors: | , , , , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2022-12-01
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| Series: | Microbiome |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s40168-022-01336-6 |
| _version_ | 1811207952948789248 |
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| author | Gang Wang Xinyu Wang Yonghang Ma Shuang Cai Lijie Yang Yuxin Fan Xiangfang Zeng Shiyan Qiao |
| author_facet | Gang Wang Xinyu Wang Yonghang Ma Shuang Cai Lijie Yang Yuxin Fan Xiangfang Zeng Shiyan Qiao |
| author_sort | Gang Wang |
| collection | DOAJ |
| description | Abstract Background The immature neonatal fecal microbiota substantially impacts the development of gut health and greatly increases the risk of disease. Developing effective strategies to modulate the development of neonatal fecal microbiota has great significance. Herein, we investigated whether the maternal dietary supplementation and oral administration of Lactobacillus reuteri could effectively promote the development and maturation of the fecal microbiome in piglets from birth to weaning. Results Metagenomic analysis of colostrum showed that maternal dietary L. reuteri supplementation influenced the overall microbiota composition, decreased the abundance of the phylum Proteobacteria and increased that of the species Bifidobacterium choerinum. KEGG pathway analysis revealed that maternal L. reuteri supplementation enriched the lysine biosynthesis and glycolysis/gluconeogenesis pathways and downregulated the bacterial invasion of epithelial cells in the colostrum. In addition, L. reuteri supplementation significantly altered the metabolite features and modules in umbilical cord blood serum based on metabolomics. Further, a significant covariation was observed between these differential metabolites and the species in colostrum. Maternal dietary L. reuteri supplementation also significantly influenced the microbiota composition and increased the meconium abundance of beneficial bacteria (such as Romboutsia, Lactobacillus, Blautia, Butyricicoccus, and Ruminococcus), some of which were markedly associated with several differential metabolites in umbilical cord blood serum between two groups. Notably, both the maternal dietary supplementation and oral intake of L. reuteri had strong impacts on the overall microbial composition and maturation of fecal microbiota in piglets during early life, and these effects were dependent on the growth stage. Oral administration of L. reuteri promoted diarrhea resistance in neonates, while maternal supplementation of L. reuteri enhanced the abilities of antioxidants and decreased inflammation. Moreover, the administration of L. reuteri via both methods in combination improved the growth performances of piglets. Conclusion Overall, our data demonstrated that L. reuteri had the ability to modulate the composition of fecal microbiota in newborn piglets by influencing the microbial community and functional composition in the colostrum and by altering several key metabolites in the umbilical cord blood serum. Also, both the maternal dietary supplementation and oral administration of L. reuteri effectively promoted the development and maturation of the fecal microbiome in piglets during early life. Both the maternal dietary supplementation and oral administration of L. reuteri in combination optimized the growth performances of piglets. Video Abstract |
| first_indexed | 2024-04-12T04:13:46Z |
| format | Article |
| id | doaj.art-ed9ca6d0c84f421f8844a66392b641a1 |
| institution | Directory Open Access Journal |
| issn | 2049-2618 |
| language | English |
| last_indexed | 2024-04-12T04:13:46Z |
| publishDate | 2022-12-01 |
| publisher | BMC |
| record_format | Article |
| series | Microbiome |
| spelling | doaj.art-ed9ca6d0c84f421f8844a66392b641a12022-12-22T03:48:27ZengBMCMicrobiome2049-26182022-12-0110112110.1186/s40168-022-01336-6Lactobacillus reuteri improves the development and maturation of fecal microbiota in piglets through mother-to-infant microbe and metabolite vertical transmissionGang Wang0Xinyu Wang1Yonghang Ma2Shuang Cai3Lijie Yang4Yuxin Fan5Xiangfang Zeng6Shiyan Qiao7State Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural UniversityState Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural UniversityState Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural UniversityState Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural UniversityState Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural UniversityState Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural UniversityState Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural UniversityState Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural UniversityAbstract Background The immature neonatal fecal microbiota substantially impacts the development of gut health and greatly increases the risk of disease. Developing effective strategies to modulate the development of neonatal fecal microbiota has great significance. Herein, we investigated whether the maternal dietary supplementation and oral administration of Lactobacillus reuteri could effectively promote the development and maturation of the fecal microbiome in piglets from birth to weaning. Results Metagenomic analysis of colostrum showed that maternal dietary L. reuteri supplementation influenced the overall microbiota composition, decreased the abundance of the phylum Proteobacteria and increased that of the species Bifidobacterium choerinum. KEGG pathway analysis revealed that maternal L. reuteri supplementation enriched the lysine biosynthesis and glycolysis/gluconeogenesis pathways and downregulated the bacterial invasion of epithelial cells in the colostrum. In addition, L. reuteri supplementation significantly altered the metabolite features and modules in umbilical cord blood serum based on metabolomics. Further, a significant covariation was observed between these differential metabolites and the species in colostrum. Maternal dietary L. reuteri supplementation also significantly influenced the microbiota composition and increased the meconium abundance of beneficial bacteria (such as Romboutsia, Lactobacillus, Blautia, Butyricicoccus, and Ruminococcus), some of which were markedly associated with several differential metabolites in umbilical cord blood serum between two groups. Notably, both the maternal dietary supplementation and oral intake of L. reuteri had strong impacts on the overall microbial composition and maturation of fecal microbiota in piglets during early life, and these effects were dependent on the growth stage. Oral administration of L. reuteri promoted diarrhea resistance in neonates, while maternal supplementation of L. reuteri enhanced the abilities of antioxidants and decreased inflammation. Moreover, the administration of L. reuteri via both methods in combination improved the growth performances of piglets. Conclusion Overall, our data demonstrated that L. reuteri had the ability to modulate the composition of fecal microbiota in newborn piglets by influencing the microbial community and functional composition in the colostrum and by altering several key metabolites in the umbilical cord blood serum. Also, both the maternal dietary supplementation and oral administration of L. reuteri effectively promoted the development and maturation of the fecal microbiome in piglets during early life. Both the maternal dietary supplementation and oral administration of L. reuteri in combination optimized the growth performances of piglets. Video Abstracthttps://doi.org/10.1186/s40168-022-01336-6Early-life microbiotaProbioticPigletsMultiomic analysis |
| spellingShingle | Gang Wang Xinyu Wang Yonghang Ma Shuang Cai Lijie Yang Yuxin Fan Xiangfang Zeng Shiyan Qiao Lactobacillus reuteri improves the development and maturation of fecal microbiota in piglets through mother-to-infant microbe and metabolite vertical transmission Microbiome Early-life microbiota Probiotic Piglets Multiomic analysis |
| title | Lactobacillus reuteri improves the development and maturation of fecal microbiota in piglets through mother-to-infant microbe and metabolite vertical transmission |
| title_full | Lactobacillus reuteri improves the development and maturation of fecal microbiota in piglets through mother-to-infant microbe and metabolite vertical transmission |
| title_fullStr | Lactobacillus reuteri improves the development and maturation of fecal microbiota in piglets through mother-to-infant microbe and metabolite vertical transmission |
| title_full_unstemmed | Lactobacillus reuteri improves the development and maturation of fecal microbiota in piglets through mother-to-infant microbe and metabolite vertical transmission |
| title_short | Lactobacillus reuteri improves the development and maturation of fecal microbiota in piglets through mother-to-infant microbe and metabolite vertical transmission |
| title_sort | lactobacillus reuteri improves the development and maturation of fecal microbiota in piglets through mother to infant microbe and metabolite vertical transmission |
| topic | Early-life microbiota Probiotic Piglets Multiomic analysis |
| url | https://doi.org/10.1186/s40168-022-01336-6 |
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