In vivo systematic analysis of microbiota-prebiotic crosstalk reveals a synbiotic that effectively ameliorates DSS-induced colitis in mice
Systematic identification of prebiotic–microbe interactions is essential for developing precision microbiome-targeted interventions to improve human health. In this study, we developed an in vivo systematic screening platform to evaluate microbiota-prebiotic crosstalk and applied it to identify a sy...
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| Format: | Article |
| Language: | English |
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Taylor & Francis Group
2025-12-01
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| Series: | Gut Microbes |
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| Online Access: | https://www.tandfonline.com/doi/10.1080/19490976.2025.2541028 |
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| author | Qianwen Peng Puzi Jiang Liwen Yi Yun Li Qianqian Yang Xuchun Wan Junqing He Zihao Mo Haorui Niu Qing Lan Haidong Jia Dezheng Xu Chenhui Wang Hongju Yang Zhi Liu Wei-Hua Chen |
| author_facet | Qianwen Peng Puzi Jiang Liwen Yi Yun Li Qianqian Yang Xuchun Wan Junqing He Zihao Mo Haorui Niu Qing Lan Haidong Jia Dezheng Xu Chenhui Wang Hongju Yang Zhi Liu Wei-Hua Chen |
| author_sort | Qianwen Peng |
| collection | DOAJ |
| description | Systematic identification of prebiotic–microbe interactions is essential for developing precision microbiome-targeted interventions to improve human health. In this study, we developed an in vivo systematic screening platform to evaluate microbiota-prebiotic crosstalk and applied it to identify a synbiotic combination effective against dextran sulfate sodium (DSS)-induced colitis in mice. Specifically, we first established a humanized gut microbiota mouse model by colonizing mice with 73 microbial strains, which showed highly abundant and prevalent in the human gut. Concurrently, we administered the mice with 28 different prebiotic or prebiotic candidates, including polyphenols, polysaccharides, vitamins, and minerals common in the market. Following the DSS-induced colitis, we evaluated the protective effects of each microbiota–prebiotic pairing. Fourteen prebiotic or prebiotic candidates, designated as the ESS group, significantly alleviated colitis, partly by enriching specific beneficial microbes such as Bacteroides thetaiotaomicron, Akkermansia muciniphila, and Erysipelatoclostridium ramosum prior to disease onset. Further experiments revealed two symbiotic combinations with the strongest anti-inflammatory effects: calcium-magnesium tablets (CMT) combined with either B. thetaiotaomicron or A. muciniphila. Mechanistically, CMT promoted the growth of B. thetaiotaomicron and alleviated inflammation by upregulating genes associated with probiotic activity. Finally, in an intervention trial involving healthy human volunteers, CMT selectively increased B. thetaiotaomicron abundance without altering the overall gut microbiota composition. Together, our study presents a systematic framework for elucidating microbe−prebiotic interactions, identifying synbiotic combinations with therapeutic potential, and advancing precision microbiome-based strategies for disease prevention and treatment. |
| format | Article |
| id | doaj-art-fe50a911365a459ca67f7aecc95d8711 |
| institution | Kabale University |
| issn | 1949-0976 1949-0984 |
| language | English |
| publishDate | 2025-12-01 |
| publisher | Taylor & Francis Group |
| record_format | Article |
| series | Gut Microbes |
| spelling | doaj-art-fe50a911365a459ca67f7aecc95d87112025-08-20T03:44:04ZengTaylor & Francis GroupGut Microbes1949-09761949-09842025-12-0117110.1080/19490976.2025.2541028In vivo systematic analysis of microbiota-prebiotic crosstalk reveals a synbiotic that effectively ameliorates DSS-induced colitis in miceQianwen Peng0Puzi Jiang1Liwen Yi2Yun Li3Qianqian Yang4Xuchun Wan5Junqing He6Zihao Mo7Haorui Niu8Qing Lan9Haidong Jia10Dezheng Xu11Chenhui Wang12Hongju Yang13Zhi Liu14Wei-Hua Chen15Key Laboratory of Molecular Biophysics of the Ministry of Education, Hubei Key Laboratory of Bioinformatics and Molecular Imaging, Department of Biotechnology, College of Life Science and Technology, Huazhong University of Science and Technology, Wuhan, Hubei, ChinaDepartment of Bioinformatics and Systems Biology, College of Life Science and Technology, Huazhong University of Science and Technology, Wuhan, Hubei, ChinaKey Laboratory of Molecular Biophysics of the Ministry of Education, Hubei Key Laboratory of Bioinformatics and Molecular Imaging, Department of Biotechnology, College of Life Science and Technology, Huazhong University of Science and Technology, Wuhan, Hubei, ChinaDepartment of Bioinformatics and Systems Biology, College of Life Science and Technology, Huazhong University of Science and Technology, Wuhan, Hubei, ChinaKey Laboratory of Molecular Biophysics of the Ministry of Education, Hubei Key Laboratory of Bioinformatics and Molecular Imaging, Department of Biotechnology, College of Life Science and Technology, Huazhong University of Science and Technology, Wuhan, Hubei, ChinaKey Laboratory of Molecular Biophysics of the Ministry of Education, Hubei Key Laboratory of Bioinformatics and Molecular Imaging, Department of Biotechnology, College of Life Science and Technology, Huazhong University of Science and Technology, Wuhan, Hubei, ChinaKey Laboratory of Molecular Biophysics of the Ministry of Education, Hubei Key Laboratory of Bioinformatics and Molecular Imaging, Department of Biotechnology, College of Life Science and Technology, Huazhong University of Science and Technology, Wuhan, Hubei, ChinaKey Laboratory of Molecular Biophysics of the Ministry of Education, Hubei Key Laboratory of Bioinformatics and Molecular Imaging, Department of Biotechnology, College of Life Science and Technology, Huazhong University of Science and Technology, Wuhan, Hubei, ChinaKey Laboratory of Molecular Biophysics of the Ministry of Education, Hubei Key Laboratory of Bioinformatics and Molecular Imaging, Department of Biotechnology, College of Life Science and Technology, Huazhong University of Science and Technology, Wuhan, Hubei, ChinaDivision of Geriatric Gastroenterology, The First Affiliated Hospital of Kunming Medical University, Kunming, Yunnan, ChinaShanghai Jahwa United Co., Ltd., Shanghai, ChinaShanghai Jahwa United Co., Ltd., Shanghai, ChinaThe Key Laboratory for Human Disease Gene Study of Sichuan Province and the Department of Laboratory Medicine, Sichuan Provincial People’s Hospital, University of Electronic Science and Technology of China, Chengdu, ChinaDivision of Geriatric Gastroenterology, The First Affiliated Hospital of Kunming Medical University, Kunming, Yunnan, ChinaKey Laboratory of Molecular Biophysics of the Ministry of Education, Hubei Key Laboratory of Bioinformatics and Molecular Imaging, Department of Biotechnology, College of Life Science and Technology, Huazhong University of Science and Technology, Wuhan, Hubei, ChinaDepartment of Bioinformatics and Systems Biology, College of Life Science and Technology, Huazhong University of Science and Technology, Wuhan, Hubei, ChinaSystematic identification of prebiotic–microbe interactions is essential for developing precision microbiome-targeted interventions to improve human health. In this study, we developed an in vivo systematic screening platform to evaluate microbiota-prebiotic crosstalk and applied it to identify a synbiotic combination effective against dextran sulfate sodium (DSS)-induced colitis in mice. Specifically, we first established a humanized gut microbiota mouse model by colonizing mice with 73 microbial strains, which showed highly abundant and prevalent in the human gut. Concurrently, we administered the mice with 28 different prebiotic or prebiotic candidates, including polyphenols, polysaccharides, vitamins, and minerals common in the market. Following the DSS-induced colitis, we evaluated the protective effects of each microbiota–prebiotic pairing. Fourteen prebiotic or prebiotic candidates, designated as the ESS group, significantly alleviated colitis, partly by enriching specific beneficial microbes such as Bacteroides thetaiotaomicron, Akkermansia muciniphila, and Erysipelatoclostridium ramosum prior to disease onset. Further experiments revealed two symbiotic combinations with the strongest anti-inflammatory effects: calcium-magnesium tablets (CMT) combined with either B. thetaiotaomicron or A. muciniphila. Mechanistically, CMT promoted the growth of B. thetaiotaomicron and alleviated inflammation by upregulating genes associated with probiotic activity. Finally, in an intervention trial involving healthy human volunteers, CMT selectively increased B. thetaiotaomicron abundance without altering the overall gut microbiota composition. Together, our study presents a systematic framework for elucidating microbe−prebiotic interactions, identifying synbiotic combinations with therapeutic potential, and advancing precision microbiome-based strategies for disease prevention and treatment.https://www.tandfonline.com/doi/10.1080/19490976.2025.2541028Prebiotics and prebiotic candidatesmicrobiotaprebiotic−microbe interactionDSS-induced colitisCalcium-magnesium tablets (CMT)bacteroides thetaiotaomicron |
| spellingShingle | Qianwen Peng Puzi Jiang Liwen Yi Yun Li Qianqian Yang Xuchun Wan Junqing He Zihao Mo Haorui Niu Qing Lan Haidong Jia Dezheng Xu Chenhui Wang Hongju Yang Zhi Liu Wei-Hua Chen In vivo systematic analysis of microbiota-prebiotic crosstalk reveals a synbiotic that effectively ameliorates DSS-induced colitis in mice Gut Microbes Prebiotics and prebiotic candidates microbiota prebiotic−microbe interaction DSS-induced colitis Calcium-magnesium tablets (CMT) bacteroides thetaiotaomicron |
| title | In vivo systematic analysis of microbiota-prebiotic crosstalk reveals a synbiotic that effectively ameliorates DSS-induced colitis in mice |
| title_full | In vivo systematic analysis of microbiota-prebiotic crosstalk reveals a synbiotic that effectively ameliorates DSS-induced colitis in mice |
| title_fullStr | In vivo systematic analysis of microbiota-prebiotic crosstalk reveals a synbiotic that effectively ameliorates DSS-induced colitis in mice |
| title_full_unstemmed | In vivo systematic analysis of microbiota-prebiotic crosstalk reveals a synbiotic that effectively ameliorates DSS-induced colitis in mice |
| title_short | In vivo systematic analysis of microbiota-prebiotic crosstalk reveals a synbiotic that effectively ameliorates DSS-induced colitis in mice |
| title_sort | in vivo systematic analysis of microbiota prebiotic crosstalk reveals a synbiotic that effectively ameliorates dss induced colitis in mice |
| topic | Prebiotics and prebiotic candidates microbiota prebiotic−microbe interaction DSS-induced colitis Calcium-magnesium tablets (CMT) bacteroides thetaiotaomicron |
| url | https://www.tandfonline.com/doi/10.1080/19490976.2025.2541028 |
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