Dietary D-xylose promotes intestinal health by inducing phage production in Escherichia coli
Abstract Elimination of specific enteropathogenic microorganisms is critical to gut health. However, the complexity of the gut community makes it challenging to target specific bacterial organisms. Accumulating evidence suggests that various foods can change the abundance of intestinal bacteria by m...
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| Format: | Article |
| Language: | English |
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Nature Portfolio
2023-10-01
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| Series: | npj Biofilms and Microbiomes |
| Online Access: | https://doi.org/10.1038/s41522-023-00445-w |
| _version_ | 1827724257258373120 |
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| author | Jie Hu Yifan Wu Luyuan Kang Yisi Liu Hao Ye Ran Wang Jinbiao Zhao Guolong Zhang Xilong Li Junjun Wang Dandan Han |
| author_facet | Jie Hu Yifan Wu Luyuan Kang Yisi Liu Hao Ye Ran Wang Jinbiao Zhao Guolong Zhang Xilong Li Junjun Wang Dandan Han |
| author_sort | Jie Hu |
| collection | DOAJ |
| description | Abstract Elimination of specific enteropathogenic microorganisms is critical to gut health. However, the complexity of the gut community makes it challenging to target specific bacterial organisms. Accumulating evidence suggests that various foods can change the abundance of intestinal bacteria by modulating prophage induction. By using pathogenic Escherichia coli (E. coli) ATCC 25922 as a model in this research, we explored the potential of dietary modulation of prophage induction and subsequent bacterial survival. Among a panel of sugars tested in vitro, D-xylose was shown to efficiently induce prophages in E. coli ATCC 25922, which depends, in part, upon the production of D-lactic acid. In an enteric mouse model, prophage induction was found to be further enhanced in response to propionic acid. Dietary D-xylose increased the proportion of Clostridia which converted D-lactic acid to propionic acid. Intestinal propionic acid levels were diminished, following either oral gavage with the dehydrogenase gene (ldhA)-deficient E. coli ATCC 25922 or depletion of intestinal Clostridia by administration of streptomycin. D-Xylose metabolism and exposure to propionic acid triggered E. coli ATCC 25922 SOS response that promoted prophage induction. E. coli ATCC 25922 mutant of RecA, a key component of SOS system, exhibited decreased phage production. These findings suggest the potential of using dietary components that can induce prophages as antimicrobial alternatives for disease control and prevention by targeted elimination of harmful gut bacteria. |
| first_indexed | 2024-03-10T22:13:14Z |
| format | Article |
| id | doaj.art-5679e7a194554c51a4c1629812bc83d4 |
| institution | Directory Open Access Journal |
| issn | 2055-5008 |
| language | English |
| last_indexed | 2024-03-10T22:13:14Z |
| publishDate | 2023-10-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | npj Biofilms and Microbiomes |
| spelling | doaj.art-5679e7a194554c51a4c1629812bc83d42023-11-19T12:32:16ZengNature Portfolionpj Biofilms and Microbiomes2055-50082023-10-019111410.1038/s41522-023-00445-wDietary D-xylose promotes intestinal health by inducing phage production in Escherichia coliJie Hu0Yifan Wu1Luyuan Kang2Yisi Liu3Hao Ye4Ran Wang5Jinbiao Zhao6Guolong Zhang7Xilong Li8Junjun Wang9Dandan Han10State Key Laboratory of Animal Nutrition and Feeding, College of Animal Science and Technology, China Agricultural UniversityState Key Laboratory of Animal Nutrition and Feeding, College of Animal Science and Technology, China Agricultural UniversityState Key Laboratory of Animal Nutrition and Feeding, College of Animal Science and Technology, China Agricultural UniversityState Key Laboratory of Animal Nutrition and Feeding, College of Animal Science and Technology, China Agricultural UniversityDepartment of Animal Sciences, Wageningen University & ResearchKey Laboratory for Control Technology and Standard for Agro-product Safety and Quality, Ministry of Agriculture and Rural Affairs, Jiangsu Key Laboratory for Food Quality and Safety-State Key Laboratory Cultivation Base of Ministry of Science and Technology, Institute of Food Safety and Nutrition, Jiangsu Academy of Agricultural SciencesState Key Laboratory of Animal Nutrition and Feeding, College of Animal Science and Technology, China Agricultural UniversityDepartment of Animal and Food Sciences, Oklahoma State UniversityKey Laboratory of Feed Biotechnology of Ministry of Agriculture and Rural Affairs, Institute of Feed Research, Chinese Academy of Agricultural SciencesState Key Laboratory of Animal Nutrition and Feeding, College of Animal Science and Technology, China Agricultural UniversityState Key Laboratory of Animal Nutrition and Feeding, College of Animal Science and Technology, China Agricultural UniversityAbstract Elimination of specific enteropathogenic microorganisms is critical to gut health. However, the complexity of the gut community makes it challenging to target specific bacterial organisms. Accumulating evidence suggests that various foods can change the abundance of intestinal bacteria by modulating prophage induction. By using pathogenic Escherichia coli (E. coli) ATCC 25922 as a model in this research, we explored the potential of dietary modulation of prophage induction and subsequent bacterial survival. Among a panel of sugars tested in vitro, D-xylose was shown to efficiently induce prophages in E. coli ATCC 25922, which depends, in part, upon the production of D-lactic acid. In an enteric mouse model, prophage induction was found to be further enhanced in response to propionic acid. Dietary D-xylose increased the proportion of Clostridia which converted D-lactic acid to propionic acid. Intestinal propionic acid levels were diminished, following either oral gavage with the dehydrogenase gene (ldhA)-deficient E. coli ATCC 25922 or depletion of intestinal Clostridia by administration of streptomycin. D-Xylose metabolism and exposure to propionic acid triggered E. coli ATCC 25922 SOS response that promoted prophage induction. E. coli ATCC 25922 mutant of RecA, a key component of SOS system, exhibited decreased phage production. These findings suggest the potential of using dietary components that can induce prophages as antimicrobial alternatives for disease control and prevention by targeted elimination of harmful gut bacteria.https://doi.org/10.1038/s41522-023-00445-w |
| spellingShingle | Jie Hu Yifan Wu Luyuan Kang Yisi Liu Hao Ye Ran Wang Jinbiao Zhao Guolong Zhang Xilong Li Junjun Wang Dandan Han Dietary D-xylose promotes intestinal health by inducing phage production in Escherichia coli npj Biofilms and Microbiomes |
| title | Dietary D-xylose promotes intestinal health by inducing phage production in Escherichia coli |
| title_full | Dietary D-xylose promotes intestinal health by inducing phage production in Escherichia coli |
| title_fullStr | Dietary D-xylose promotes intestinal health by inducing phage production in Escherichia coli |
| title_full_unstemmed | Dietary D-xylose promotes intestinal health by inducing phage production in Escherichia coli |
| title_short | Dietary D-xylose promotes intestinal health by inducing phage production in Escherichia coli |
| title_sort | dietary d xylose promotes intestinal health by inducing phage production in escherichia coli |
| url | https://doi.org/10.1038/s41522-023-00445-w |
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