Genome-wide multi-omics analysis reveals the nutrient-dependent metabolic features of mucin-degrading gut bacteria
ABSTRACTThe prevalence and occurrence of mucin-degrading (MD) bacteria, such as Akkermansia muciniphila and Ruminococcus gnavus, is highly associated with human health and disease states. However, MD bacterial physiology and metabolism remain elusive. Here, we assessed functional modules of mucin ca...
| Main Authors: | , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Taylor & Francis Group
2023-12-01
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| Series: | Gut Microbes |
| Subjects: | |
| Online Access: | https://www.tandfonline.com/doi/10.1080/19490976.2023.2221811 |
| _version_ | 1827303739538538496 |
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| author | Kyoung Su Kim Eunike Tiffany Ji-Young Lee Ara Oh Hyeon-Su Jin Ji-Sun Kim Jung-Sook Lee Myung Hee Nam Soo-Jong Hong Sowon Park Hong Koh Bong-Soo Kim Yun Kyung Lee Dong-Woo Lee |
| author_facet | Kyoung Su Kim Eunike Tiffany Ji-Young Lee Ara Oh Hyeon-Su Jin Ji-Sun Kim Jung-Sook Lee Myung Hee Nam Soo-Jong Hong Sowon Park Hong Koh Bong-Soo Kim Yun Kyung Lee Dong-Woo Lee |
| author_sort | Kyoung Su Kim |
| collection | DOAJ |
| description | ABSTRACTThe prevalence and occurrence of mucin-degrading (MD) bacteria, such as Akkermansia muciniphila and Ruminococcus gnavus, is highly associated with human health and disease states. However, MD bacterial physiology and metabolism remain elusive. Here, we assessed functional modules of mucin catabolism, through a comprehensive bioinformatics-aided functional annotation, to identify 54 A. muciniphila genes and 296 R. gnavus genes. The reconstructed core metabolic pathways coincided with the growth kinetics and fermentation profiles of A. muciniphila and R. gnavus grown in the presence of mucin and its constituents. Genome-wide multi-omics analyses validated the nutrient-dependent fermentation profiles of the MD bacteria and identified their distinct mucolytic enzymes. The distinct metabolic features of the two MD bacteria induced differences in the metabolite receptor levels and inflammatory signals of the host immune cells. In addition, in vivo experiments and community-scale metabolic modeling demonstrated that different dietary intakes influenced the abundance of MD bacteria, their metabolic fluxes, and gut barrier integrity. Thus, this study provides insights into how diet-induced metabolic differences in MD bacteria determine their distinct physiological roles in the host immune response and the gut ecosystem. |
| first_indexed | 2024-03-11T14:20:31Z |
| format | Article |
| id | doaj.art-8ac1ee5a11ef4b51ae0cd6ceb2e3845d |
| institution | Directory Open Access Journal |
| issn | 1949-0976 1949-0984 |
| language | English |
| last_indexed | 2024-04-24T17:07:26Z |
| publishDate | 2023-12-01 |
| publisher | Taylor & Francis Group |
| record_format | Article |
| series | Gut Microbes |
| spelling | doaj.art-8ac1ee5a11ef4b51ae0cd6ceb2e3845d2024-03-28T22:38:20ZengTaylor & Francis GroupGut Microbes1949-09761949-09842023-12-0115110.1080/19490976.2023.2221811Genome-wide multi-omics analysis reveals the nutrient-dependent metabolic features of mucin-degrading gut bacteriaKyoung Su Kim0Eunike Tiffany1Ji-Young Lee2Ara Oh3Hyeon-Su Jin4Ji-Sun Kim5Jung-Sook Lee6Myung Hee Nam7Soo-Jong Hong8Sowon Park9Hong Koh10Bong-Soo Kim11Yun Kyung Lee12Dong-Woo Lee13Department of Biotechnology, Yonsei University, Seoul, Republic of KoreaDepartment of Integrated Biomedical Science, Soonchunhyang Institute of Medi-Bio Science, Soonchunhyang University, Cheonan, Republic of KoreaDepartment of Biotechnology, Yonsei University, Seoul, Republic of KoreaDepartment of Integrated Biomedical Science, Soonchunhyang Institute of Medi-Bio Science, Soonchunhyang University, Cheonan, Republic of KoreaDepartment of Biotechnology, Yonsei University, Seoul, Republic of KoreaKorean Collection for Type Cultures, Korea Research Institute of Bioscience and Biotechnology (KRIBB), Jeongeup, Republic of KoreaKorean Collection for Type Cultures, Korea Research Institute of Bioscience and Biotechnology (KRIBB), Jeongeup, Republic of KoreaSeoul Center, Korea Basic Science Institute, Seoul, Republic of KoreaDepartment of Pediatrics, Childhood Asthma Atopy Center, Humidifier Disinfectant Health Center, University of Ulsan College of Medicine, Seoul, Republic of KoreaDepartment of Pediatrics, Yonsei University College of Medicine, Seoul, Republic of KoreaDepartment of Pediatrics, Yonsei University College of Medicine, Seoul, Republic of KoreaDepartment of Life Science, Hallym University, Chuncheon, Republic of KoreaDepartment of Integrated Biomedical Science, Soonchunhyang Institute of Medi-Bio Science, Soonchunhyang University, Cheonan, Republic of KoreaDepartment of Biotechnology, Yonsei University, Seoul, Republic of KoreaABSTRACTThe prevalence and occurrence of mucin-degrading (MD) bacteria, such as Akkermansia muciniphila and Ruminococcus gnavus, is highly associated with human health and disease states. However, MD bacterial physiology and metabolism remain elusive. Here, we assessed functional modules of mucin catabolism, through a comprehensive bioinformatics-aided functional annotation, to identify 54 A. muciniphila genes and 296 R. gnavus genes. The reconstructed core metabolic pathways coincided with the growth kinetics and fermentation profiles of A. muciniphila and R. gnavus grown in the presence of mucin and its constituents. Genome-wide multi-omics analyses validated the nutrient-dependent fermentation profiles of the MD bacteria and identified their distinct mucolytic enzymes. The distinct metabolic features of the two MD bacteria induced differences in the metabolite receptor levels and inflammatory signals of the host immune cells. In addition, in vivo experiments and community-scale metabolic modeling demonstrated that different dietary intakes influenced the abundance of MD bacteria, their metabolic fluxes, and gut barrier integrity. Thus, this study provides insights into how diet-induced metabolic differences in MD bacteria determine their distinct physiological roles in the host immune response and the gut ecosystem.https://www.tandfonline.com/doi/10.1080/19490976.2023.2221811Mucin-degrading bacteriagenome annotationnutrient-dependent fermentationhost immune responsethe gut ecosystem |
| spellingShingle | Kyoung Su Kim Eunike Tiffany Ji-Young Lee Ara Oh Hyeon-Su Jin Ji-Sun Kim Jung-Sook Lee Myung Hee Nam Soo-Jong Hong Sowon Park Hong Koh Bong-Soo Kim Yun Kyung Lee Dong-Woo Lee Genome-wide multi-omics analysis reveals the nutrient-dependent metabolic features of mucin-degrading gut bacteria Gut Microbes Mucin-degrading bacteria genome annotation nutrient-dependent fermentation host immune response the gut ecosystem |
| title | Genome-wide multi-omics analysis reveals the nutrient-dependent metabolic features of mucin-degrading gut bacteria |
| title_full | Genome-wide multi-omics analysis reveals the nutrient-dependent metabolic features of mucin-degrading gut bacteria |
| title_fullStr | Genome-wide multi-omics analysis reveals the nutrient-dependent metabolic features of mucin-degrading gut bacteria |
| title_full_unstemmed | Genome-wide multi-omics analysis reveals the nutrient-dependent metabolic features of mucin-degrading gut bacteria |
| title_short | Genome-wide multi-omics analysis reveals the nutrient-dependent metabolic features of mucin-degrading gut bacteria |
| title_sort | genome wide multi omics analysis reveals the nutrient dependent metabolic features of mucin degrading gut bacteria |
| topic | Mucin-degrading bacteria genome annotation nutrient-dependent fermentation host immune response the gut ecosystem |
| url | https://www.tandfonline.com/doi/10.1080/19490976.2023.2221811 |
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