Microbiome and metabolome features in inflammatory bowel disease via multi-omics integration analyses across cohorts
Abstract The perturbations of the gut microbiota and metabolites are closely associated with the progression of inflammatory bowel disease (IBD). However, inconsistent findings across studies impede a comprehensive understanding of their roles in IBD and their potential as reliable diagnostic biomar...
| Main Authors: | , , , , , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Nature Portfolio
2023-11-01
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| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-023-42788-0 |
| _version_ | 1827764260858494976 |
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| author | Lijun Ning Yi-Lu Zhou Han Sun Youwei Zhang Chaoqin Shen Zhenhua Wang Baoqin Xuan Ying Zhao Yanru Ma Yuqing Yan Tianying Tong Xiaowen Huang Muni Hu Xiaoqiang Zhu Jinmei Ding Yue Zhang Zhe Cui Jing-Yuan Fang Haoyan Chen Jie Hong |
| author_facet | Lijun Ning Yi-Lu Zhou Han Sun Youwei Zhang Chaoqin Shen Zhenhua Wang Baoqin Xuan Ying Zhao Yanru Ma Yuqing Yan Tianying Tong Xiaowen Huang Muni Hu Xiaoqiang Zhu Jinmei Ding Yue Zhang Zhe Cui Jing-Yuan Fang Haoyan Chen Jie Hong |
| author_sort | Lijun Ning |
| collection | DOAJ |
| description | Abstract The perturbations of the gut microbiota and metabolites are closely associated with the progression of inflammatory bowel disease (IBD). However, inconsistent findings across studies impede a comprehensive understanding of their roles in IBD and their potential as reliable diagnostic biomarkers. To address this challenge, here we comprehensively analyze 9 metagenomic and 4 metabolomics cohorts of IBD from different populations. Through cross-cohort integrative analysis (CCIA), we identify a consistent characteristic of commensal gut microbiota. Especially, three bacteria, namely Asaccharobacter celatus, Gemmiger formicilis, and Erysipelatoclostridium ramosum, which are rarely reported in IBD. Metagenomic functional analysis reveals that essential gene of Two-component system pathway, linked to fecal calprotectin, are implicated in IBD. Metabolomics analysis shows 36 identified metabolites with significant differences, while the roles of these metabolites in IBD are still unknown. To further elucidate the relationship between gut microbiota and metabolites, we construct multi-omics biological correlation (MOBC) maps, which highlights gut microbial biotransformation deficiencies and significant alterations in aminoacyl-tRNA synthetases. Finally, we identify multi-omics biomarkers for IBD diagnosis, validated across multiple global cohorts (AUROC values ranging from 0.92 to 0.98). Our results offer valuable insights and a significant resource for developing mechanistic hypotheses on host-microbiome interactions in IBD. |
| first_indexed | 2024-03-11T11:02:53Z |
| format | Article |
| id | doaj.art-0cefa117012443ef9d9614437bf11688 |
| institution | Directory Open Access Journal |
| issn | 2041-1723 |
| language | English |
| last_indexed | 2024-03-11T11:02:53Z |
| publishDate | 2023-11-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj.art-0cefa117012443ef9d9614437bf116882023-11-12T12:23:56ZengNature PortfolioNature Communications2041-17232023-11-0114111710.1038/s41467-023-42788-0Microbiome and metabolome features in inflammatory bowel disease via multi-omics integration analyses across cohortsLijun Ning0Yi-Lu Zhou1Han Sun2Youwei Zhang3Chaoqin Shen4Zhenhua Wang5Baoqin Xuan6Ying Zhao7Yanru Ma8Yuqing Yan9Tianying Tong10Xiaowen Huang11Muni Hu12Xiaoqiang Zhu13Jinmei Ding14Yue Zhang15Zhe Cui16Jing-Yuan Fang17Haoyan Chen18Jie Hong19State Key Laboratory of Systems Medicine for Cancer; Key Laboratory of Gastroenterology & Hepatology, Ministry of Health; Division of Gastroenterology and Hepatology; Shanghai Cancer Institute; Shanghai Institute of Digestive Disease; Renji Hospital, Shanghai Jiao Tong University School of Medicine. 145 Middle Shandong RoadState Key Laboratory of Systems Medicine for Cancer; Key Laboratory of Gastroenterology & Hepatology, Ministry of Health; Division of Gastroenterology and Hepatology; Shanghai Cancer Institute; Shanghai Institute of Digestive Disease; Renji Hospital, Shanghai Jiao Tong University School of Medicine. 145 Middle Shandong RoadDepartment of Gastroenterology, Xuzhou Central Hospital, Clinical School of Xuzhou Medical UniversityDepartment of Medical Oncology, Xuzhou Central Hospital, Clinical School of Xuzhou Medical UniversityDepartment of Gastroenterology and Hepatology, Zhongshan Hospital, Fudan UniversityState Key Laboratory of Systems Medicine for Cancer; Key Laboratory of Gastroenterology & Hepatology, Ministry of Health; Division of Gastroenterology and Hepatology; Shanghai Cancer Institute; Shanghai Institute of Digestive Disease; Renji Hospital, Shanghai Jiao Tong University School of Medicine. 145 Middle Shandong RoadState Key Laboratory of Systems Medicine for Cancer; Key Laboratory of Gastroenterology & Hepatology, Ministry of Health; Division of Gastroenterology and Hepatology; Shanghai Cancer Institute; Shanghai Institute of Digestive Disease; Renji Hospital, Shanghai Jiao Tong University School of Medicine. 145 Middle Shandong RoadState Key Laboratory of Systems Medicine for Cancer; Key Laboratory of Gastroenterology & Hepatology, Ministry of Health; Division of Gastroenterology and Hepatology; Shanghai Cancer Institute; Shanghai Institute of Digestive Disease; Renji Hospital, Shanghai Jiao Tong University School of Medicine. 145 Middle Shandong RoadState Key Laboratory of Systems Medicine for Cancer; Key Laboratory of Gastroenterology & Hepatology, Ministry of Health; Division of Gastroenterology and Hepatology; Shanghai Cancer Institute; Shanghai Institute of Digestive Disease; Renji Hospital, Shanghai Jiao Tong University School of Medicine. 145 Middle Shandong RoadState Key Laboratory of Systems Medicine for Cancer; Key Laboratory of Gastroenterology & Hepatology, Ministry of Health; Division of Gastroenterology and Hepatology; Shanghai Cancer Institute; Shanghai Institute of Digestive Disease; Renji Hospital, Shanghai Jiao Tong University School of Medicine. 145 Middle Shandong RoadState Key Laboratory of Systems Medicine for Cancer; Key Laboratory of Gastroenterology & Hepatology, Ministry of Health; Division of Gastroenterology and Hepatology; Shanghai Cancer Institute; Shanghai Institute of Digestive Disease; Renji Hospital, Shanghai Jiao Tong University School of Medicine. 145 Middle Shandong RoadState Key Laboratory of Systems Medicine for Cancer; Key Laboratory of Gastroenterology & Hepatology, Ministry of Health; Division of Gastroenterology and Hepatology; Shanghai Cancer Institute; Shanghai Institute of Digestive Disease; Renji Hospital, Shanghai Jiao Tong University School of Medicine. 145 Middle Shandong RoadState Key Laboratory of Systems Medicine for Cancer; Key Laboratory of Gastroenterology & Hepatology, Ministry of Health; Division of Gastroenterology and Hepatology; Shanghai Cancer Institute; Shanghai Institute of Digestive Disease; Renji Hospital, Shanghai Jiao Tong University School of Medicine. 145 Middle Shandong RoadState Key Laboratory of Systems Medicine for Cancer; Key Laboratory of Gastroenterology & Hepatology, Ministry of Health; Division of Gastroenterology and Hepatology; Shanghai Cancer Institute; Shanghai Institute of Digestive Disease; Renji Hospital, Shanghai Jiao Tong University School of Medicine. 145 Middle Shandong RoadState Key Laboratory of Systems Medicine for Cancer; Key Laboratory of Gastroenterology & Hepatology, Ministry of Health; Division of Gastroenterology and Hepatology; Shanghai Cancer Institute; Shanghai Institute of Digestive Disease; Renji Hospital, Shanghai Jiao Tong University School of Medicine. 145 Middle Shandong RoadState Key Laboratory of Systems Medicine for Cancer; Key Laboratory of Gastroenterology & Hepatology, Ministry of Health; Division of Gastroenterology and Hepatology; Shanghai Cancer Institute; Shanghai Institute of Digestive Disease; Renji Hospital, Shanghai Jiao Tong University School of Medicine. 145 Middle Shandong RoadDepartment of Gastrointestinal Surgery, Renji Hospital, Shanghai Jiao Tong University School of Medicine. 145 Middle Shandong RoadState Key Laboratory of Systems Medicine for Cancer; Key Laboratory of Gastroenterology & Hepatology, Ministry of Health; Division of Gastroenterology and Hepatology; Shanghai Cancer Institute; Shanghai Institute of Digestive Disease; Renji Hospital, Shanghai Jiao Tong University School of Medicine. 145 Middle Shandong RoadState Key Laboratory of Systems Medicine for Cancer; Key Laboratory of Gastroenterology & Hepatology, Ministry of Health; Division of Gastroenterology and Hepatology; Shanghai Cancer Institute; Shanghai Institute of Digestive Disease; Renji Hospital, Shanghai Jiao Tong University School of Medicine. 145 Middle Shandong RoadState Key Laboratory of Systems Medicine for Cancer; Key Laboratory of Gastroenterology & Hepatology, Ministry of Health; Division of Gastroenterology and Hepatology; Shanghai Cancer Institute; Shanghai Institute of Digestive Disease; Renji Hospital, Shanghai Jiao Tong University School of Medicine. 145 Middle Shandong RoadAbstract The perturbations of the gut microbiota and metabolites are closely associated with the progression of inflammatory bowel disease (IBD). However, inconsistent findings across studies impede a comprehensive understanding of their roles in IBD and their potential as reliable diagnostic biomarkers. To address this challenge, here we comprehensively analyze 9 metagenomic and 4 metabolomics cohorts of IBD from different populations. Through cross-cohort integrative analysis (CCIA), we identify a consistent characteristic of commensal gut microbiota. Especially, three bacteria, namely Asaccharobacter celatus, Gemmiger formicilis, and Erysipelatoclostridium ramosum, which are rarely reported in IBD. Metagenomic functional analysis reveals that essential gene of Two-component system pathway, linked to fecal calprotectin, are implicated in IBD. Metabolomics analysis shows 36 identified metabolites with significant differences, while the roles of these metabolites in IBD are still unknown. To further elucidate the relationship between gut microbiota and metabolites, we construct multi-omics biological correlation (MOBC) maps, which highlights gut microbial biotransformation deficiencies and significant alterations in aminoacyl-tRNA synthetases. Finally, we identify multi-omics biomarkers for IBD diagnosis, validated across multiple global cohorts (AUROC values ranging from 0.92 to 0.98). Our results offer valuable insights and a significant resource for developing mechanistic hypotheses on host-microbiome interactions in IBD.https://doi.org/10.1038/s41467-023-42788-0 |
| spellingShingle | Lijun Ning Yi-Lu Zhou Han Sun Youwei Zhang Chaoqin Shen Zhenhua Wang Baoqin Xuan Ying Zhao Yanru Ma Yuqing Yan Tianying Tong Xiaowen Huang Muni Hu Xiaoqiang Zhu Jinmei Ding Yue Zhang Zhe Cui Jing-Yuan Fang Haoyan Chen Jie Hong Microbiome and metabolome features in inflammatory bowel disease via multi-omics integration analyses across cohorts Nature Communications |
| title | Microbiome and metabolome features in inflammatory bowel disease via multi-omics integration analyses across cohorts |
| title_full | Microbiome and metabolome features in inflammatory bowel disease via multi-omics integration analyses across cohorts |
| title_fullStr | Microbiome and metabolome features in inflammatory bowel disease via multi-omics integration analyses across cohorts |
| title_full_unstemmed | Microbiome and metabolome features in inflammatory bowel disease via multi-omics integration analyses across cohorts |
| title_short | Microbiome and metabolome features in inflammatory bowel disease via multi-omics integration analyses across cohorts |
| title_sort | microbiome and metabolome features in inflammatory bowel disease via multi omics integration analyses across cohorts |
| url | https://doi.org/10.1038/s41467-023-42788-0 |
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