Deciphering the microbiome–metabolome landscape of an inflammatory bowel disease inception cohort

The gut microbiota contribute to the etiopathogenesis of inflammatory bowel disease (IBD), but limitations of prior studies include the use of sequencing alone (restricting exploration of the contribution of microbiota functionality) and the recruitment of patients with well-established disease (int...

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Main Authors: Shiva T. Radhakrishnan, Benjamin H. Mullish, Marton L. Olbei, Nathan P. Danckert, Maria A. Valdivia-Garcia, Jose I. Serrano-Contreras, Despoina Chrysostomou, Sharmili Balarajah, Robert W. Perry, John P. Thomas, Lejla Potari-Gul, Dezso Modos, Lucy C. Hicks, Nick Powell, Timothy R. Orchard, Jia V. Li, Julian R. Marchesi, Tamas Korcsmaros, James L. Alexander, Horace R. T. Williams
Format: Article
Language:English
Published: Taylor & Francis Group 2025-12-01
Series:Gut Microbes
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Online Access:https://www.tandfonline.com/doi/10.1080/19490976.2025.2527863
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author Shiva T. Radhakrishnan
Benjamin H. Mullish
Marton L. Olbei
Nathan P. Danckert
Maria A. Valdivia-Garcia
Jose I. Serrano-Contreras
Despoina Chrysostomou
Sharmili Balarajah
Robert W. Perry
John P. Thomas
Lejla Potari-Gul
Dezso Modos
Lucy C. Hicks
Nick Powell
Timothy R. Orchard
Jia V. Li
Julian R. Marchesi
Tamas Korcsmaros
James L. Alexander
Horace R. T. Williams
author_facet Shiva T. Radhakrishnan
Benjamin H. Mullish
Marton L. Olbei
Nathan P. Danckert
Maria A. Valdivia-Garcia
Jose I. Serrano-Contreras
Despoina Chrysostomou
Sharmili Balarajah
Robert W. Perry
John P. Thomas
Lejla Potari-Gul
Dezso Modos
Lucy C. Hicks
Nick Powell
Timothy R. Orchard
Jia V. Li
Julian R. Marchesi
Tamas Korcsmaros
James L. Alexander
Horace R. T. Williams
author_sort Shiva T. Radhakrishnan
collection DOAJ
description The gut microbiota contribute to the etiopathogenesis of inflammatory bowel disease (IBD), but limitations of prior studies include the use of sequencing alone (restricting exploration of the contribution of microbiota functionality) and the recruitment of patients with well-established disease (introducing potential confounders, such as immunomodulatory medication). Here, we analyze a true IBD inception cohort and healthy controls (HCs) via stool 16S rRNA gene sequencing and multi-system metabolomic phenotyping (using nuclear magnetic spectroscopy and mass spectroscopy), with subsequent integrative network analysis employed to delineate novel microbiota–metabolome interactions in IBD. Marked differences in β diversity and taxonomic profiles were observed both between IBD and HCs, as well as between Crohn’s disease (CD) and ulcerative colitis (UC) patients. Multiple between-group metabolomic differences were also observed, particularly with regard to tryptophan-/indole-related metabolites; for example, UC patients had higher levels of serum metabolites including xanthurenic acid (q = 0.0092) and picolinic acid (q = 0.018). Network analysis demonstrated multiple unique interactions in CD compared to HCs with minimal overlap, indicating a loss of ‘health-associated’ interactions in CD. Compared to HCs, UC patients demonstrated increased pathway activity related to nitrogen and butanoate metabolism, whilst CD patients displayed increased leucine and valine synthesis. Networks from IBD patients overall showed negative correlation with health-specific associations, including an increase in taurine metabolism. Collectively, this work characterizes multiple novel perturbed microbiota–metabolome interactions that are present even at the diagnosis of IBD, which may inform potential future targets to aid diagnosis and direct therapeutic options.
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spelling doaj-art-285e9110d0de4fbd9b52be4b2fa7a6042025-08-20T03:12:51ZengTaylor & Francis GroupGut Microbes1949-09761949-09842025-12-0117110.1080/19490976.2025.2527863Deciphering the microbiome–metabolome landscape of an inflammatory bowel disease inception cohortShiva T. Radhakrishnan0Benjamin H. Mullish1Marton L. Olbei2Nathan P. Danckert3Maria A. Valdivia-Garcia4Jose I. Serrano-Contreras5Despoina Chrysostomou6Sharmili Balarajah7Robert W. Perry8John P. Thomas9Lejla Potari-Gul10Dezso Modos11Lucy C. Hicks12Nick Powell13Timothy R. Orchard14Jia V. Li15Julian R. Marchesi16Tamas Korcsmaros17James L. Alexander18Horace R. T. Williams19Division of Digestive Diseases, Department of Metabolism, Digestion and Reproduction, Faculty of Medicine, Imperial College London, London, UKDivision of Digestive Diseases, Department of Metabolism, Digestion and Reproduction, Faculty of Medicine, Imperial College London, London, UKDivision of Digestive Diseases, Department of Metabolism, Digestion and Reproduction, Faculty of Medicine, Imperial College London, London, UKDivision of Digestive Diseases, Department of Metabolism, Digestion and Reproduction, Faculty of Medicine, Imperial College London, London, UKDivision of Digestive Diseases, Department of Metabolism, Digestion and Reproduction, Faculty of Medicine, Imperial College London, London, UKDivision of Digestive Diseases, Department of Metabolism, Digestion and Reproduction, Faculty of Medicine, Imperial College London, London, UKDivision of Digestive Diseases, Department of Metabolism, Digestion and Reproduction, Faculty of Medicine, Imperial College London, London, UKDivision of Digestive Diseases, Department of Metabolism, Digestion and Reproduction, Faculty of Medicine, Imperial College London, London, UKDivision of Digestive Diseases, Department of Metabolism, Digestion and Reproduction, Faculty of Medicine, Imperial College London, London, UKDivision of Digestive Diseases, Department of Metabolism, Digestion and Reproduction, Faculty of Medicine, Imperial College London, London, UKDivision of Digestive Diseases, Department of Metabolism, Digestion and Reproduction, Faculty of Medicine, Imperial College London, London, UKDivision of Systems Medicine, Department of Metabolism, Digestion and Reproduction, Faculty of Medicine, Imperial College London, London, UKDivision of Digestive Diseases, Department of Metabolism, Digestion and Reproduction, Faculty of Medicine, Imperial College London, London, UKDivision of Digestive Diseases, Department of Metabolism, Digestion and Reproduction, Faculty of Medicine, Imperial College London, London, UKDivision of Digestive Diseases, Department of Metabolism, Digestion and Reproduction, Faculty of Medicine, Imperial College London, London, UKDivision of Digestive Diseases, Department of Metabolism, Digestion and Reproduction, Faculty of Medicine, Imperial College London, London, UKDivision of Digestive Diseases, Department of Metabolism, Digestion and Reproduction, Faculty of Medicine, Imperial College London, London, UKDivision of Digestive Diseases, Department of Metabolism, Digestion and Reproduction, Faculty of Medicine, Imperial College London, London, UKDivision of Digestive Diseases, Department of Metabolism, Digestion and Reproduction, Faculty of Medicine, Imperial College London, London, UKDivision of Digestive Diseases, Department of Metabolism, Digestion and Reproduction, Faculty of Medicine, Imperial College London, London, UKThe gut microbiota contribute to the etiopathogenesis of inflammatory bowel disease (IBD), but limitations of prior studies include the use of sequencing alone (restricting exploration of the contribution of microbiota functionality) and the recruitment of patients with well-established disease (introducing potential confounders, such as immunomodulatory medication). Here, we analyze a true IBD inception cohort and healthy controls (HCs) via stool 16S rRNA gene sequencing and multi-system metabolomic phenotyping (using nuclear magnetic spectroscopy and mass spectroscopy), with subsequent integrative network analysis employed to delineate novel microbiota–metabolome interactions in IBD. Marked differences in β diversity and taxonomic profiles were observed both between IBD and HCs, as well as between Crohn’s disease (CD) and ulcerative colitis (UC) patients. Multiple between-group metabolomic differences were also observed, particularly with regard to tryptophan-/indole-related metabolites; for example, UC patients had higher levels of serum metabolites including xanthurenic acid (q = 0.0092) and picolinic acid (q = 0.018). Network analysis demonstrated multiple unique interactions in CD compared to HCs with minimal overlap, indicating a loss of ‘health-associated’ interactions in CD. Compared to HCs, UC patients demonstrated increased pathway activity related to nitrogen and butanoate metabolism, whilst CD patients displayed increased leucine and valine synthesis. Networks from IBD patients overall showed negative correlation with health-specific associations, including an increase in taurine metabolism. Collectively, this work characterizes multiple novel perturbed microbiota–metabolome interactions that are present even at the diagnosis of IBD, which may inform potential future targets to aid diagnosis and direct therapeutic options.https://www.tandfonline.com/doi/10.1080/19490976.2025.2527863MicrobiomeMetabolomeIBDNetwork analysesInception cohortCrohn‘s Disease
spellingShingle Shiva T. Radhakrishnan
Benjamin H. Mullish
Marton L. Olbei
Nathan P. Danckert
Maria A. Valdivia-Garcia
Jose I. Serrano-Contreras
Despoina Chrysostomou
Sharmili Balarajah
Robert W. Perry
John P. Thomas
Lejla Potari-Gul
Dezso Modos
Lucy C. Hicks
Nick Powell
Timothy R. Orchard
Jia V. Li
Julian R. Marchesi
Tamas Korcsmaros
James L. Alexander
Horace R. T. Williams
Deciphering the microbiome–metabolome landscape of an inflammatory bowel disease inception cohort
Gut Microbes
Microbiome
Metabolome
IBD
Network analyses
Inception cohort
Crohn‘s Disease
title Deciphering the microbiome–metabolome landscape of an inflammatory bowel disease inception cohort
title_full Deciphering the microbiome–metabolome landscape of an inflammatory bowel disease inception cohort
title_fullStr Deciphering the microbiome–metabolome landscape of an inflammatory bowel disease inception cohort
title_full_unstemmed Deciphering the microbiome–metabolome landscape of an inflammatory bowel disease inception cohort
title_short Deciphering the microbiome–metabolome landscape of an inflammatory bowel disease inception cohort
title_sort deciphering the microbiome metabolome landscape of an inflammatory bowel disease inception cohort
topic Microbiome
Metabolome
IBD
Network analyses
Inception cohort
Crohn‘s Disease
url https://www.tandfonline.com/doi/10.1080/19490976.2025.2527863
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