Integrated fecal microbiome–metabolome signatures reflect stress and serotonin metabolism in irritable bowel syndrome
To gain insight into the complex microbiome-gut-brain axis in irritable bowel syndrome (IBS), several modalities of biological and clinical data must be combined. We aimed to identify profiles of fecal microbiota and metabolites associated with IBS and to delineate specific phenotypes of IBS that re...
Saved in:
| Main Authors: | , , , , , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Taylor & Francis Group
2022-12-01
|
| Series: | Gut Microbes |
| Subjects: | |
| Online Access: | https://www.tandfonline.com/doi/10.1080/19490976.2022.2063016 |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| _version_ | 1849716930922938368 |
|---|---|
| author | Zlatan Mujagic Melpomeni Kasapi Daisy MAE Jonkers Isabel Garcia-Perez Lisa Vork Zsa Zsa R.M. Weerts Jose Ivan Serrano-Contreras Alexandra Zhernakova Alexander Kurilshikov Jamie Scotcher Elaine Holmes Cisca Wijmenga Daniel Keszthelyi Jeremy K Nicholson Joram M Posma Ad AM Masclee |
| author_facet | Zlatan Mujagic Melpomeni Kasapi Daisy MAE Jonkers Isabel Garcia-Perez Lisa Vork Zsa Zsa R.M. Weerts Jose Ivan Serrano-Contreras Alexandra Zhernakova Alexander Kurilshikov Jamie Scotcher Elaine Holmes Cisca Wijmenga Daniel Keszthelyi Jeremy K Nicholson Joram M Posma Ad AM Masclee |
| author_sort | Zlatan Mujagic |
| collection | DOAJ |
| description | To gain insight into the complex microbiome-gut-brain axis in irritable bowel syndrome (IBS), several modalities of biological and clinical data must be combined. We aimed to identify profiles of fecal microbiota and metabolites associated with IBS and to delineate specific phenotypes of IBS that represent potential pathophysiological mechanisms. Fecal metabolites were measured using proton nuclear magnetic resonance (1H-NMR) spectroscopy and gut microbiome using shotgun metagenomic sequencing (MGS) in a combined dataset of 142 IBS patients and 120 healthy controls (HCs) with extensive clinical, biological and phenotype information. Data were analyzed using support vector classification and regression and kernel t-SNE. Microbiome and metabolome profiles could distinguish IBS and HC with an area-under-the-receiver-operator-curve of 77.3% and 79.5%, respectively, but this could be improved by combining microbiota and metabolites to 83.6%. No significant differences in predictive ability of the microbiome–metabolome data were observed between the three classical, stool pattern-based, IBS subtypes. However, unsupervised clustering showed distinct subsets of IBS patients based on fecal microbiome–metabolome data. These clusters could be related plasma levels of serotonin and its metabolite 5-hydroxyindoleacetate, effects of psychological stress on gastrointestinal (GI) symptoms, onset of IBS after stressful events, medical history of previous abdominal surgery, dietary caloric intake and IBS symptom duration. Furthermore, pathways in metabolic reaction networks were integrated with microbiota data, that reflect the host-microbiome interactions in IBS. The identified microbiome–metabolome signatures for IBS, associated with altered serotonin metabolism and unfavorable stress response related to GI symptoms, support the microbiota-gut-brain link in the pathogenesis of IBS. |
| format | Article |
| id | doaj-art-e79d1f03f017403cb6d067e98bd9b458 |
| institution | DOAJ |
| issn | 1949-0976 1949-0984 |
| language | English |
| publishDate | 2022-12-01 |
| publisher | Taylor & Francis Group |
| record_format | Article |
| series | Gut Microbes |
| spelling | doaj-art-e79d1f03f017403cb6d067e98bd9b4582025-08-20T03:12:50ZengTaylor & Francis GroupGut Microbes1949-09761949-09842022-12-0114110.1080/19490976.2022.2063016Integrated fecal microbiome–metabolome signatures reflect stress and serotonin metabolism in irritable bowel syndromeZlatan Mujagic0Melpomeni Kasapi1Daisy MAE Jonkers2Isabel Garcia-Perez3Lisa Vork4Zsa Zsa R.M. Weerts5Jose Ivan Serrano-Contreras6Alexandra Zhernakova7Alexander Kurilshikov8Jamie Scotcher9Elaine Holmes10Cisca Wijmenga11Daniel Keszthelyi12Jeremy K Nicholson13Joram M Posma14Ad AM Masclee15Division Gastroenterology-Hepatology, Maastricht University Medical Center+, Maastricht, The NetherlandsDivision of Systems Medicine, Department of Metabolism, Digestion and Reproduction, Faculty of Medicine, South Kensington Campus, Imperial College London, London, UKDivision Gastroenterology-Hepatology, Maastricht University Medical Center+, Maastricht, The NetherlandsDivision of Digestive Diseases, Department of Metabolism, Digestion and Reproduction, Faculty of Medicine, Hammersmith Campus, Imperial College London, London, UKDivision Gastroenterology-Hepatology, Maastricht University Medical Center+, Maastricht, The NetherlandsDivision Gastroenterology-Hepatology, Maastricht University Medical Center+, Maastricht, The NetherlandsDivision of Systems Medicine, Department of Metabolism, Digestion and Reproduction, Faculty of Medicine, South Kensington Campus, Imperial College London, London, UKDepartment of Genetics, University of Groningen, University Medical Center Groningen, Groningen, The NetherlandsDepartment of Genetics, University of Groningen, University Medical Center Groningen, Groningen, The NetherlandsDivision of Systems Medicine, Department of Metabolism, Digestion and Reproduction, Faculty of Medicine, South Kensington Campus, Imperial College London, London, UKDivision of Digestive Diseases, Department of Metabolism, Digestion and Reproduction, Faculty of Medicine, Hammersmith Campus, Imperial College London, London, UKDepartment of Genetics, University of Groningen, University Medical Center Groningen, Groningen, The NetherlandsDivision Gastroenterology-Hepatology, Maastricht University Medical Center+, Maastricht, The NetherlandsThe Australian National Phenome Center, Harry Perkins Institute, Murdoch University, Perth, AustraliaDivision of Systems Medicine, Department of Metabolism, Digestion and Reproduction, Faculty of Medicine, South Kensington Campus, Imperial College London, London, UKDivision Gastroenterology-Hepatology, Maastricht University Medical Center+, Maastricht, The NetherlandsTo gain insight into the complex microbiome-gut-brain axis in irritable bowel syndrome (IBS), several modalities of biological and clinical data must be combined. We aimed to identify profiles of fecal microbiota and metabolites associated with IBS and to delineate specific phenotypes of IBS that represent potential pathophysiological mechanisms. Fecal metabolites were measured using proton nuclear magnetic resonance (1H-NMR) spectroscopy and gut microbiome using shotgun metagenomic sequencing (MGS) in a combined dataset of 142 IBS patients and 120 healthy controls (HCs) with extensive clinical, biological and phenotype information. Data were analyzed using support vector classification and regression and kernel t-SNE. Microbiome and metabolome profiles could distinguish IBS and HC with an area-under-the-receiver-operator-curve of 77.3% and 79.5%, respectively, but this could be improved by combining microbiota and metabolites to 83.6%. No significant differences in predictive ability of the microbiome–metabolome data were observed between the three classical, stool pattern-based, IBS subtypes. However, unsupervised clustering showed distinct subsets of IBS patients based on fecal microbiome–metabolome data. These clusters could be related plasma levels of serotonin and its metabolite 5-hydroxyindoleacetate, effects of psychological stress on gastrointestinal (GI) symptoms, onset of IBS after stressful events, medical history of previous abdominal surgery, dietary caloric intake and IBS symptom duration. Furthermore, pathways in metabolic reaction networks were integrated with microbiota data, that reflect the host-microbiome interactions in IBS. The identified microbiome–metabolome signatures for IBS, associated with altered serotonin metabolism and unfavorable stress response related to GI symptoms, support the microbiota-gut-brain link in the pathogenesis of IBS.https://www.tandfonline.com/doi/10.1080/19490976.2022.2063016Irritable bowel syndromegut microbiotamicrobiomegut metabolomefecal metabolomestress |
| spellingShingle | Zlatan Mujagic Melpomeni Kasapi Daisy MAE Jonkers Isabel Garcia-Perez Lisa Vork Zsa Zsa R.M. Weerts Jose Ivan Serrano-Contreras Alexandra Zhernakova Alexander Kurilshikov Jamie Scotcher Elaine Holmes Cisca Wijmenga Daniel Keszthelyi Jeremy K Nicholson Joram M Posma Ad AM Masclee Integrated fecal microbiome–metabolome signatures reflect stress and serotonin metabolism in irritable bowel syndrome Gut Microbes Irritable bowel syndrome gut microbiota microbiome gut metabolome fecal metabolome stress |
| title | Integrated fecal microbiome–metabolome signatures reflect stress and serotonin metabolism in irritable bowel syndrome |
| title_full | Integrated fecal microbiome–metabolome signatures reflect stress and serotonin metabolism in irritable bowel syndrome |
| title_fullStr | Integrated fecal microbiome–metabolome signatures reflect stress and serotonin metabolism in irritable bowel syndrome |
| title_full_unstemmed | Integrated fecal microbiome–metabolome signatures reflect stress and serotonin metabolism in irritable bowel syndrome |
| title_short | Integrated fecal microbiome–metabolome signatures reflect stress and serotonin metabolism in irritable bowel syndrome |
| title_sort | integrated fecal microbiome metabolome signatures reflect stress and serotonin metabolism in irritable bowel syndrome |
| topic | Irritable bowel syndrome gut microbiota microbiome gut metabolome fecal metabolome stress |
| url | https://www.tandfonline.com/doi/10.1080/19490976.2022.2063016 |
| work_keys_str_mv | AT zlatanmujagic integratedfecalmicrobiomemetabolomesignaturesreflectstressandserotoninmetabolisminirritablebowelsyndrome AT melpomenikasapi integratedfecalmicrobiomemetabolomesignaturesreflectstressandserotoninmetabolisminirritablebowelsyndrome AT daisymaejonkers integratedfecalmicrobiomemetabolomesignaturesreflectstressandserotoninmetabolisminirritablebowelsyndrome AT isabelgarciaperez integratedfecalmicrobiomemetabolomesignaturesreflectstressandserotoninmetabolisminirritablebowelsyndrome AT lisavork integratedfecalmicrobiomemetabolomesignaturesreflectstressandserotoninmetabolisminirritablebowelsyndrome AT zsazsarmweerts integratedfecalmicrobiomemetabolomesignaturesreflectstressandserotoninmetabolisminirritablebowelsyndrome AT joseivanserranocontreras integratedfecalmicrobiomemetabolomesignaturesreflectstressandserotoninmetabolisminirritablebowelsyndrome AT alexandrazhernakova integratedfecalmicrobiomemetabolomesignaturesreflectstressandserotoninmetabolisminirritablebowelsyndrome AT alexanderkurilshikov integratedfecalmicrobiomemetabolomesignaturesreflectstressandserotoninmetabolisminirritablebowelsyndrome AT jamiescotcher integratedfecalmicrobiomemetabolomesignaturesreflectstressandserotoninmetabolisminirritablebowelsyndrome AT elaineholmes integratedfecalmicrobiomemetabolomesignaturesreflectstressandserotoninmetabolisminirritablebowelsyndrome AT ciscawijmenga integratedfecalmicrobiomemetabolomesignaturesreflectstressandserotoninmetabolisminirritablebowelsyndrome AT danielkeszthelyi integratedfecalmicrobiomemetabolomesignaturesreflectstressandserotoninmetabolisminirritablebowelsyndrome AT jeremyknicholson integratedfecalmicrobiomemetabolomesignaturesreflectstressandserotoninmetabolisminirritablebowelsyndrome AT jorammposma integratedfecalmicrobiomemetabolomesignaturesreflectstressandserotoninmetabolisminirritablebowelsyndrome AT adammasclee integratedfecalmicrobiomemetabolomesignaturesreflectstressandserotoninmetabolisminirritablebowelsyndrome |