Gut microbiome structure and metabolic activity in inflammatory bowel disease
The inflammatory bowel diseases (IBDs), which include Crohn’s disease (CD) and ulcerative colitis (UC), are multifactorial chronic conditions of the gastrointestinal tract. While IBD has been associated with dramatic changes in the gut microbiota, changes in the gut metabolome—the molecular interfac...
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| Published in | Nature microbiology Vol. 4; no. 2; pp. 293 - 305 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
London
Nature Publishing Group UK
01.02.2019
Nature Publishing Group |
| Subjects | |
| Online Access | Get full text |
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| Abstract | The inflammatory bowel diseases (IBDs), which include Crohn’s disease (CD) and ulcerative colitis (UC), are multifactorial chronic conditions of the gastrointestinal tract. While IBD has been associated with dramatic changes in the gut microbiota, changes in the gut metabolome—the molecular interface between host and microbiota—are less well understood. To address this gap, we performed untargeted metabolomic and shotgun metagenomic profiling of cross-sectional stool samples from discovery (
n
= 155) and validation (
n
= 65) cohorts of CD, UC and non-IBD control patients. Metabolomic and metagenomic profiles were broadly correlated with faecal calprotectin levels (a measure of gut inflammation). Across >8,000 measured metabolite features, we identified chemicals and chemical classes that were differentially abundant in IBD, including enrichments for sphingolipids and bile acids, and depletions for triacylglycerols and tetrapyrroles. While > 50% of differentially abundant metabolite features were uncharacterized, many could be assigned putative roles through metabolomic ‘guilt by association’ (covariation with known metabolites). Differentially abundant species and functions from the metagenomic profiles reflected adaptation to oxidative stress in the IBD gut, and were individually consistent with previous findings. Integrating these data, however, we identified 122 robust associations between differentially abundant species and well-characterized differentially abundant metabolites, indicating possible mechanistic relationships that are perturbed in IBD. Finally, we found that metabolome- and metagenome-based classifiers of IBD status were highly accurate and, like the vast majority of individual trends, generalized well to the independent validation cohort. Our findings thus provide an improved understanding of perturbations of the microbiome–metabolome interface in IBD, including identification of many potential diagnostic and therapeutic targets.
Using metabolomics and shotgun metagenomics on stool samples from individuals with and without inflammatory bowel disease, metabolites, microbial species and genes associated with disease were identified and validated in an independent cohort. |
|---|---|
| AbstractList | The inflammatory bowel diseases (IBDs), which include Crohn's disease (CD) and ulcerative colitis (UC), are multifactorial chronic conditions of the gastrointestinal tract. While IBD has been associated with dramatic changes in the gut microbiota, changes in the gut metabolome-the molecular interface between host and microbiota-are less well understood. To address this gap, we performed untargeted metabolomic and shotgun metagenomic profiling of cross-sectional stool samples from discovery (n = 155) and validation (n = 65) cohorts of CD, UC and non-IBD control patients. Metabolomic and metagenomic profiles were broadly correlated with faecal calprotectin levels (a measure of gut inflammation). Across >8,000 measured metabolite features, we identified chemicals and chemical classes that were differentially abundant in IBD, including enrichments for sphingolipids and bile acids, and depletions for triacylglycerols and tetrapyrroles. While > 50% of differentially abundant metabolite features were uncharacterized, many could be assigned putative roles through metabolomic 'guilt by association' (covariation with known metabolites). Differentially abundant species and functions from the metagenomic profiles reflected adaptation to oxidative stress in the IBD gut, and were individually consistent with previous findings. Integrating these data, however, we identified 122 robust associations between differentially abundant species and well-characterized differentially abundant metabolites, indicating possible mechanistic relationships that are perturbed in IBD. Finally, we found that metabolome- and metagenome-based classifiers of IBD status were highly accurate and, like the vast majority of individual trends, generalized well to the independent validation cohort. Our findings thus provide an improved understanding of perturbations of the microbiome-metabolome interface in IBD, including identification of many potential diagnostic and therapeutic targets.The inflammatory bowel diseases (IBDs), which include Crohn's disease (CD) and ulcerative colitis (UC), are multifactorial chronic conditions of the gastrointestinal tract. While IBD has been associated with dramatic changes in the gut microbiota, changes in the gut metabolome-the molecular interface between host and microbiota-are less well understood. To address this gap, we performed untargeted metabolomic and shotgun metagenomic profiling of cross-sectional stool samples from discovery (n = 155) and validation (n = 65) cohorts of CD, UC and non-IBD control patients. Metabolomic and metagenomic profiles were broadly correlated with faecal calprotectin levels (a measure of gut inflammation). Across >8,000 measured metabolite features, we identified chemicals and chemical classes that were differentially abundant in IBD, including enrichments for sphingolipids and bile acids, and depletions for triacylglycerols and tetrapyrroles. While > 50% of differentially abundant metabolite features were uncharacterized, many could be assigned putative roles through metabolomic 'guilt by association' (covariation with known metabolites). Differentially abundant species and functions from the metagenomic profiles reflected adaptation to oxidative stress in the IBD gut, and were individually consistent with previous findings. Integrating these data, however, we identified 122 robust associations between differentially abundant species and well-characterized differentially abundant metabolites, indicating possible mechanistic relationships that are perturbed in IBD. Finally, we found that metabolome- and metagenome-based classifiers of IBD status were highly accurate and, like the vast majority of individual trends, generalized well to the independent validation cohort. Our findings thus provide an improved understanding of perturbations of the microbiome-metabolome interface in IBD, including identification of many potential diagnostic and therapeutic targets. The inflammatory bowel diseases (IBDs), which include Crohn's disease (CD) and ulcerative colitis (UC), are multifactorial chronic conditions of the gastrointestinal tract. While IBD has been associated with dramatic changes in the gut microbiota, changes in the gut metabolome-the molecular interface between host and microbiota-are less well understood. To address this gap, we performed untargeted metabolomic and shotgun metagenomic profiling of cross-sectional stool samples from discovery (n = 155) and validation (n = 65) cohorts of CD, UC and non-IBD control patients. Metabolomic and metagenomic profiles were broadly correlated with faecal calprotectin levels (a measure of gut inflammation). Across >8,000 measured metabolite features, we identified chemicals and chemical classes that were differentially abundant in IBD, including enrichments for sphingolipids and bile acids, and depletions for triacylglycerols and tetrapyrroles. While > 50% of differentially abundant metabolite features were uncharacterized, many could be assigned putative roles through metabolomic 'guilt by association' (covariation with known metabolites). Differentially abundant species and functions from the metagenomic profiles reflected adaptation to oxidative stress in the IBD gut, and were individually consistent with previous findings. Integrating these data, however, we identified 122 robust associations between differentially abundant species and well-characterized differentially abundant metabolites, indicating possible mechanistic relationships that are perturbed in IBD. Finally, we found that metabolome- and metagenome-based classifiers of IBD status were highly accurate and, like the vast majority of individual trends, generalized well to the independent validation cohort. Our findings thus provide an improved understanding of perturbations of the microbiome-metabolome interface in IBD, including identification of many potential diagnostic and therapeutic targets. The inflammatory bowel diseases (IBDs), which include Crohn’s disease (CD) and ulcerative colitis (UC), are multifactorial chronic conditions of the gastrointestinal tract. While IBD has been associated with dramatic changes in the gut microbiota, changes in the gut metabolome—the molecular interface between host and microbiota—are less well understood. To address this gap, we performed untargeted metabolomic and shotgun metagenomic profiling of cross-sectional stool samples from discovery ( n = 155) and validation ( n = 65) cohorts of CD, UC and non-IBD control patients. Metabolomic and metagenomic profiles were broadly correlated with faecal calprotectin levels (a measure of gut inflammation). Across >8,000 measured metabolite features, we identified chemicals and chemical classes that were differentially abundant in IBD, including enrichments for sphingolipids and bile acids, and depletions for triacylglycerols and tetrapyrroles. While > 50% of differentially abundant metabolite features were uncharacterized, many could be assigned putative roles through metabolomic ‘guilt by association’ (covariation with known metabolites). Differentially abundant species and functions from the metagenomic profiles reflected adaptation to oxidative stress in the IBD gut, and were individually consistent with previous findings. Integrating these data, however, we identified 122 robust associations between differentially abundant species and well-characterized differentially abundant metabolites, indicating possible mechanistic relationships that are perturbed in IBD. Finally, we found that metabolome- and metagenome-based classifiers of IBD status were highly accurate and, like the vast majority of individual trends, generalized well to the independent validation cohort. Our findings thus provide an improved understanding of perturbations of the microbiome–metabolome interface in IBD, including identification of many potential diagnostic and therapeutic targets. Using metabolomics and shotgun metagenomics on stool samples from individuals with and without inflammatory bowel disease, metabolites, microbial species and genes associated with disease were identified and validated in an independent cohort. The inflammatory bowel diseases (IBD), which include Crohn’s disease (CD) and ulcerative colitis (UC), are multifactorial, chronic conditions of the gastrointestinal tract. While IBD has been associated with dramatic changes in the gut microbiota, changes in the gut metabolome -- the molecular interface between host and microbiota -- are less-well understood. To address this gap, we performed untargeted LC-MS metabolomic and shotgun metagenomic profiling of cross-sectional stool samples from discovery ( n =155) and validation ( n =65) cohorts of CD, UC, and non-IBD control subjects. Metabolomic and metagenomic profiles were broadly correlated with fecal calprotectin levels (a measure of gut inflammation). Across >8,000 measured metabolite features, we identified chemicals and chemical classes that were differentially abundant (DA) in IBD, including enrichments for sphingolipids and bile acids, and depletions for triacylglycerols and tetrapyrroles. While >50% of DA metabolite features were uncharacterized, many could be assigned putative roles through metabolomic “guilt-by-association” (covariation with known metabolites). DA species and functions from the metagenomic profiles reflected adaptation to oxidative stress in the IBD gut, and were individually consistent with previous findings. Integrating these data, however, we identified 122 robust associations between DA species and well-characterized DA metabolites, indicating possible mechanistic relationships that are perturbed in IBD. Finally, we found that metabolome- and metagenome-based classifiers of IBD status were highly accurate and, like the vast majority of individual trends, generalized well to the independent validation cohort. Our findings thus provide an improved understanding of perturbations of the microbiome-metabolome interface in IBD, including identification of many potential diagnostic and therapeutic targets. |
| Author | Wijmenga, Cisca Avila-Pacheco, Julian Imhann, Floris Stevens, Betsy W. Clish, Clary B. Franzosa, Eric A. Haiser, Henry J. Vatanen, Tommi Scott, Justin M. Weersma, Rinse K. Bullock, Kevin Deik, Amy A. Hall, A. Brantley McIver, Lauren J. Huttenhower, Curtis Fu, Jingyuan Pierce, Kerry Fornelos, Nadine Porter, Jeffrey A. Mallick, Himel Sirota-Madi, Alexandra Xavier, Ramnik J. Wilson, Robin G. Reinker, Stefan Zhernakova, Alexandra Sauk, Jenny S. Vlamakis, Hera |
| AuthorAffiliation | 4 Gastrointestinal Unit and Center for the Study of Inflammatory Bowel Disease, Massachusetts General Hospital and Harvard Medical School, Boston, MA 02114, USA 2 Department of Biostatistics, Harvard School of Public Health, Boston, MA 02115, USA 8 K.G. Jebsen Coeliac Disease Research Centre, Department of Immunology, University of Oslo, Norway 7 University of Groningen and University Medical Center Groningen, Department of Pediatrics, Groningen, the Netherlands 3 Novartis Institute for Biomedical Research Inc., Cambridge, MA 02139, USA 5 University of Groningen and University Medical Center Groningen, Department of Gastroenterology and Hepatology, Groningen, the Netherlands 6 University of Groningen and University Medical Center Groningen, Department of Genetics, Groningen, the Netherlands 9 Center for Microbiome Informatics and Therapeutics, Massachusetts Institute of Technology, Cambridge, MA 02139, USA 1 Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA |
| AuthorAffiliation_xml | – name: 8 K.G. Jebsen Coeliac Disease Research Centre, Department of Immunology, University of Oslo, Norway – name: 1 Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA – name: 5 University of Groningen and University Medical Center Groningen, Department of Gastroenterology and Hepatology, Groningen, the Netherlands – name: 2 Department of Biostatistics, Harvard School of Public Health, Boston, MA 02115, USA – name: 9 Center for Microbiome Informatics and Therapeutics, Massachusetts Institute of Technology, Cambridge, MA 02139, USA – name: 4 Gastrointestinal Unit and Center for the Study of Inflammatory Bowel Disease, Massachusetts General Hospital and Harvard Medical School, Boston, MA 02114, USA – name: 6 University of Groningen and University Medical Center Groningen, Department of Genetics, Groningen, the Netherlands – name: 3 Novartis Institute for Biomedical Research Inc., Cambridge, MA 02139, USA – name: 7 University of Groningen and University Medical Center Groningen, Department of Pediatrics, Groningen, the Netherlands |
| Author_xml | – sequence: 1 givenname: Eric A. orcidid: 0000-0002-8798-7068 surname: Franzosa fullname: Franzosa, Eric A. organization: Broad Institute of MIT and Harvard, Department of Biostatistics, Harvard School of Public Health – sequence: 2 givenname: Alexandra surname: Sirota-Madi fullname: Sirota-Madi, Alexandra organization: Broad Institute of MIT and Harvard – sequence: 3 givenname: Julian surname: Avila-Pacheco fullname: Avila-Pacheco, Julian organization: Broad Institute of MIT and Harvard – sequence: 4 givenname: Nadine surname: Fornelos fullname: Fornelos, Nadine organization: Broad Institute of MIT and Harvard – sequence: 5 givenname: Henry J. surname: Haiser fullname: Haiser, Henry J. organization: Novartis Institute for Biomedical Research Inc – sequence: 6 givenname: Stefan surname: Reinker fullname: Reinker, Stefan organization: Novartis Institute for Biomedical Research Inc – sequence: 7 givenname: Tommi orcidid: 0000-0003-0949-1291 surname: Vatanen fullname: Vatanen, Tommi organization: Broad Institute of MIT and Harvard – sequence: 8 givenname: A. Brantley surname: Hall fullname: Hall, A. Brantley organization: Broad Institute of MIT and Harvard – sequence: 9 givenname: Himel surname: Mallick fullname: Mallick, Himel organization: Broad Institute of MIT and Harvard, Department of Biostatistics, Harvard School of Public Health – sequence: 10 givenname: Lauren J. surname: McIver fullname: McIver, Lauren J. organization: Broad Institute of MIT and Harvard, Department of Biostatistics, Harvard School of Public Health – sequence: 11 givenname: Jenny S. surname: Sauk fullname: Sauk, Jenny S. organization: Gastrointestinal Unit and Center for the Study of Inflammatory Bowel Disease, Massachusetts General Hospital and Harvard Medical School – sequence: 12 givenname: Robin G. surname: Wilson fullname: Wilson, Robin G. organization: Gastrointestinal Unit and Center for the Study of Inflammatory Bowel Disease, Massachusetts General Hospital and Harvard Medical School – sequence: 13 givenname: Betsy W. surname: Stevens fullname: Stevens, Betsy W. organization: Gastrointestinal Unit and Center for the Study of Inflammatory Bowel Disease, Massachusetts General Hospital and Harvard Medical School – sequence: 14 givenname: Justin M. surname: Scott fullname: Scott, Justin M. organization: Broad Institute of MIT and Harvard – sequence: 15 givenname: Kerry surname: Pierce fullname: Pierce, Kerry organization: Broad Institute of MIT and Harvard – sequence: 16 givenname: Amy A. surname: Deik fullname: Deik, Amy A. organization: Broad Institute of MIT and Harvard – sequence: 17 givenname: Kevin surname: Bullock fullname: Bullock, Kevin organization: Broad Institute of MIT and Harvard – sequence: 18 givenname: Floris orcidid: 0000-0001-5278-903X surname: Imhann fullname: Imhann, Floris organization: Department of Gastroenterology and Hepatology, University of Groningen and University Medical Center Groningen, Department of Genetics, University of Groningen and University Medical Center Groningen – sequence: 19 givenname: Jeffrey A. surname: Porter fullname: Porter, Jeffrey A. organization: Novartis Institute for Biomedical Research Inc – sequence: 20 givenname: Alexandra surname: Zhernakova fullname: Zhernakova, Alexandra organization: Department of Genetics, University of Groningen and University Medical Center Groningen – sequence: 21 givenname: Jingyuan surname: Fu fullname: Fu, Jingyuan organization: Department of Genetics, University of Groningen and University Medical Center Groningen, Department of Pediatrics, University of Groningen and University Medical Center Groningen – sequence: 22 givenname: Rinse K. surname: Weersma fullname: Weersma, Rinse K. organization: Department of Gastroenterology and Hepatology, University of Groningen and University Medical Center Groningen – sequence: 23 givenname: Cisca surname: Wijmenga fullname: Wijmenga, Cisca organization: Department of Genetics, University of Groningen and University Medical Center Groningen, Department of Immunology, K.G. Jebsen Coeliac Disease Research Centre, University of Oslo – sequence: 24 givenname: Clary B. orcidid: 0000-0001-8259-9245 surname: Clish fullname: Clish, Clary B. organization: Broad Institute of MIT and Harvard – sequence: 25 givenname: Hera surname: Vlamakis fullname: Vlamakis, Hera organization: Broad Institute of MIT and Harvard – sequence: 26 givenname: Curtis orcidid: 0000-0002-1110-0096 surname: Huttenhower fullname: Huttenhower, Curtis email: chuttenh@hsph.harvard.edu organization: Broad Institute of MIT and Harvard, Department of Biostatistics, Harvard School of Public Health – sequence: 27 givenname: Ramnik J. orcidid: 0000-0002-5630-5167 surname: Xavier fullname: Xavier, Ramnik J. email: xavier@molbio.mgh.harvard.edu organization: Broad Institute of MIT and Harvard, Gastrointestinal Unit and Center for the Study of Inflammatory Bowel Disease, Massachusetts General Hospital and Harvard Medical School, Center for Microbiome Informatics and Therapeutics, Massachusetts Institute of Technology |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/30531976$$D View this record in MEDLINE/PubMed |
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| Snippet | The inflammatory bowel diseases (IBDs), which include Crohn’s disease (CD) and ulcerative colitis (UC), are multifactorial chronic conditions of the... The inflammatory bowel diseases (IBDs), which include Crohn's disease (CD) and ulcerative colitis (UC), are multifactorial chronic conditions of the... The inflammatory bowel diseases (IBD), which include Crohn’s disease (CD) and ulcerative colitis (UC), are multifactorial, chronic conditions of the... |
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| SubjectTerms | 631/326/2565/2134 631/326/2565/2142 631/61/320 692/699/1503/257 Bile acids Biodiversity Biomarkers - metabolism Biomedical and Life Sciences Colitis, Ulcerative - immunology Colitis, Ulcerative - metabolism Colitis, Ulcerative - microbiology Crohn Disease - immunology Crohn Disease - metabolism Crohn Disease - microbiology Digestive system Feces - chemistry Feces - microbiology Gastrointestinal Microbiome - genetics Gastrointestinal Microbiome - immunology Gastrointestinal tract Humans Infectious Diseases Inflammation - metabolism Inflammation - microbiology Inflammatory bowel disease Inflammatory bowel diseases Inflammatory Bowel Diseases - immunology Inflammatory Bowel Diseases - metabolism Inflammatory Bowel Diseases - microbiology Intestinal microflora Intestine Leukocyte L1 Antigen Complex - analysis Life Sciences Medical Microbiology Metabolites Metabolome Metabolomics Metagenome Microbiology Microbiomes Microbiota Oxidative stress Parasitology Sphingolipids Tetrapyrroles Therapeutic applications Ulcerative colitis Virology |
| Title | Gut microbiome structure and metabolic activity in inflammatory bowel disease |
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