Multi-omics of the gut microbial ecosystem in inflammatory bowel diseases

Jason Lloyd-Price, Cesar Arze, Ashwin N. Ananthakrishnan, Melanie Schirmer, Julian Avila-Pacheco, Tiffany W. Poon, Elizabeth Andrews, Nadim J. Ajami, Kevin S. Bonham, Colin J. Brislawn, David Casero, Holly Courtney, Antonio Gonzalez, Thomas G. Graeber, A. Brantley Hall, Kathleen Lake, Carol J. Landers, Himel Mallick, Damian R. Plichta, Mahadev Prasad, Gholamali Rahnavard, Jenny Sauk, Dmitry Shungin, Yoshiki Vázquez-Baeza, Richard A. White, Jonathan Braun, Lee A. Denson, Janet K. Jansson, Rob Knight, Subra Kugathasan, Dermot P. B. McGovern, Joseph F. Petrosino, Thaddeus S. Stappenbeck, Harland S. Winter, Clary B. Clish, Eric A. Franzosa, Hera Vlamakis, Ramnik J. Xavier and Curtis Huttenhower ()
Additional contact information
Jason Lloyd-Price: Broad Institute of MIT and Harvard
Cesar Arze: Harvard T. H. Chan School of Public Health
Ashwin N. Ananthakrishnan: Gastroenterology, Massachusetts General Hospital
Melanie Schirmer: Broad Institute of MIT and Harvard
Julian Avila-Pacheco: Broad Institute of MIT and Harvard
Tiffany W. Poon: Broad Institute of MIT and Harvard
Elizabeth Andrews: Gastroenterology, Massachusetts General Hospital
Nadim J. Ajami: Baylor College of Medicine
Kevin S. Bonham: Broad Institute of MIT and Harvard
Colin J. Brislawn: Pacific Northwest National Lab
David Casero: University of California Los Angeles
Holly Courtney: Gastroenterology, Massachusetts General Hospital
Antonio Gonzalez: University of California San Diego
Thomas G. Graeber: University of California Los Angeles
A. Brantley Hall: Broad Institute of MIT and Harvard
Kathleen Lake: Cincinnati Children’s Hospital Medical Center
Carol J. Landers: Cedars-Sinai Medical Center
Himel Mallick: Broad Institute of MIT and Harvard
Damian R. Plichta: Broad Institute of MIT and Harvard
Mahadev Prasad: Emory University
Gholamali Rahnavard: Broad Institute of MIT and Harvard
Jenny Sauk: University of California Los Angeles
Dmitry Shungin: Broad Institute of MIT and Harvard
Yoshiki Vázquez-Baeza: University of California San Diego
Richard A. White: Pacific Northwest National Lab
Jonathan Braun: University of California Los Angeles
Lee A. Denson: Cincinnati Children’s Hospital Medical Center
Janet K. Jansson: Pacific Northwest National Lab
Rob Knight: University of California San Diego
Subra Kugathasan: Emory University
Dermot P. B. McGovern: Cedars-Sinai Medical Center
Joseph F. Petrosino: Baylor College of Medicine
Thaddeus S. Stappenbeck: Washington University
Harland S. Winter: MassGeneral Hospital for Children
Clary B. Clish: Broad Institute of MIT and Harvard
Eric A. Franzosa: Harvard T. H. Chan School of Public Health
Hera Vlamakis: Broad Institute of MIT and Harvard
Ramnik J. Xavier: Broad Institute of MIT and Harvard
Curtis Huttenhower: Broad Institute of MIT and Harvard

Nature, 2019, vol. 569, issue 7758, 655-662

Abstract: Abstract Inflammatory bowel diseases, which include Crohn’s disease and ulcerative colitis, affect several million individuals worldwide. Crohn’s disease and ulcerative colitis are complex diseases that are heterogeneous at the clinical, immunological, molecular, genetic, and microbial levels. Individual contributing factors have been the focus of extensive research. As part of the Integrative Human Microbiome Project (HMP2 or iHMP), we followed 132 subjects for one year each to generate integrated longitudinal molecular profiles of host and microbial activity during disease (up to 24 time points each; in total 2,965 stool, biopsy, and blood specimens). Here we present the results, which provide a comprehensive view of functional dysbiosis in the gut microbiome during inflammatory bowel disease activity. We demonstrate a characteristic increase in facultative anaerobes at the expense of obligate anaerobes, as well as molecular disruptions in microbial transcription (for example, among clostridia), metabolite pools (acylcarnitines, bile acids, and short-chain fatty acids), and levels of antibodies in host serum. Periods of disease activity were also marked by increases in temporal variability, with characteristic taxonomic, functional, and biochemical shifts. Finally, integrative analysis identified microbial, biochemical, and host factors central to this dysregulation. The study’s infrastructure resources, results, and data, which are available through the Inflammatory Bowel Disease Multi’omics Database ( http://ibdmdb.org ), provide the most comprehensive description to date of host and microbial activities in inflammatory bowel diseases.

Date: 2019
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DOI: 10.1038/s41586-019-1237-9

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