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

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. Lastly, 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 Inflammatorymore » Bowel Disease Multi’omics Database (http://ibdmdb.org), provide the most comprehensive description to date of host and microbial activities in inflammatory bowel diseases.« less

Authors:
 [1];  [2];  [3];  [4];  [5];  [5];  [3];  [6];  [7];  [8];  [9];  [3];  [10];  [9];  [5];  [11];  [12];  [7];  [5];  [13] more »;  [7];  [9];  [14];  [10];  [8];  [9];  [15];  [8];  [10];  [13];  [12];  [6];  [16];  [17];  [5];  [18];  [5];  [19];  [7] « less
+ Show Author Affiliations
  1. Broad Institute of MIT and Harvard, Cambridge, MA (United States); Harvard T.H. Chan School of Public Health, Boston, MA (United States)
  2. Harvard T.H. Chan School of Public Health, Boston, MA (United States)
  3. Massachusetts General Hospital, Boston, MA (United States)
  4. Broad Institute of MIT and Harvard, Cambridge, MA (United States); Massachusetts General Hospital, Boston, MA (United States)
  5. Broad Institute of MIT and Harvard, Cambridge, MA (United States)
  6. Baylor College of Medicine, Houston, TX (United States)
  7. Broad Institute of MIT and Harvard, Cambridge, MA (United States); Harvard T. H. Chan School of Public Health, Boston, MA (United States)
  8. Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
  9. Univ. of California Los Angeles, Los Angeles, CA (United States)
  10. Univ. of California San Diego, La Jolla, CA (United States)
  11. Cincinnati Children’s Hospital Medical Center, Cincinnati, OH (United States)
  12. Cedars-Sinai Medical Center, Los Angeles, CA (United States)
  13. Emory Univ., Atlanta, GA (United States)
  14. Broad Institute of MIT and Harvard, Cambridge, MA (United States); Umea Univ., Umea (Sweden)
  15. Cincinnati Children’s Hospital Medical Center, Cincinnati, OH (United States); Univ. of Cincinnati College of Medicine, Cincinnati, OH (United States)
  16. Washington Univ., St. Louis, MO (United States)
  17. MassGeneral Hospital for Children, Boston, MA (United States); Harvard Medical School, Boston, MA (United States)
  18. Harvard T. H. Chan School of Public Health, Boston, MA (United States)
  19. Broad Institute of MIT and Harvard, Cambridge, MA (United States); Massachusetts General Hospital, Boston, MA (United States); Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States)
Publication Date:
Research Org.:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE
Contributing Org.:
IBDMDB Investigators
OSTI Identifier:
1573018
Report Number(s):
PNNL-SA-132723
Journal ID: ISSN 0028-0836
Grant/Contract Number:  
AC05-76RL01830
Resource Type:
Accepted Manuscript
Journal Name:
Nature (London)
Additional Journal Information:
Journal Name: Nature (London); Journal Volume: 569; Journal Issue: 7758; Journal ID: ISSN 0028-0836
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
60 APPLIED LIFE SCIENCES; microbiome; IBD; multiomics

Citation Formats

Lloyd-Price, Jason, Arze, Cesar, Ananthakrishnan, Ashwin N., Schirmer, Melanie, Avila-Pacheco, Julian, Poon, Tiffany W., Andrews, Elizabeth, Ajami, Nadim J., Bonham, Kevin S., Brislawn, Colin J., Casero, David, Courtney, Holly, Gonzalez, Antonio, Graeber, Thomas G., Hall, A. Brantley, Lake, Kathleen, Landers, Carol J., Mallick, Himel, Plichta, Damian R., Prasad, Mahadev, Rahnavard, Gholamali, Sauk, Jenny, Shungin, Dmitry, Vázquez-Baeza, Yoshiki, White, III, Richard A., Braun, Jonathan, Denson, Lee A., Jansson, Janet K., Knight, Rob, Kugathasan, Subra, McGovern, Dermot P. B., Petrosino, Joseph F., Stappenbeck, Thaddeus S., Winter, Harland S., Clish, Clary B., Franzosa, Eric A., Vlamakis, Hera, Xavier, Ramnik J., and Huttenhower, Curtis. Multi-omics of the gut microbial ecosystem in inflammatory bowel diseases. United States: N. p., 2019. Web. doi:10.1038/s41586-019-1237-9.
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Lloyd-Price, Jason, Arze, Cesar, Ananthakrishnan, Ashwin N., Schirmer, Melanie, Avila-Pacheco, Julian, Poon, Tiffany W., Andrews, Elizabeth, Ajami, Nadim J., Bonham, Kevin S., Brislawn, Colin J., Casero, David, Courtney, Holly, Gonzalez, Antonio, Graeber, Thomas G., Hall, A. Brantley, Lake, Kathleen, Landers, Carol J., Mallick, Himel, Plichta, Damian R., Prasad, Mahadev, Rahnavard, Gholamali, Sauk, Jenny, Shungin, Dmitry, Vázquez-Baeza, Yoshiki, White, III, Richard A., Braun, Jonathan, Denson, Lee A., Jansson, Janet K., Knight, Rob, Kugathasan, Subra, McGovern, Dermot P. B., Petrosino, Joseph F., Stappenbeck, Thaddeus S., Winter, Harland S., Clish, Clary B., Franzosa, Eric A., Vlamakis, Hera, Xavier, Ramnik J., & Huttenhower, Curtis. Multi-omics of the gut microbial ecosystem in inflammatory bowel diseases. United States. https://doi.org/10.1038/s41586-019-1237-9
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Lloyd-Price, Jason, Arze, Cesar, Ananthakrishnan, Ashwin N., Schirmer, Melanie, Avila-Pacheco, Julian, Poon, Tiffany W., Andrews, Elizabeth, Ajami, Nadim J., Bonham, Kevin S., Brislawn, Colin J., Casero, David, Courtney, Holly, Gonzalez, Antonio, Graeber, Thomas G., Hall, A. Brantley, Lake, Kathleen, Landers, Carol J., Mallick, Himel, Plichta, Damian R., Prasad, Mahadev, Rahnavard, Gholamali, Sauk, Jenny, Shungin, Dmitry, Vázquez-Baeza, Yoshiki, White, III, Richard A., Braun, Jonathan, Denson, Lee A., Jansson, Janet K., Knight, Rob, Kugathasan, Subra, McGovern, Dermot P. B., Petrosino, Joseph F., Stappenbeck, Thaddeus S., Winter, Harland S., Clish, Clary B., Franzosa, Eric A., Vlamakis, Hera, Xavier, Ramnik J., and Huttenhower, Curtis. Wed . "Multi-omics of the gut microbial ecosystem in inflammatory bowel diseases". United States. https://doi.org/10.1038/s41586-019-1237-9. https://www.osti.gov/servlets/purl/1573018.
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@article{osti_1573018,
title = {Multi-omics of the gut microbial ecosystem in inflammatory bowel diseases},
author = {Lloyd-Price, Jason and Arze, Cesar and Ananthakrishnan, Ashwin N. and Schirmer, Melanie and Avila-Pacheco, Julian and Poon, Tiffany W. and Andrews, Elizabeth and Ajami, Nadim J. and Bonham, Kevin S. and Brislawn, Colin J. and Casero, David and Courtney, Holly and Gonzalez, Antonio and Graeber, Thomas G. and Hall, A. Brantley and Lake, Kathleen and Landers, Carol J. and Mallick, Himel and Plichta, Damian R. and Prasad, Mahadev and Rahnavard, Gholamali and Sauk, Jenny and Shungin, Dmitry and Vázquez-Baeza, Yoshiki and White, III, Richard A. and Braun, Jonathan and Denson, Lee A. and Jansson, Janet K. and Knight, Rob and Kugathasan, Subra and McGovern, Dermot P. B. and Petrosino, Joseph F. and Stappenbeck, Thaddeus S. and Winter, Harland S. and Clish, Clary B. and Franzosa, Eric A. and Vlamakis, Hera and Xavier, Ramnik J. and Huttenhower, Curtis},
abstractNote = {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. Lastly, 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.},
doi = {10.1038/s41586-019-1237-9},
journal = {Nature (London)},
number = 7758,
volume = 569,
place = {United States},
year = {2019},
month = {5}
}
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Fine-mapping inflammatory bowel disease loci to single-variant resolution.
text, January 2017

  • Huang, Hailiang; Fang, Ming; Jostins, Luke
  • Apollo - University of Cambridge Repository
  • DOI: 10.17863/cam.24524

The Dynamics of the Human Infant Gut Microbiome in Development and in Progression toward Type 1 Diabetes
journal, July 2016

A global reference for human genetic variation
text, January 2015

  • Xiaosen, Guo,; Meifang, Tang,; Tianming, Lan,
  • The University of North Carolina at Chapel Hill University Libraries
  • DOI: 10.17615/0ez3-8z76

A communal catalogue reveals Earths multiscale microbial diversity
text, January 2017

limma powers differential expression analyses for RNA-sequencing and microarray studies
text, January 2015

  • Ritchie, Matthew E.; Phipson, Belinda; Wu, Di
  • Oxford University Press
  • DOI: 10.5167/uzh-155268

Density Estimation for Statistics and Data Analysis
journal, November 1987

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