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Research Article | Host-Microbe Biology

American Gut: an Open Platform for Citizen Science Microbiome Research

Daniel McDonald, Embriette Hyde, Justine W. Debelius, James T. Morton, Antonio Gonzalez, Gail Ackermann, Alexander A. Aksenov, Bahar Behsaz, Caitriona Brennan, Yingfeng Chen, Lindsay DeRight Goldasich, Pieter C. Dorrestein, Robert R. Dunn, Ashkaan K. Fahimipour, James Gaffney, Jack A. Gilbert, Grant Gogul, Jessica L. Green, Philip Hugenholtz, Greg Humphrey, Curtis Huttenhower, Matthew A. Jackson, Stefan Janssen, Dilip V. Jeste, Lingjing Jiang, Scott T. Kelley, Dan Knights, Tomasz Kosciolek, Joshua Ladau, Jeff Leach, Clarisse Marotz, Dmitry Meleshko, Alexey V. Melnik, Jessica L. Metcalf, Hosein Mohimani, Emmanuel Montassier, Jose Navas-Molina, Tanya T. Nguyen, Shyamal Peddada, Pavel Pevzner, Katherine S. Pollard, Gholamali Rahnavard, Adam Robbins-Pianka, Naseer Sangwan, Joshua Shorenstein, Larry Smarr, Se Jin Song, Timothy Spector, Austin D. Swafford, Varykina G. Thackray, Luke R. Thompson, Anupriya Tripathi, Yoshiki Vázquez-Baeza, Alison Vrbanac, Paul Wischmeyer, Elaine Wolfe, Qiyun Zhu, The American Gut Consortium, Rob Knight
Casey S. Greene, Editor
Daniel McDonald
aDepartment of Pediatrics, University of California San Diego, La Jolla, California, USA
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Embriette Hyde
aDepartment of Pediatrics, University of California San Diego, La Jolla, California, USA
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Justine W. Debelius
aDepartment of Pediatrics, University of California San Diego, La Jolla, California, USA
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James T. Morton
aDepartment of Pediatrics, University of California San Diego, La Jolla, California, USA
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Antonio Gonzalez
aDepartment of Pediatrics, University of California San Diego, La Jolla, California, USA
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Gail Ackermann
aDepartment of Pediatrics, University of California San Diego, La Jolla, California, USA
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Alexander A. Aksenov
bCollaborative Mass Spectrometry Innovation Center, University of California, San Diego, La Jolla, California, USA
cSkaggs School of Pharmacy and Pharmaceutical Sciences, University of California, San Diego, La Jolla, California, USA
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Bahar Behsaz
dDepartment of Computer Science and Engineering, University of California, San Diego, La Jolla, California, USA
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Caitriona Brennan
aDepartment of Pediatrics, University of California San Diego, La Jolla, California, USA
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Yingfeng Chen
eDepartment of Biology, San Diego State University, San Diego, California, USA
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Lindsay DeRight Goldasich
aDepartment of Pediatrics, University of California San Diego, La Jolla, California, USA
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Pieter C. Dorrestein
bCollaborative Mass Spectrometry Innovation Center, University of California, San Diego, La Jolla, California, USA
cSkaggs School of Pharmacy and Pharmaceutical Sciences, University of California, San Diego, La Jolla, California, USA
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Robert R. Dunn
fDepartment of Applied Ecology, North Carolina State University, Raleigh, North Carolina, USA
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Ashkaan K. Fahimipour
gBiology and the Built Environment Center, University of Oregon, Eugene, Oregon, USA
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James Gaffney
aDepartment of Pediatrics, University of California San Diego, La Jolla, California, USA
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Jack A. Gilbert
hDepartment of Surgery, University of Chicago, Chicago, Illinois, USA
iInstitute for Genomic and Systems Biology, University of Chicago, Chicago, Illinois, USA
jDepartment of Biosciences, Argonne National Laboratory, Chicago, Illinois, USA
kMarine Biology Laboratory, University of Chicago, Chicago, Illinois, USA
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Grant Gogul
aDepartment of Pediatrics, University of California San Diego, La Jolla, California, USA
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Jessica L. Green
gBiology and the Built Environment Center, University of Oregon, Eugene, Oregon, USA
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Philip Hugenholtz
lAustralian Centre for Ecogenomics, School of Chemistry and Molecular Biosciences, the University of Queensland, Brisbane, QLD, Australia
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Greg Humphrey
aDepartment of Pediatrics, University of California San Diego, La Jolla, California, USA
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Curtis Huttenhower
mHarvard T. H. Chan School of Public Health, Boston, Massachusetts, USA
nThe Broad Institute of MIT and Harvard, Cambridge, Massachusetts, USA
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Matthew A. Jackson
oDepartment of Twin Research and Genetic Epidemiology, King’s College London, London, United Kingdom
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Stefan Janssen
aDepartment of Pediatrics, University of California San Diego, La Jolla, California, USA
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Dilip V. Jeste
pDepartments of Psychiatry and Neurosciences, University of California San Diego, La Jolla, California, USA
qSam and Rose Stein Institute for Research on Aging and Center for Healthy Aging, University of California San Diego, La Jolla, California, USA
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Lingjing Jiang
aDepartment of Pediatrics, University of California San Diego, La Jolla, California, USA
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Scott T. Kelley
eDepartment of Biology, San Diego State University, San Diego, California, USA
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Dan Knights
rDepartment of Computer Science and Engineering, University of Minnesota, Minneapolis, Minnesota, USA
sBiotechnology Institute, University of Minnesota, Minneapolis, Minnesota, USA
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Tomasz Kosciolek
aDepartment of Pediatrics, University of California San Diego, La Jolla, California, USA
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Joshua Ladau
tThe Gladstone Institutes, University of California, San Francisco, California, USA
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Jeff Leach
uHuman Food Project, Terlingua, Texas, USA
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Clarisse Marotz
aDepartment of Pediatrics, University of California San Diego, La Jolla, California, USA
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Dmitry Meleshko
vSt. Petersburg State University, Center for Algorithmic Biotechnology, Saint Petersburg, Russia
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Alexey V. Melnik
bCollaborative Mass Spectrometry Innovation Center, University of California, San Diego, La Jolla, California, USA
cSkaggs School of Pharmacy and Pharmaceutical Sciences, University of California, San Diego, La Jolla, California, USA
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Jessica L. Metcalf
wDepartment of Animal Science, Colorado State University, Fort Collins, Colorado, USA
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Hosein Mohimani
xDepartment of Computational Biology, Carnegie Mellon University, Pittsburgh, Pennsylvania, USA
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Emmanuel Montassier
rDepartment of Computer Science and Engineering, University of Minnesota, Minneapolis, Minnesota, USA
yUniversité de Nantes, Microbiotas Hosts Antibiotics and Bacterial Resistances (MiHAR), Nantes, France
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Jose Navas-Molina
aDepartment of Pediatrics, University of California San Diego, La Jolla, California, USA
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Tanya T. Nguyen
pDepartments of Psychiatry and Neurosciences, University of California San Diego, La Jolla, California, USA
qSam and Rose Stein Institute for Research on Aging and Center for Healthy Aging, University of California San Diego, La Jolla, California, USA
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Shyamal Peddada
zDepartment of Biostatistics, University of Pittsburgh, Pittsburgh, Pennsylvania, USA
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Pavel Pevzner
bCollaborative Mass Spectrometry Innovation Center, University of California, San Diego, La Jolla, California, USA
dDepartment of Computer Science and Engineering, University of California, San Diego, La Jolla, California, USA
aaCenter for Microbiome Innovation, University of California, San Diego, La Jolla, California, USA
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Katherine S. Pollard
tThe Gladstone Institutes, University of California, San Francisco, California, USA
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Gholamali Rahnavard
mHarvard T. H. Chan School of Public Health, Boston, Massachusetts, USA
nThe Broad Institute of MIT and Harvard, Cambridge, Massachusetts, USA
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Adam Robbins-Pianka
bbDepartment of Computer Science, University of Colorado Boulder, Boulder, Colorado, USA
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Naseer Sangwan
jDepartment of Biosciences, Argonne National Laboratory, Chicago, Illinois, USA
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Joshua Shorenstein
aDepartment of Pediatrics, University of California San Diego, La Jolla, California, USA
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Larry Smarr
dDepartment of Computer Science and Engineering, University of California, San Diego, La Jolla, California, USA
aaCenter for Microbiome Innovation, University of California, San Diego, La Jolla, California, USA
ccCalifornia Institute for Telecommunications and Information Technology (Calit2), University of California San Diego, La Jolla, California, USA
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Se Jin Song
aDepartment of Pediatrics, University of California San Diego, La Jolla, California, USA
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Timothy Spector
oDepartment of Twin Research and Genetic Epidemiology, King’s College London, London, United Kingdom
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Austin D. Swafford
aaCenter for Microbiome Innovation, University of California, San Diego, La Jolla, California, USA
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Varykina G. Thackray
ddDepartment of Obstetrics, Gynecology and Reproductive Sciences, University of California San Diego, La Jolla, California, USA
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Luke R. Thompson
eeOcean Chemistry and Ecosystems Division, Atlantic Oceanographic and Meteorological Laboratory, National Oceanic and Atmospheric Administration, stationed at Southwest Fisheries Science Center, La Jolla, California, USA
ffDepartment of Biological Sciences and Northern Gulf Institute, University of Southern Mississippi, Hattiesburg, Mississippi, USA
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Anupriya Tripathi
aDepartment of Pediatrics, University of California San Diego, La Jolla, California, USA
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Yoshiki Vázquez-Baeza
aDepartment of Pediatrics, University of California San Diego, La Jolla, California, USA
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Alison Vrbanac
aDepartment of Pediatrics, University of California San Diego, La Jolla, California, USA
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Paul Wischmeyer
ggDepartment of Anesthesiology and Surgery, Duke University School of Medicine, Durham, North Carolina, USA
hhDuke Clinical Research Institute, Duke University School of Medicine, Durham, North Carolina, USA
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Elaine Wolfe
aDepartment of Pediatrics, University of California San Diego, La Jolla, California, USA
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Qiyun Zhu
aDepartment of Pediatrics, University of California San Diego, La Jolla, California, USA
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Rob Knight
aDepartment of Pediatrics, University of California San Diego, La Jolla, California, USA
dDepartment of Computer Science and Engineering, University of California, San Diego, La Jolla, California, USA
aaCenter for Microbiome Innovation, University of California, San Diego, La Jolla, California, USA
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Casey S. Greene
University of Pennsylvania
Roles: Editor
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DOI: 10.1128/mSystems.00031-18
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ABSTRACT

Although much work has linked the human microbiome to specific phenotypes and lifestyle variables, data from different projects have been challenging to integrate and the extent of microbial and molecular diversity in human stool remains unknown. Using standardized protocols from the Earth Microbiome Project and sample contributions from over 10,000 citizen-scientists, together with an open research network, we compare human microbiome specimens primarily from the United States, United Kingdom, and Australia to one another and to environmental samples. Our results show an unexpected range of beta-diversity in human stool microbiomes compared to environmental samples; demonstrate the utility of procedures for removing the effects of overgrowth during room-temperature shipping for revealing phenotype correlations; uncover new molecules and kinds of molecular communities in the human stool metabolome; and examine emergent associations among the microbiome, metabolome, and the diversity of plants that are consumed (rather than relying on reductive categorical variables such as veganism, which have little or no explanatory power). We also demonstrate the utility of the living data resource and cross-cohort comparison to confirm existing associations between the microbiome and psychiatric illness and to reveal the extent of microbiome change within one individual during surgery, providing a paradigm for open microbiome research and education.

IMPORTANCE We show that a citizen science, self-selected cohort shipping samples through the mail at room temperature recaptures many known microbiome results from clinically collected cohorts and reveals new ones. Of particular interest is integrating n = 1 study data with the population data, showing that the extent of microbiome change after events such as surgery can exceed differences between distinct environmental biomes, and the effect of diverse plants in the diet, which we confirm with untargeted metabolomics on hundreds of samples.

FOOTNOTES

    • Received March 8, 2018.
    • Accepted April 16, 2018.
  • For a commentary on this article, see https://doi.org/10.1128/mSystems.00060-18.

  • Copyright © 2018 McDonald et al.

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

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American Gut: an Open Platform for Citizen Science Microbiome Research
Daniel McDonald, Embriette Hyde, Justine W. Debelius, James T. Morton, Antonio Gonzalez, Gail Ackermann, Alexander A. Aksenov, Bahar Behsaz, Caitriona Brennan, Yingfeng Chen, Lindsay DeRight Goldasich, Pieter C. Dorrestein, Robert R. Dunn, Ashkaan K. Fahimipour, James Gaffney, Jack A. Gilbert, Grant Gogul, Jessica L. Green, Philip Hugenholtz, Greg Humphrey, Curtis Huttenhower, Matthew A. Jackson, Stefan Janssen, Dilip V. Jeste, Lingjing Jiang, Scott T. Kelley, Dan Knights, Tomasz Kosciolek, Joshua Ladau, Jeff Leach, Clarisse Marotz, Dmitry Meleshko, Alexey V. Melnik, Jessica L. Metcalf, Hosein Mohimani, Emmanuel Montassier, Jose Navas-Molina, Tanya T. Nguyen, Shyamal Peddada, Pavel Pevzner, Katherine S. Pollard, Gholamali Rahnavard, Adam Robbins-Pianka, Naseer Sangwan, Joshua Shorenstein, Larry Smarr, Se Jin Song, Timothy Spector, Austin D. Swafford, Varykina G. Thackray, Luke R. Thompson, Anupriya Tripathi, Yoshiki Vázquez-Baeza, Alison Vrbanac, Paul Wischmeyer, Elaine Wolfe, Qiyun Zhu, The American Gut Consortium, Rob Knight
mSystems May 2018, 3 (3) e00031-18; DOI: 10.1128/mSystems.00031-18

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American Gut: an Open Platform for Citizen Science Microbiome Research
Daniel McDonald, Embriette Hyde, Justine W. Debelius, James T. Morton, Antonio Gonzalez, Gail Ackermann, Alexander A. Aksenov, Bahar Behsaz, Caitriona Brennan, Yingfeng Chen, Lindsay DeRight Goldasich, Pieter C. Dorrestein, Robert R. Dunn, Ashkaan K. Fahimipour, James Gaffney, Jack A. Gilbert, Grant Gogul, Jessica L. Green, Philip Hugenholtz, Greg Humphrey, Curtis Huttenhower, Matthew A. Jackson, Stefan Janssen, Dilip V. Jeste, Lingjing Jiang, Scott T. Kelley, Dan Knights, Tomasz Kosciolek, Joshua Ladau, Jeff Leach, Clarisse Marotz, Dmitry Meleshko, Alexey V. Melnik, Jessica L. Metcalf, Hosein Mohimani, Emmanuel Montassier, Jose Navas-Molina, Tanya T. Nguyen, Shyamal Peddada, Pavel Pevzner, Katherine S. Pollard, Gholamali Rahnavard, Adam Robbins-Pianka, Naseer Sangwan, Joshua Shorenstein, Larry Smarr, Se Jin Song, Timothy Spector, Austin D. Swafford, Varykina G. Thackray, Luke R. Thompson, Anupriya Tripathi, Yoshiki Vázquez-Baeza, Alison Vrbanac, Paul Wischmeyer, Elaine Wolfe, Qiyun Zhu, The American Gut Consortium, Rob Knight
mSystems May 2018, 3 (3) e00031-18; DOI: 10.1128/mSystems.00031-18
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KEYWORDS

citizen science
microbiome

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