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Title: American Gut: an Open Platform for Citizen Science Microbiome Research

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 microbiomemore » research and education. 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.« less

Authors:
ORCiD logo; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; more »; ; ; ORCiD logo; ; ; ORCiD logo; ; ; ; ; ; ; ; ; ; ORCiD logo; ; ; ; ; ; ORCiD logo; ; ; ; ; ORCiD logo; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; « less
Publication Date:
Research Org.:
Argonne National Lab. (ANL), Argonne, IL (United States); Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Sponsoring Org.:
National Science Foundation (NSF); USDOE Office of Science (SC)
Contributing Org.:
American Gut Project (AGP)
OSTI Identifier:
1493907
Alternate Identifier(s):
OSTI ID: 1504427
Report Number(s):
PNNL-SA-113423
Journal ID: ISSN 2379-5077; 148306
Grant/Contract Number:  
AC02-06CH11357; AC05-76RL01830
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
mSystems
Additional Journal Information:
Journal Volume: 3; Journal Issue: 3; Journal ID: ISSN 2379-5077
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; citizen science; microbiome

Citation Formats

McDonald, Daniel, Hyde, Embriette, Debelius, Justine W., Morton, James T., Gonzalez, Antonio, Ackermann, Gail, Aksenov, Alexander A., Behsaz, Bahar, Brennan, Caitriona, Chen, Yingfeng, DeRight Goldasich, Lindsay, Dorrestein, Pieter C., Dunn, Robert R., Fahimipour, Ashkaan K., Gaffney, James, Gilbert, Jack A., Gogul, Grant, Green, Jessica L., Hugenholtz, Philip, Humphrey, Greg, Huttenhower, Curtis, Jackson, Matthew A., Janssen, Stefan, Jeste, Dilip V., Jiang, Lingjing, Kelley, Scott T., Knights, Dan, Kosciolek, Tomasz, Ladau, Joshua, Leach, Jeff, Marotz, Clarisse, Meleshko, Dmitry, Melnik, Alexey V., Metcalf, Jessica L., Mohimani, Hosein, Montassier, Emmanuel, Navas-Molina, Jose, Nguyen, Tanya T., Peddada, Shyamal, Pevzner, Pavel, Pollard, Katherine S., Rahnavard, Gholamali, Robbins-Pianka, Adam, Sangwan, Naseer, Shorenstein, Joshua, Smarr, Larry, Song, Se Jin, Spector, Timothy, Swafford, Austin D., Thackray, Varykina G., Thompson, Luke R., Tripathi, Anupriya, Vázquez-Baeza, Yoshiki, Vrbanac, Alison, Wischmeyer, Paul, Wolfe, Elaine, Zhu, Qiyun, Knight, Rob, Greene, Casey S., Mann, Allison E., Amir, Amnon, Frazier, Angel, Martino, Cameron, Lebrilla, Carlito, Lozupone, Catherine, Lewis, Cecil M., Raison, Charles, Zhang, Chi, Lauber, Christian L., Warinner, Christina, Lowry, Christopher A., Callewaert, Chris, Bloss, Cinnamon, Willner, Dana, Galzerani, Daniela Domingos, Gonzalez, David J., Mills, David A., Chopra, Deepak, Gevers, Dirk, Berg-Lyons, Donna, Sears, Dorothy D., Wendel, Doug, Lovelace, Elijah, Pierce, Emily, TerAvest, Emily, Bolyen, Evan, Bushman, Frederic D., Wu, Gary D., Church, George M., Saxe, Gordon, Holscher, Hanna D., Ugrina, Ivo, German, J. Bruce, Caporaso, J. Gregory, Wozniak, Jacob M., Kerr, Jacqueline, Ravel, Jacques, Lewis, James D., Suchodolski, Jan S., Jansson, Janet K., Hampton-Marcell, Jarrad T., Bobe, Jason, Raes, Jeroen, Chase, John H., Eisen, Jonathan A., Monk, Jonathan, Clemente, Jose C., Petrosino, Joseph, Goodrich, Julia, Gauglitz, Julia, Jacobs, Julian, Zengler, Karsten, Swanson, Kelly S., Lewis, Kim, Mayer, Kris, Bittinger, Kyle, Dillon, Lindsay, Zaramela, Livia S., Schriml, Lynn M., Dominguez-Bello, Maria G., Jankowska, Marta M., Blaser, Martin, Pirrung, Meg, Minson, Michael, Kurisu, Mike, Ajami, Nadim, Gottel, Neil R., Chia, Nicholas, Fierer, Noah, White, Owen, Cani, Patrice D., Gajer, Pawel, Strandwitz, Philip, Kashyap, Purna, Dutton, Rachel, Park, Rachel S., Xavier, Ramnik J., Mills, Robert H., Krajmalnik-Brown, Rosa, Ley, Ruth, Owens, Sarah M., Klemmer, Scott, Matamoros, Sébastien, Mirarab, Siavash, Moorman, Stephanie, Holmes, Susan, Schwartz, Tara, Eshoo-Anton, Tifani W., Vigers, Tim, Pandey, Vineet, Treuren, Will Van, Fang, Xin, Zech Xu, Zhenjiang, Jarmusch, Alan, Geier, Justin, Reeve, Nicolai, Silva, Ricardo, Kopylova, Evguenia, Nguyen, Dominic, Sanders, Karenina, Salido Benitez, Rodolfo Antonio, Heale, Arthur Cole, Abramson, Max, Waldispühl, Jérôme, Butyaev, Alexander, Drogaris, Chris, Nazarova, Elena, Ball, Madeleine, and Gunderson, Beau. American Gut: an Open Platform for Citizen Science Microbiome Research. United States: N. p., 2018. Web. doi:10.1128/mSystems.00031-18.
McDonald, Daniel, Hyde, Embriette, Debelius, Justine W., Morton, James T., Gonzalez, Antonio, Ackermann, Gail, Aksenov, Alexander A., Behsaz, Bahar, Brennan, Caitriona, Chen, Yingfeng, DeRight Goldasich, Lindsay, Dorrestein, Pieter C., Dunn, Robert R., Fahimipour, Ashkaan K., Gaffney, James, Gilbert, Jack A., Gogul, Grant, Green, Jessica L., Hugenholtz, Philip, Humphrey, Greg, Huttenhower, Curtis, Jackson, Matthew A., Janssen, Stefan, Jeste, Dilip V., Jiang, Lingjing, Kelley, Scott T., Knights, Dan, Kosciolek, Tomasz, Ladau, Joshua, Leach, Jeff, Marotz, Clarisse, Meleshko, Dmitry, Melnik, Alexey V., Metcalf, Jessica L., Mohimani, Hosein, Montassier, Emmanuel, Navas-Molina, Jose, Nguyen, Tanya T., Peddada, Shyamal, Pevzner, Pavel, Pollard, Katherine S., Rahnavard, Gholamali, Robbins-Pianka, Adam, Sangwan, Naseer, Shorenstein, Joshua, Smarr, Larry, Song, Se Jin, Spector, Timothy, Swafford, Austin D., Thackray, Varykina G., Thompson, Luke R., Tripathi, Anupriya, Vázquez-Baeza, Yoshiki, Vrbanac, Alison, Wischmeyer, Paul, Wolfe, Elaine, Zhu, Qiyun, Knight, Rob, Greene, Casey S., Mann, Allison E., Amir, Amnon, Frazier, Angel, Martino, Cameron, Lebrilla, Carlito, Lozupone, Catherine, Lewis, Cecil M., Raison, Charles, Zhang, Chi, Lauber, Christian L., Warinner, Christina, Lowry, Christopher A., Callewaert, Chris, Bloss, Cinnamon, Willner, Dana, Galzerani, Daniela Domingos, Gonzalez, David J., Mills, David A., Chopra, Deepak, Gevers, Dirk, Berg-Lyons, Donna, Sears, Dorothy D., Wendel, Doug, Lovelace, Elijah, Pierce, Emily, TerAvest, Emily, Bolyen, Evan, Bushman, Frederic D., Wu, Gary D., Church, George M., Saxe, Gordon, Holscher, Hanna D., Ugrina, Ivo, German, J. Bruce, Caporaso, J. Gregory, Wozniak, Jacob M., Kerr, Jacqueline, Ravel, Jacques, Lewis, James D., Suchodolski, Jan S., Jansson, Janet K., Hampton-Marcell, Jarrad T., Bobe, Jason, Raes, Jeroen, Chase, John H., Eisen, Jonathan A., Monk, Jonathan, Clemente, Jose C., Petrosino, Joseph, Goodrich, Julia, Gauglitz, Julia, Jacobs, Julian, Zengler, Karsten, Swanson, Kelly S., Lewis, Kim, Mayer, Kris, Bittinger, Kyle, Dillon, Lindsay, Zaramela, Livia S., Schriml, Lynn M., Dominguez-Bello, Maria G., Jankowska, Marta M., Blaser, Martin, Pirrung, Meg, Minson, Michael, Kurisu, Mike, Ajami, Nadim, Gottel, Neil R., Chia, Nicholas, Fierer, Noah, White, Owen, Cani, Patrice D., Gajer, Pawel, Strandwitz, Philip, Kashyap, Purna, Dutton, Rachel, Park, Rachel S., Xavier, Ramnik J., Mills, Robert H., Krajmalnik-Brown, Rosa, Ley, Ruth, Owens, Sarah M., Klemmer, Scott, Matamoros, Sébastien, Mirarab, Siavash, Moorman, Stephanie, Holmes, Susan, Schwartz, Tara, Eshoo-Anton, Tifani W., Vigers, Tim, Pandey, Vineet, Treuren, Will Van, Fang, Xin, Zech Xu, Zhenjiang, Jarmusch, Alan, Geier, Justin, Reeve, Nicolai, Silva, Ricardo, Kopylova, Evguenia, Nguyen, Dominic, Sanders, Karenina, Salido Benitez, Rodolfo Antonio, Heale, Arthur Cole, Abramson, Max, Waldispühl, Jérôme, Butyaev, Alexander, Drogaris, Chris, Nazarova, Elena, Ball, Madeleine, & Gunderson, Beau. American Gut: an Open Platform for Citizen Science Microbiome Research. United States. doi:10.1128/mSystems.00031-18.
McDonald, Daniel, Hyde, Embriette, Debelius, Justine W., Morton, James T., Gonzalez, Antonio, Ackermann, Gail, Aksenov, Alexander A., Behsaz, Bahar, Brennan, Caitriona, Chen, Yingfeng, DeRight Goldasich, Lindsay, Dorrestein, Pieter C., Dunn, Robert R., Fahimipour, Ashkaan K., Gaffney, James, Gilbert, Jack A., Gogul, Grant, Green, Jessica L., Hugenholtz, Philip, Humphrey, Greg, Huttenhower, Curtis, Jackson, Matthew A., Janssen, Stefan, Jeste, Dilip V., Jiang, Lingjing, Kelley, Scott T., Knights, Dan, Kosciolek, Tomasz, Ladau, Joshua, Leach, Jeff, Marotz, Clarisse, Meleshko, Dmitry, Melnik, Alexey V., Metcalf, Jessica L., Mohimani, Hosein, Montassier, Emmanuel, Navas-Molina, Jose, Nguyen, Tanya T., Peddada, Shyamal, Pevzner, Pavel, Pollard, Katherine S., Rahnavard, Gholamali, Robbins-Pianka, Adam, Sangwan, Naseer, Shorenstein, Joshua, Smarr, Larry, Song, Se Jin, Spector, Timothy, Swafford, Austin D., Thackray, Varykina G., Thompson, Luke R., Tripathi, Anupriya, Vázquez-Baeza, Yoshiki, Vrbanac, Alison, Wischmeyer, Paul, Wolfe, Elaine, Zhu, Qiyun, Knight, Rob, Greene, Casey S., Mann, Allison E., Amir, Amnon, Frazier, Angel, Martino, Cameron, Lebrilla, Carlito, Lozupone, Catherine, Lewis, Cecil M., Raison, Charles, Zhang, Chi, Lauber, Christian L., Warinner, Christina, Lowry, Christopher A., Callewaert, Chris, Bloss, Cinnamon, Willner, Dana, Galzerani, Daniela Domingos, Gonzalez, David J., Mills, David A., Chopra, Deepak, Gevers, Dirk, Berg-Lyons, Donna, Sears, Dorothy D., Wendel, Doug, Lovelace, Elijah, Pierce, Emily, TerAvest, Emily, Bolyen, Evan, Bushman, Frederic D., Wu, Gary D., Church, George M., Saxe, Gordon, Holscher, Hanna D., Ugrina, Ivo, German, J. Bruce, Caporaso, J. Gregory, Wozniak, Jacob M., Kerr, Jacqueline, Ravel, Jacques, Lewis, James D., Suchodolski, Jan S., Jansson, Janet K., Hampton-Marcell, Jarrad T., Bobe, Jason, Raes, Jeroen, Chase, John H., Eisen, Jonathan A., Monk, Jonathan, Clemente, Jose C., Petrosino, Joseph, Goodrich, Julia, Gauglitz, Julia, Jacobs, Julian, Zengler, Karsten, Swanson, Kelly S., Lewis, Kim, Mayer, Kris, Bittinger, Kyle, Dillon, Lindsay, Zaramela, Livia S., Schriml, Lynn M., Dominguez-Bello, Maria G., Jankowska, Marta M., Blaser, Martin, Pirrung, Meg, Minson, Michael, Kurisu, Mike, Ajami, Nadim, Gottel, Neil R., Chia, Nicholas, Fierer, Noah, White, Owen, Cani, Patrice D., Gajer, Pawel, Strandwitz, Philip, Kashyap, Purna, Dutton, Rachel, Park, Rachel S., Xavier, Ramnik J., Mills, Robert H., Krajmalnik-Brown, Rosa, Ley, Ruth, Owens, Sarah M., Klemmer, Scott, Matamoros, Sébastien, Mirarab, Siavash, Moorman, Stephanie, Holmes, Susan, Schwartz, Tara, Eshoo-Anton, Tifani W., Vigers, Tim, Pandey, Vineet, Treuren, Will Van, Fang, Xin, Zech Xu, Zhenjiang, Jarmusch, Alan, Geier, Justin, Reeve, Nicolai, Silva, Ricardo, Kopylova, Evguenia, Nguyen, Dominic, Sanders, Karenina, Salido Benitez, Rodolfo Antonio, Heale, Arthur Cole, Abramson, Max, Waldispühl, Jérôme, Butyaev, Alexander, Drogaris, Chris, Nazarova, Elena, Ball, Madeleine, and Gunderson, Beau. Tue . "American Gut: an Open Platform for Citizen Science Microbiome Research". United States. doi:10.1128/mSystems.00031-18. https://www.osti.gov/servlets/purl/1493907.
@article{osti_1493907,
title = {American Gut: an Open Platform for Citizen Science Microbiome Research},
author = {McDonald, Daniel and Hyde, Embriette and Debelius, Justine W. and Morton, James T. and Gonzalez, Antonio and Ackermann, Gail and Aksenov, Alexander A. and Behsaz, Bahar and Brennan, Caitriona and Chen, Yingfeng and DeRight Goldasich, Lindsay and Dorrestein, Pieter C. and Dunn, Robert R. and Fahimipour, Ashkaan K. and Gaffney, James and Gilbert, Jack A. and Gogul, Grant and Green, Jessica L. and Hugenholtz, Philip and Humphrey, Greg and Huttenhower, Curtis and Jackson, Matthew A. and Janssen, Stefan and Jeste, Dilip V. and Jiang, Lingjing and Kelley, Scott T. and Knights, Dan and Kosciolek, Tomasz and Ladau, Joshua and Leach, Jeff and Marotz, Clarisse and Meleshko, Dmitry and Melnik, Alexey V. and Metcalf, Jessica L. and Mohimani, Hosein and Montassier, Emmanuel and Navas-Molina, Jose and Nguyen, Tanya T. and Peddada, Shyamal and Pevzner, Pavel and Pollard, Katherine S. and Rahnavard, Gholamali and Robbins-Pianka, Adam and Sangwan, Naseer and Shorenstein, Joshua and Smarr, Larry and Song, Se Jin and Spector, Timothy and Swafford, Austin D. and Thackray, Varykina G. and Thompson, Luke R. and Tripathi, Anupriya and Vázquez-Baeza, Yoshiki and Vrbanac, Alison and Wischmeyer, Paul and Wolfe, Elaine and Zhu, Qiyun and Knight, Rob and Greene, Casey S. and Mann, Allison E. and Amir, Amnon and Frazier, Angel and Martino, Cameron and Lebrilla, Carlito and Lozupone, Catherine and Lewis, Cecil M. and Raison, Charles and Zhang, Chi and Lauber, Christian L. and Warinner, Christina and Lowry, Christopher A. and Callewaert, Chris and Bloss, Cinnamon and Willner, Dana and Galzerani, Daniela Domingos and Gonzalez, David J. and Mills, David A. and Chopra, Deepak and Gevers, Dirk and Berg-Lyons, Donna and Sears, Dorothy D. and Wendel, Doug and Lovelace, Elijah and Pierce, Emily and TerAvest, Emily and Bolyen, Evan and Bushman, Frederic D. and Wu, Gary D. and Church, George M. and Saxe, Gordon and Holscher, Hanna D. and Ugrina, Ivo and German, J. Bruce and Caporaso, J. Gregory and Wozniak, Jacob M. and Kerr, Jacqueline and Ravel, Jacques and Lewis, James D. and Suchodolski, Jan S. and Jansson, Janet K. and Hampton-Marcell, Jarrad T. and Bobe, Jason and Raes, Jeroen and Chase, John H. and Eisen, Jonathan A. and Monk, Jonathan and Clemente, Jose C. and Petrosino, Joseph and Goodrich, Julia and Gauglitz, Julia and Jacobs, Julian and Zengler, Karsten and Swanson, Kelly S. and Lewis, Kim and Mayer, Kris and Bittinger, Kyle and Dillon, Lindsay and Zaramela, Livia S. and Schriml, Lynn M. and Dominguez-Bello, Maria G. and Jankowska, Marta M. and Blaser, Martin and Pirrung, Meg and Minson, Michael and Kurisu, Mike and Ajami, Nadim and Gottel, Neil R. and Chia, Nicholas and Fierer, Noah and White, Owen and Cani, Patrice D. and Gajer, Pawel and Strandwitz, Philip and Kashyap, Purna and Dutton, Rachel and Park, Rachel S. and Xavier, Ramnik J. and Mills, Robert H. and Krajmalnik-Brown, Rosa and Ley, Ruth and Owens, Sarah M. and Klemmer, Scott and Matamoros, Sébastien and Mirarab, Siavash and Moorman, Stephanie and Holmes, Susan and Schwartz, Tara and Eshoo-Anton, Tifani W. and Vigers, Tim and Pandey, Vineet and Treuren, Will Van and Fang, Xin and Zech Xu, Zhenjiang and Jarmusch, Alan and Geier, Justin and Reeve, Nicolai and Silva, Ricardo and Kopylova, Evguenia and Nguyen, Dominic and Sanders, Karenina and Salido Benitez, Rodolfo Antonio and Heale, Arthur Cole and Abramson, Max and Waldispühl, Jérôme and Butyaev, Alexander and Drogaris, Chris and Nazarova, Elena and Ball, Madeleine and Gunderson, Beau},
abstractNote = {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. 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.},
doi = {10.1128/mSystems.00031-18},
journal = {mSystems},
issn = {2379-5077},
number = 3,
volume = 3,
place = {United States},
year = {2018},
month = {5}
}

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Figures / Tables:

FIG 1 FIG 1: Population characteristics. (A) Participants across the world have sent in samples to American Gut, although the primary geographic regions of participation are in North America and the United Kingdom; the report that a participant receives is depicted. (B) The primary sample breakdown for subsequent analyses. Red denotes themore » reasons that samples were removed. (C) Between the two largest populations, the United States (n = 6,634) and the United Kingdom (n = 2,071), we observe a significant difference in alpha-diversity. (D) In a meta-analysis, the largely industrialized population that makes up American Gut exhibits significant differential abundances compared to nonindustrialized populations.« less

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