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Metabolic independence drives gut microbial colonization and resilience in health and disease

View ORCID ProfileAndrea R. Watson, View ORCID ProfileJessika Füssel, Iva Veseli, Johanna Zaal DeLongchamp, Marisela Silva, Florian Trigodet, Karen Lolans, Alon Shaiber, Emily Fogarty, Joseph M. Runde, Christopher Quince, Michael K. Yu, Arda Söylev, Hilary G. Morrison, Sonny T.M. Lee, Dina Kao, David T. Rubin, Bana Jabri, Thomas Louie, View ORCID ProfileA. Murat Eren
doi: https://doi.org/10.1101/2021.03.02.433653
Andrea R. Watson
1Department of Medicine, The University of Chicago, Chicago, IL 60637, USA
2Committee on Microbiology, The University of Chicago, Chicago, IL 60637, USA
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  • ORCID record for Andrea R. Watson
Jessika Füssel
1Department of Medicine, The University of Chicago, Chicago, IL 60637, USA
3Institute for Chemistry and Biology of the Marine Environment, University of Oldenburg, 26129 Oldenburg, Germany
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Iva Veseli
4Biophysical Sciences Program, The University of Chicago, Chicago, IL 60637, USA
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Johanna Zaal DeLongchamp
5Department of Medicine, The University of Calgary, Calgary, AB T2N 1N4, Canada
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Marisela Silva
5Department of Medicine, The University of Calgary, Calgary, AB T2N 1N4, Canada
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Florian Trigodet
1Department of Medicine, The University of Chicago, Chicago, IL 60637, USA
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Karen Lolans
1Department of Medicine, The University of Chicago, Chicago, IL 60637, USA
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Alon Shaiber
4Biophysical Sciences Program, The University of Chicago, Chicago, IL 60637, USA
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Emily Fogarty
1Department of Medicine, The University of Chicago, Chicago, IL 60637, USA
2Committee on Microbiology, The University of Chicago, Chicago, IL 60637, USA
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Joseph M. Runde
6Department of Pediatrics, Lurie Children’s Hospital of Chicago, Chicago, IL 60611, USA
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Christopher Quince
7Organisms and Ecosystems, Earlham Institute, Norwich, Norwich, NR4 7UZ, United Kingdom
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Michael K. Yu
8Toyota Technological Institute at Chicago, Chicago, IL 60637, USA
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Arda Söylev
9Department of Computer Engineering, Konya Food and Agriculture University, Konya, Turkey
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Hilary G. Morrison
10Josephine Bay Paul Center, Marine Biological Laboratory, Woods Hole, MA 02543, USA
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Sonny T.M. Lee
1Department of Medicine, The University of Chicago, Chicago, IL 60637, USA
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Dina Kao
11Department of Medicine, University of Alberta, Edmonton, AB T6G 2G3, Canada
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David T. Rubin
1Department of Medicine, The University of Chicago, Chicago, IL 60637, USA
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Bana Jabri
1Department of Medicine, The University of Chicago, Chicago, IL 60637, USA
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Thomas Louie
5Department of Medicine, The University of Calgary, Calgary, AB T2N 1N4, Canada
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A. Murat Eren
1Department of Medicine, The University of Chicago, Chicago, IL 60637, USA
2Committee on Microbiology, The University of Chicago, Chicago, IL 60637, USA
3Institute for Chemistry and Biology of the Marine Environment, University of Oldenburg, 26129 Oldenburg, Germany
10Josephine Bay Paul Center, Marine Biological Laboratory, Woods Hole, MA 02543, USA
12Helmholtz Institute for Functional Marine Biodiversity, 26129 Oldenburg, Germany
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  • ORCID record for A. Murat Eren
  • For correspondence: meren@hifmb.de
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Abstract

Changes in microbial community composition as a function of human health and disease states have sparked remarkable interest in the human gut microbiome. However, establishing reproducible insights into the determinants of microbial succession in disease has been a formidable challenge. Here we use fecal microbiota transplantation (FMT) as an in natura experimental model to investigate the association between metabolic independence and resilience in stressed gut environments. Our genome-resolved metagenomics survey suggests that FMT serves as an environmental filter that favors populations with higher metabolic independence, the genomes of which encode complete metabolic modules to synthesize critical metabolites, including amino acids, nucleotides, and vitamins. Interestingly, we observe higher completion of the same biosynthetic pathways in microbes enriched in IBD patients. These observations suggest a general mechanism that underlies changes in diversity in perturbed gut environments, and reveal taxon-independent markers of ‘dysbiosis’ that may explain why widespread yet typically low abundance members of healthy gut microbiomes can dominate under inflammatory conditions without any causal association with disease.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • Shortened the manuscript by removing a section, and streamlined some of the analyses for better contextualization of concepts observed.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-ND 4.0 International license.
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Posted August 23, 2022.
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Metabolic independence drives gut microbial colonization and resilience in health and disease
Andrea R. Watson, Jessika Füssel, Iva Veseli, Johanna Zaal DeLongchamp, Marisela Silva, Florian Trigodet, Karen Lolans, Alon Shaiber, Emily Fogarty, Joseph M. Runde, Christopher Quince, Michael K. Yu, Arda Söylev, Hilary G. Morrison, Sonny T.M. Lee, Dina Kao, David T. Rubin, Bana Jabri, Thomas Louie, A. Murat Eren
bioRxiv 2021.03.02.433653; doi: https://doi.org/10.1101/2021.03.02.433653
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Metabolic independence drives gut microbial colonization and resilience in health and disease
Andrea R. Watson, Jessika Füssel, Iva Veseli, Johanna Zaal DeLongchamp, Marisela Silva, Florian Trigodet, Karen Lolans, Alon Shaiber, Emily Fogarty, Joseph M. Runde, Christopher Quince, Michael K. Yu, Arda Söylev, Hilary G. Morrison, Sonny T.M. Lee, Dina Kao, David T. Rubin, Bana Jabri, Thomas Louie, A. Murat Eren
bioRxiv 2021.03.02.433653; doi: https://doi.org/10.1101/2021.03.02.433653

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