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

Fecal microbiota transplantation Human gut microbiome Metabolic independence Microbial colonization Microbial metabolism

Journal

Genome biology
ISSN: 1474-760X
Titre abrégé: Genome Biol
Pays: England
ID NLM: 100960660

Informations de publication

Date de publication:
17 04 2023
Historique:
received: 03 07 2022
accepted: 07 04 2023
medline: 19 4 2023
entrez: 18 4 2023
pubmed: 19 4 2023
Statut: epublish

Résumé

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.

Sections du résumé

BACKGROUND
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.
RESULTS
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.
CONCLUSIONS
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.

Identifiants

pubmed: 37069665
doi: 10.1186/s13059-023-02924-x
pii: 10.1186/s13059-023-02924-x
pmc: PMC10108530
doi:

Substances chimiques

Amino Acids 0

Types de publication

Journal Article Research Support, U.S. Gov't, Non-P.H.S. Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

78

Subventions

Organisme : NIDDK NIH HHS
ID : P30 DK042086
Pays : United States
Organisme : NCI NIH HHS
ID : P30 CA014599
Pays : United States
Organisme : NIDDK NIH HHS
ID : RC2 DK122394
Pays : United States

Informations de copyright

© 2023. The Author(s).

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Auteurs

Andrea R Watson (AR)

Department of Medicine, The University of Chicago, Chicago, IL, 60637, USA.
Committee On Microbiology, The University of Chicago, Chicago, IL, 60637, USA.

Jessika Füssel (J)

Department of Medicine, The University of Chicago, Chicago, IL, 60637, USA.
Institute for Chemistry and Biology of the Marine Environment, University of Oldenburg, 26129, Oldenburg, Germany.

Iva Veseli (I)

Biophysical Sciences Program, The University of Chicago, Chicago, IL, 60637, USA.

Johanna Zaal DeLongchamp (JZ)

Department of Medicine, The University of Calgary, Calgary, AB, T2N 1N4, Canada.

Marisela Silva (M)

Department of Medicine, The University of Calgary, Calgary, AB, T2N 1N4, Canada.

Florian Trigodet (F)

Department of Medicine, The University of Chicago, Chicago, IL, 60637, USA.

Karen Lolans (K)

Department of Medicine, The University of Chicago, Chicago, IL, 60637, USA.

Alon Shaiber (A)

Biophysical Sciences Program, The University of Chicago, Chicago, IL, 60637, USA.

Emily Fogarty (E)

Department of Medicine, The University of Chicago, Chicago, IL, 60637, USA.
Committee On Microbiology, The University of Chicago, Chicago, IL, 60637, USA.

Joseph M Runde (JM)

Department of Pediatrics, Lurie Children's Hospital of Chicago, Chicago, IL, 60611, USA.

Christopher Quince (C)

Organisms and Ecosystems, Earlham Institute, Norwich, Norwich, NR4 7UZ, UK.
Gut Microbes and Health, Quadram Institute, Norwich, NR4 7UQ, UK.

Michael K Yu (MK)

Toyota Technological Institute at Chicago, Chicago, IL, 60637, USA.

Arda Söylev (A)

Department of Computer Engineering, Konya Food and Agriculture University, Konya, Turkey.

Hilary G Morrison (HG)

Marine Biological Laboratory, Josephine Bay Paul Center, Woods Hole, Falmouth, MA, 02543, USA.

Sonny T M Lee (STM)

Department of Medicine, The University of Chicago, Chicago, IL, 60637, USA.

Dina Kao (D)

Department of Medicine, University of Alberta, Edmonton, AB, T6G 2G3, Canada.

David T Rubin (DT)

Department of Medicine, The University of Chicago, Chicago, IL, 60637, USA.

Bana Jabri (B)

Department of Medicine, The University of Chicago, Chicago, IL, 60637, USA.

Thomas Louie (T)

Department of Medicine, The University of Calgary, Calgary, AB, T2N 1N4, Canada.

A Murat Eren (AM)

Department of Medicine, The University of Chicago, Chicago, IL, 60637, USA. meren@hifmb.de.
Committee On Microbiology, The University of Chicago, Chicago, IL, 60637, USA. meren@hifmb.de.
Institute for Chemistry and Biology of the Marine Environment, University of Oldenburg, 26129, Oldenburg, Germany. meren@hifmb.de.
Marine Biological Laboratory, Josephine Bay Paul Center, Woods Hole, Falmouth, MA, 02543, USA. meren@hifmb.de.
Helmholtz Institute for Functional Marine Biodiversity, 26129, Oldenburg, Germany. meren@hifmb.de.

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