Dynamic genetic adaptation of Bacteroides thetaiotaomicron during murine gut colonization.

Bacteroides thetaiotaomicron BarSeq CP: Microbiology IS elements commensal bacteria gut colonization insertion sequence microbial adaptation microbial metabolism microbiome-based therapy

Journal

Cell reports
ISSN: 2211-1247
Titre abrégé: Cell Rep
Pays: United States
ID NLM: 101573691

Informations de publication

Date de publication:
29 08 2023
Historique:
received: 08 05 2022
revised: 17 05 2023
accepted: 03 08 2023
medline: 4 9 2023
pubmed: 20 8 2023
entrez: 20 8 2023
Statut: ppublish

Résumé

To understand how a bacterium ultimately succeeds or fails in adapting to a new host, it is essential to assess the temporal dynamics of its fitness over the course of colonization. Here, we introduce a human-derived commensal organism, Bacteroides thetaiotaomicron (Bt), into the guts of germ-free mice to determine whether and how the genetic requirements for colonization shift over time. Combining a high-throughput functional genetics assay and transcriptomics, we find that gene usage changes drastically during the first days of colonization, shifting from high expression of amino acid biosynthesis genes to broad upregulation of diverse polysaccharide utilization loci. Within the first week, metabolism becomes centered around utilization of a predominant dietary oligosaccharide, and these changes are largely sustained through 6 weeks of colonization. Spontaneous mutations in wild-type Bt also evolve around this locus. These findings highlight the importance of considering temporal colonization dynamics in developing more effective microbiome-based therapies.

Identifiants

pubmed: 37598339
pii: S2211-1247(23)01020-3
doi: 10.1016/j.celrep.2023.113009
pmc: PMC10528517
mid: NIHMS1928301
pii:
doi:

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

113009

Subventions

Organisme : NIDDK NIH HHS
ID : P30 DK042086
Pays : United States
Organisme : NIDDK NIH HHS
ID : RC2 DK122394
Pays : United States
Organisme : NIDDK NIH HHS
ID : T32 DK007074
Pays : United States
Organisme : NIGMS NIH HHS
ID : T32 GM150375
Pays : United States

Informations de copyright

Copyright © 2023 The Authors. Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests The authors declare no competing interests.

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Auteurs

Megan S Kennedy (MS)

Medical Scientist Training Program, Pritzker School of Medicine, The University of Chicago, Chicago, IL, USA; Department of Ecology & Evolution, The University of Chicago, Chicago, IL, USA.

Manjing Zhang (M)

Committee on Microbiology, The University of Chicago, Chicago, IL, USA.

Orlando DeLeon (O)

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

Jacie Bissell (J)

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

Florian Trigodet (F)

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

Karen Lolans (K)

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

Sara Temelkova (S)

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

Katherine T Carroll (KT)

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

Aretha Fiebig (A)

Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, MI, USA.

Adam Deutschbauer (A)

Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA; Department of Plant and Microbial Biology, University of California, Berkeley, Berkeley, CA, USA.

Ashley M Sidebottom (AM)

Duchossois Family Institute, Department of Biomedical Sciences, The University of Chicago, Chicago, IL, USA.

Joash Lake (J)

Committee on Immunology, The University of Chicago, Chicago, IL, USA.

Chris Henry (C)

Mathematics and Computer Science Division, Argonne National Laboratory, Lemont, IL, USA.

Phoebe A Rice (PA)

Department of Biochemistry & Molecular Biology, The University of Chicago, Chicago, IL, USA.

Joy Bergelson (J)

Committee on Microbiology, The University of Chicago, Chicago, IL, USA.

Eugene B Chang (EB)

Department of Medicine, The University of Chicago, Chicago, IL, USA. Electronic address: echang@medicine.bsd.uchicago.edu.

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Classifications MeSH