Infection trains the host for microbiota-enhanced resistance to pathogens.

Citrobacter rodentium Enterococcus faecalis Klebsiella pneumoniae aerobic respiration bile acid bismuth subsalicylate colonization resistance gut microbiome hydrogen sulfide taurine

Journal

Cell
ISSN: 1097-4172
Titre abrégé: Cell
Pays: United States
ID NLM: 0413066

Informations de publication

Date de publication:
04 02 2021
Historique:
received: 30 04 2020
revised: 19 11 2020
accepted: 08 12 2020
pubmed: 17 1 2021
medline: 25 8 2021
entrez: 16 1 2021
Statut: ppublish

Résumé

The microbiota shields the host against infections in a process known as colonization resistance. How infections themselves shape this fundamental process remains largely unknown. Here, we show that gut microbiota from previously infected hosts display enhanced resistance to infection. This long-term functional remodeling is associated with altered bile acid metabolism leading to the expansion of taxa that utilize the sulfonic acid taurine. Notably, supplying exogenous taurine alone is sufficient to induce this alteration in microbiota function and enhance resistance. Mechanistically, taurine potentiates the microbiota's production of sulfide, an inhibitor of cellular respiration, which is key to host invasion by numerous pathogens. As such, pharmaceutical sequestration of sulfide perturbs the microbiota's composition and promotes pathogen invasion. Together, this work reveals a process by which the host, triggered by infection, can deploy taurine as a nutrient to nourish and train the microbiota, promoting its resistance to subsequent infection.

Identifiants

pubmed: 33453153
pii: S0092-8674(20)31681-0
doi: 10.1016/j.cell.2020.12.011
pmc: PMC8786454
mid: NIHMS1654488
pii:
doi:

Substances chimiques

Sulfides 0
Taurine 1EQV5MLY3D

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

615-627.e17

Subventions

Organisme : Intramural NIH HHS
ID : ZIA DK054508
Pays : United States
Organisme : Intramural NIH HHS
ID : ZIA BC011153
Pays : United States
Organisme : Intramural NIH HHS
ID : ZIA AI001115
Pays : United States
Organisme : NIGMS NIH HHS
ID : FI2 GM128736
Pays : United States
Organisme : Intramural NIH HHS
ID : ZIA HG000180
Pays : United States

Commentaires et corrections

Type : CommentIn
Type : CommentIn
Type : CommentIn
Type : CommentIn
Type : CommentIn

Informations de copyright

Published by Elsevier Inc.

Déclaration de conflit d'intérêts

Declaration of interests NIDDK licensed wildR mice to Taconic Biosciences.

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Auteurs

Apollo Stacy (A)

Metaorganism Immunity Section, Laboratory of Host Immunity and Microbiome, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA; NIAID Microbiome Program, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA; Postdoctoral Research Associate Training Program, National Institute of General Medical Sciences, National Institutes of Health, Bethesda, MD 20892, USA. Electronic address: apollo.stacy@nih.gov.

Vinicius Andrade-Oliveira (V)

Metaorganism Immunity Section, Laboratory of Host Immunity and Microbiome, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

John A McCulloch (JA)

Laboratory of Integrative Cancer Immunology, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Bethesda, MD 20892, USA.

Benedikt Hild (B)

Immunology Section, Liver Diseases Branch, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

Ji Hoon Oh (JH)

Immunology Section, Liver Diseases Branch, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

P Juliana Perez-Chaparro (PJ)

NIAID Microbiome Program, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

Choon K Sim (CK)

Microbial Genomics Section, Translational and Functional Genomics Branch, National Human Genome Research Institute, National Institutes of Health, Bethesda, MD 20892, USA.

Ai Ing Lim (AI)

Metaorganism Immunity Section, Laboratory of Host Immunity and Microbiome, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

Verena M Link (VM)

Metaorganism Immunity Section, Laboratory of Host Immunity and Microbiome, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

Michel Enamorado (M)

Metaorganism Immunity Section, Laboratory of Host Immunity and Microbiome, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

Giorgio Trinchieri (G)

Laboratory of Integrative Cancer Immunology, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Bethesda, MD 20892, USA.

Julia A Segre (JA)

Microbial Genomics Section, Translational and Functional Genomics Branch, National Human Genome Research Institute, National Institutes of Health, Bethesda, MD 20892, USA.

Barbara Rehermann (B)

Immunology Section, Liver Diseases Branch, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

Yasmine Belkaid (Y)

Metaorganism Immunity Section, Laboratory of Host Immunity and Microbiome, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA; NIAID Microbiome Program, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA. Electronic address: ybelkaid@niaid.nih.gov.

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Classifications MeSH