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A single respiratory tract infection early in life reroutes healthy microbiome development and affects adult metabolism in a preclinical animal model

In adult animals, acute viral infections only temporarily alter the composition of both respiratory and intestinal commensal microbiota, potentially due to the intrinsic stability of this microbial ecosystem. In stark contrast, commensal bacterial communities are rather vulnerable to perturbation in...

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Autores principales: Yildiz, Soner, Mazel-Sanchez, Beryl, Bonifacio, Joao P. P., Schmolke, Mirco
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9250495/
https://www.ncbi.nlm.nih.gov/pubmed/35780244
http://dx.doi.org/10.1038/s41522-022-00315-x
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author Yildiz, Soner
Mazel-Sanchez, Beryl
Bonifacio, Joao P. P.
Schmolke, Mirco
author_facet Yildiz, Soner
Mazel-Sanchez, Beryl
Bonifacio, Joao P. P.
Schmolke, Mirco
author_sort Yildiz, Soner
collection PubMed
description In adult animals, acute viral infections only temporarily alter the composition of both respiratory and intestinal commensal microbiota, potentially due to the intrinsic stability of this microbial ecosystem. In stark contrast, commensal bacterial communities are rather vulnerable to perturbation in infancy. Animal models proved that disruption of a balanced microbiota development e.g., by antibiotics treatment early in life, increases the probability for metabolic disorders in adults. Importantly, infancy is also a phase in life with high incidence of acute infections. We postulated that acute viral infections in early life might pose a similarly severe perturbation and permanently shape microbiota composition with long-term physiological consequences for the adult host. As a proof of concept, we infected infant mice with a sub-lethal dose of influenza A virus. We determined microbiota composition up to early adulthood (63 days) from small intestine by 16S rRNA gene-specific next-generation sequencing. Infected mice underwent long-lasting changes in microbiota composition, associated with increase in fat mass. High-fat-high-glucose diet promoted this effect while co-housing with mock-treated animals overwrote the weight gain. Our data suggest that in the critical phase of infancy even a single silent viral infection could cast a long shadow and cause long-term microbiota perturbations, affecting adult host physiology.
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spelling pubmed-92504952022-07-04 A single respiratory tract infection early in life reroutes healthy microbiome development and affects adult metabolism in a preclinical animal model Yildiz, Soner Mazel-Sanchez, Beryl Bonifacio, Joao P. P. Schmolke, Mirco NPJ Biofilms Microbiomes Brief Communication In adult animals, acute viral infections only temporarily alter the composition of both respiratory and intestinal commensal microbiota, potentially due to the intrinsic stability of this microbial ecosystem. In stark contrast, commensal bacterial communities are rather vulnerable to perturbation in infancy. Animal models proved that disruption of a balanced microbiota development e.g., by antibiotics treatment early in life, increases the probability for metabolic disorders in adults. Importantly, infancy is also a phase in life with high incidence of acute infections. We postulated that acute viral infections in early life might pose a similarly severe perturbation and permanently shape microbiota composition with long-term physiological consequences for the adult host. As a proof of concept, we infected infant mice with a sub-lethal dose of influenza A virus. We determined microbiota composition up to early adulthood (63 days) from small intestine by 16S rRNA gene-specific next-generation sequencing. Infected mice underwent long-lasting changes in microbiota composition, associated with increase in fat mass. High-fat-high-glucose diet promoted this effect while co-housing with mock-treated animals overwrote the weight gain. Our data suggest that in the critical phase of infancy even a single silent viral infection could cast a long shadow and cause long-term microbiota perturbations, affecting adult host physiology. Nature Publishing Group UK 2022-07-02 /pmc/articles/PMC9250495/ /pubmed/35780244 http://dx.doi.org/10.1038/s41522-022-00315-x Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Brief Communication
Yildiz, Soner
Mazel-Sanchez, Beryl
Bonifacio, Joao P. P.
Schmolke, Mirco
A single respiratory tract infection early in life reroutes healthy microbiome development and affects adult metabolism in a preclinical animal model
title A single respiratory tract infection early in life reroutes healthy microbiome development and affects adult metabolism in a preclinical animal model
title_full A single respiratory tract infection early in life reroutes healthy microbiome development and affects adult metabolism in a preclinical animal model
title_fullStr A single respiratory tract infection early in life reroutes healthy microbiome development and affects adult metabolism in a preclinical animal model
title_full_unstemmed A single respiratory tract infection early in life reroutes healthy microbiome development and affects adult metabolism in a preclinical animal model
title_short A single respiratory tract infection early in life reroutes healthy microbiome development and affects adult metabolism in a preclinical animal model
title_sort single respiratory tract infection early in life reroutes healthy microbiome development and affects adult metabolism in a preclinical animal model
topic Brief Communication
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9250495/
https://www.ncbi.nlm.nih.gov/pubmed/35780244
http://dx.doi.org/10.1038/s41522-022-00315-x
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