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Unique microbial landscape in the human oropharynx during different types of acute respiratory tract infections

BACKGROUND: Secondary bacterial infections and pneumonia are major mortality causes of respiratory viruses, and the disruption of the upper respiratory tract (URT) microbiota is a crucial component of this process. However, whether this URT dysbiosis associates with the viral species (in other words...

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Autores principales: Li, Hui, Wu, Xiaorong, Zeng, Hong, Chang, Bozhen, Cui, Ying, Zhang, Jingxiang, Wang, Ruixia, Ding, Tao
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10364384/
https://www.ncbi.nlm.nih.gov/pubmed/37482605
http://dx.doi.org/10.1186/s40168-023-01597-9
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author Li, Hui
Wu, Xiaorong
Zeng, Hong
Chang, Bozhen
Cui, Ying
Zhang, Jingxiang
Wang, Ruixia
Ding, Tao
author_facet Li, Hui
Wu, Xiaorong
Zeng, Hong
Chang, Bozhen
Cui, Ying
Zhang, Jingxiang
Wang, Ruixia
Ding, Tao
author_sort Li, Hui
collection PubMed
description BACKGROUND: Secondary bacterial infections and pneumonia are major mortality causes of respiratory viruses, and the disruption of the upper respiratory tract (URT) microbiota is a crucial component of this process. However, whether this URT dysbiosis associates with the viral species (in other words, is viral type-specific) is unclear. RESULTS: Here, we recruited 735 outpatients with upper respiratory symptoms, identified the infectious virus types in 349 participants using multiplex RT-PCR, and profiled their upper respiratory microbiome using the 16S ribosomal RNA gene and metagenomic gene sequencing. Microbial and viral data were subsequently used as inputs for multivariate analysis aimed at revealing viral type-specific disruption of the upper respiratory microbiota. We found that the oropharyngeal microbiota shaped by influenza A virus (FluA), influenza B virus (FluB), respiratory syncytial virus (RSV), and human rhinovirus (HRV) infections exhibited three distinct patterns of dysbiosis, and Veillonella was identified as a prominent biomarker for any type of respiratory viral infections. Influenza virus infections are significantly correlated with increased oropharynx microbiota diversity and enrichment of functional metabolic pathways such as L-arginine biosynthesis and tetracycline resistance gene tetW. We used the GRiD algorithm and found the predicted growth rate of common respiratory pathogens was increased upon influenza virus infection, while commensal bacteria, such as Streptococcus infantis and Streptococcus mitis, may act as a colonization resistance to the overgrowth of these pathogens. CONCLUSIONS: We found that respiratory viral infections are linked with viral type-specific disruption of the upper respiratory microbiota, particularly, influenza infections uniquely associated with increased microbial diversity and growth rates of specific pathogens in URT. These findings are essential for clarifying the differences and dynamics of respiratory microbiota in healthy participants and acute respiratory viral infections, which contribute to elucidating the pathogenesis of viral-host-bacterial interactions to provide insights into future studies on effective prevention and treatment of respiratory tract infections. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-023-01597-9.
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spelling pubmed-103643842023-07-25 Unique microbial landscape in the human oropharynx during different types of acute respiratory tract infections Li, Hui Wu, Xiaorong Zeng, Hong Chang, Bozhen Cui, Ying Zhang, Jingxiang Wang, Ruixia Ding, Tao Microbiome Research BACKGROUND: Secondary bacterial infections and pneumonia are major mortality causes of respiratory viruses, and the disruption of the upper respiratory tract (URT) microbiota is a crucial component of this process. However, whether this URT dysbiosis associates with the viral species (in other words, is viral type-specific) is unclear. RESULTS: Here, we recruited 735 outpatients with upper respiratory symptoms, identified the infectious virus types in 349 participants using multiplex RT-PCR, and profiled their upper respiratory microbiome using the 16S ribosomal RNA gene and metagenomic gene sequencing. Microbial and viral data were subsequently used as inputs for multivariate analysis aimed at revealing viral type-specific disruption of the upper respiratory microbiota. We found that the oropharyngeal microbiota shaped by influenza A virus (FluA), influenza B virus (FluB), respiratory syncytial virus (RSV), and human rhinovirus (HRV) infections exhibited three distinct patterns of dysbiosis, and Veillonella was identified as a prominent biomarker for any type of respiratory viral infections. Influenza virus infections are significantly correlated with increased oropharynx microbiota diversity and enrichment of functional metabolic pathways such as L-arginine biosynthesis and tetracycline resistance gene tetW. We used the GRiD algorithm and found the predicted growth rate of common respiratory pathogens was increased upon influenza virus infection, while commensal bacteria, such as Streptococcus infantis and Streptococcus mitis, may act as a colonization resistance to the overgrowth of these pathogens. CONCLUSIONS: We found that respiratory viral infections are linked with viral type-specific disruption of the upper respiratory microbiota, particularly, influenza infections uniquely associated with increased microbial diversity and growth rates of specific pathogens in URT. These findings are essential for clarifying the differences and dynamics of respiratory microbiota in healthy participants and acute respiratory viral infections, which contribute to elucidating the pathogenesis of viral-host-bacterial interactions to provide insights into future studies on effective prevention and treatment of respiratory tract infections. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-023-01597-9. BioMed Central 2023-07-24 /pmc/articles/PMC10364384/ /pubmed/37482605 http://dx.doi.org/10.1186/s40168-023-01597-9 Text en © The Author(s) 2023 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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Li, Hui
Wu, Xiaorong
Zeng, Hong
Chang, Bozhen
Cui, Ying
Zhang, Jingxiang
Wang, Ruixia
Ding, Tao
Unique microbial landscape in the human oropharynx during different types of acute respiratory tract infections
title Unique microbial landscape in the human oropharynx during different types of acute respiratory tract infections
title_full Unique microbial landscape in the human oropharynx during different types of acute respiratory tract infections
title_fullStr Unique microbial landscape in the human oropharynx during different types of acute respiratory tract infections
title_full_unstemmed Unique microbial landscape in the human oropharynx during different types of acute respiratory tract infections
title_short Unique microbial landscape in the human oropharynx during different types of acute respiratory tract infections
title_sort unique microbial landscape in the human oropharynx during different types of acute respiratory tract infections
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10364384/
https://www.ncbi.nlm.nih.gov/pubmed/37482605
http://dx.doi.org/10.1186/s40168-023-01597-9
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