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Commensal colonization reduces Pseudomonas aeruginosa burden and subsequent airway damage

Pseudomonas aeruginosa dominates the complex polymicrobial cystic fibrosis (CF) airway and is a leading cause of death in persons with CF. Interestingly, oral streptococcal colonization has been associated with stable CF lung function. The most abundant streptococcal species found in stable patients...

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Autores principales: Stoner, Sara N., Baty, Joshua J., Novak, Lea, Scoffield, Jessica A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10248150/
https://www.ncbi.nlm.nih.gov/pubmed/37305417
http://dx.doi.org/10.3389/fcimb.2023.1144157
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author Stoner, Sara N.
Baty, Joshua J.
Novak, Lea
Scoffield, Jessica A.
author_facet Stoner, Sara N.
Baty, Joshua J.
Novak, Lea
Scoffield, Jessica A.
author_sort Stoner, Sara N.
collection PubMed
description Pseudomonas aeruginosa dominates the complex polymicrobial cystic fibrosis (CF) airway and is a leading cause of death in persons with CF. Interestingly, oral streptococcal colonization has been associated with stable CF lung function. The most abundant streptococcal species found in stable patients, Streptococcus salivarius, has been shown to downregulate pro-inflammatory cytokines in multiple colonization models. However, no studies have demonstrated how S. salivarius potentially improves lung function. Our lab previously demonstrated that the P. aeruginosa exopolysaccharide Psl promotes S. salivarius biofilm formation in vitro, suggesting a possible mechanism by which S. salivarius is incorporated into the CF airway microbial community. In this study, we demonstrate that co-infection of rats leads to enhanced S. salivarius colonization and reduced P. aeruginosa colonization. Histological scores for tissue inflammation and damage are lower in dual-infected rats compared to P. aeruginosa infected rats. Additionally, pro-inflammatory cytokines IL-1β, IL-6, CXCL2, and TNF-α are downregulated during co-infection compared to P. aeruginosa single-infection. Lastly, RNA sequencing of cultures grown in synthetic CF sputum revealed that P. aeruginosa glucose metabolism genes are downregulated in the presence of S. salivarius, suggesting a potential alteration in P. aeruginosa fitness during co-culture. Overall, our data support a model in which S. salivarius colonization is promoted during co-infection with P. aeruginosa, whereas P. aeruginosa airway bacterial burden is reduced, leading to an attenuated host inflammatory response.
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spelling pubmed-102481502023-06-09 Commensal colonization reduces Pseudomonas aeruginosa burden and subsequent airway damage Stoner, Sara N. Baty, Joshua J. Novak, Lea Scoffield, Jessica A. Front Cell Infect Microbiol Cellular and Infection Microbiology Pseudomonas aeruginosa dominates the complex polymicrobial cystic fibrosis (CF) airway and is a leading cause of death in persons with CF. Interestingly, oral streptococcal colonization has been associated with stable CF lung function. The most abundant streptococcal species found in stable patients, Streptococcus salivarius, has been shown to downregulate pro-inflammatory cytokines in multiple colonization models. However, no studies have demonstrated how S. salivarius potentially improves lung function. Our lab previously demonstrated that the P. aeruginosa exopolysaccharide Psl promotes S. salivarius biofilm formation in vitro, suggesting a possible mechanism by which S. salivarius is incorporated into the CF airway microbial community. In this study, we demonstrate that co-infection of rats leads to enhanced S. salivarius colonization and reduced P. aeruginosa colonization. Histological scores for tissue inflammation and damage are lower in dual-infected rats compared to P. aeruginosa infected rats. Additionally, pro-inflammatory cytokines IL-1β, IL-6, CXCL2, and TNF-α are downregulated during co-infection compared to P. aeruginosa single-infection. Lastly, RNA sequencing of cultures grown in synthetic CF sputum revealed that P. aeruginosa glucose metabolism genes are downregulated in the presence of S. salivarius, suggesting a potential alteration in P. aeruginosa fitness during co-culture. Overall, our data support a model in which S. salivarius colonization is promoted during co-infection with P. aeruginosa, whereas P. aeruginosa airway bacterial burden is reduced, leading to an attenuated host inflammatory response. Frontiers Media S.A. 2023-05-25 /pmc/articles/PMC10248150/ /pubmed/37305417 http://dx.doi.org/10.3389/fcimb.2023.1144157 Text en Copyright © 2023 Stoner, Baty, Novak and Scoffield https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Cellular and Infection Microbiology
Stoner, Sara N.
Baty, Joshua J.
Novak, Lea
Scoffield, Jessica A.
Commensal colonization reduces Pseudomonas aeruginosa burden and subsequent airway damage
title Commensal colonization reduces Pseudomonas aeruginosa burden and subsequent airway damage
title_full Commensal colonization reduces Pseudomonas aeruginosa burden and subsequent airway damage
title_fullStr Commensal colonization reduces Pseudomonas aeruginosa burden and subsequent airway damage
title_full_unstemmed Commensal colonization reduces Pseudomonas aeruginosa burden and subsequent airway damage
title_short Commensal colonization reduces Pseudomonas aeruginosa burden and subsequent airway damage
title_sort commensal colonization reduces pseudomonas aeruginosa burden and subsequent airway damage
topic Cellular and Infection Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10248150/
https://www.ncbi.nlm.nih.gov/pubmed/37305417
http://dx.doi.org/10.3389/fcimb.2023.1144157
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