<italic toggle="yes">Staphylococcus aureus</italic> Biofilm Growth on Cystic Fibrosis Airway Epithelial Cells Is Enhanced during Respiratory Syncytial Virus Coinfection

ABSTRACT Staphylococcus aureus is a major cause of chronic respiratory infection in patients with cystic fibrosis (CF). We recently showed that Pseudomonas aeruginosa exhibits enhanced biofilm formation during respiratory syncytial virus (RSV) coinfection on human CF airway epithelial cells (AECs)....

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Autores principales:	Megan R. Kiedrowski, Jordan R. Gaston, Brian R. Kocak, Stefanie L. Coburn, Stella Lee, Joseph M. Pilewski, Michael M. Myerburg, Jennifer M. Bomberger
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	biofilms coinfection host-pathogen interaction polymicrobial Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/51d68d59419d4857a34322c5060ac47e
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spelling	oai:doaj.org-article:51d68d59419d4857a34322c5060ac47e2021-11-15T15:25:50Z<italic toggle="yes">Staphylococcus aureus</italic> Biofilm Growth on Cystic Fibrosis Airway Epithelial Cells Is Enhanced during Respiratory Syncytial Virus Coinfection10.1128/mSphere.00341-182379-5042https://doaj.org/article/51d68d59419d4857a34322c5060ac47e2018-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00341-18https://doaj.org/toc/2379-5042ABSTRACT Staphylococcus aureus is a major cause of chronic respiratory infection in patients with cystic fibrosis (CF). We recently showed that Pseudomonas aeruginosa exhibits enhanced biofilm formation during respiratory syncytial virus (RSV) coinfection on human CF airway epithelial cells (AECs). The impact of respiratory viruses on other bacterial pathogens during polymicrobial infections in CF remains largely unknown. To investigate if S. aureus biofilm growth in the CF airways is impacted by virus coinfection, we evaluated S. aureus growth on CF AECs. Initial studies showed an increase in S. aureus growth over 24 h, and microscopy revealed biofilm-like clusters of bacteria on CF AECs. Biofilm growth was enhanced when CF AECs were coinfected with RSV, and this observation was confirmed with S. aureus CF clinical isolates. Apical conditioned medium from RSV-infected cells promoted S. aureus biofilms in the absence of the host epithelium, suggesting that a secreted factor produced during virus infection benefits S. aureus biofilms. Exogenous iron addition did not significantly alter biofilm formation, suggesting that it is not likely the secreted factor. We further characterized S. aureus-RSV coinfection in our model using dual host-pathogen RNA sequencing, allowing us to observe specific contributions of S. aureus and RSV to the host response during coinfection. Using the dual host-pathogen RNA sequencing approach, we observed increased availability of nutrients from the host and upregulation of S. aureus genes involved in growth, protein translation and export, and amino acid metabolism during RSV coinfection. IMPORTANCE The airways of individuals with cystic fibrosis (CF) are commonly chronically infected, and Staphylococcus aureus is the dominant bacterial respiratory pathogen in CF children. CF patients also experience frequent respiratory virus infections, and it has been hypothesized that virus coinfection increases the severity of S. aureus lung infections in CF. We investigated the relationship between S. aureus and the CF airway epithelium and observed that coinfection with respiratory syncytial virus (RSV) enhances S. aureus biofilm growth. However, iron, which was previously found to be a significant factor influencing Pseudomonas aeruginosa biofilms during virus coinfection, plays a minor role in S. aureus coinfections. Transcriptomic analyses provided new insight into how bacterial and viral pathogens alter host defense and suggest potential pathways by which dampening of host responses to one pathogen may favor persistence of another in the CF airways, highlighting complex interactions occurring between bacteria, viruses, and the host during polymicrobial infections.Megan R. KiedrowskiJordan R. GastonBrian R. KocakStefanie L. CoburnStella LeeJoseph M. PilewskiMichael M. MyerburgJennifer M. BombergerAmerican Society for Microbiologyarticlebiofilmscoinfectionhost-pathogen interactionpolymicrobialMicrobiologyQR1-502ENmSphere, Vol 3, Iss 4 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	biofilms coinfection host-pathogen interaction polymicrobial Microbiology QR1-502
spellingShingle	biofilms coinfection host-pathogen interaction polymicrobial Microbiology QR1-502 Megan R. Kiedrowski Jordan R. Gaston Brian R. Kocak Stefanie L. Coburn Stella Lee Joseph M. Pilewski Michael M. Myerburg Jennifer M. Bomberger <italic toggle="yes">Staphylococcus aureus</italic> Biofilm Growth on Cystic Fibrosis Airway Epithelial Cells Is Enhanced during Respiratory Syncytial Virus Coinfection
description	ABSTRACT Staphylococcus aureus is a major cause of chronic respiratory infection in patients with cystic fibrosis (CF). We recently showed that Pseudomonas aeruginosa exhibits enhanced biofilm formation during respiratory syncytial virus (RSV) coinfection on human CF airway epithelial cells (AECs). The impact of respiratory viruses on other bacterial pathogens during polymicrobial infections in CF remains largely unknown. To investigate if S. aureus biofilm growth in the CF airways is impacted by virus coinfection, we evaluated S. aureus growth on CF AECs. Initial studies showed an increase in S. aureus growth over 24 h, and microscopy revealed biofilm-like clusters of bacteria on CF AECs. Biofilm growth was enhanced when CF AECs were coinfected with RSV, and this observation was confirmed with S. aureus CF clinical isolates. Apical conditioned medium from RSV-infected cells promoted S. aureus biofilms in the absence of the host epithelium, suggesting that a secreted factor produced during virus infection benefits S. aureus biofilms. Exogenous iron addition did not significantly alter biofilm formation, suggesting that it is not likely the secreted factor. We further characterized S. aureus-RSV coinfection in our model using dual host-pathogen RNA sequencing, allowing us to observe specific contributions of S. aureus and RSV to the host response during coinfection. Using the dual host-pathogen RNA sequencing approach, we observed increased availability of nutrients from the host and upregulation of S. aureus genes involved in growth, protein translation and export, and amino acid metabolism during RSV coinfection. IMPORTANCE The airways of individuals with cystic fibrosis (CF) are commonly chronically infected, and Staphylococcus aureus is the dominant bacterial respiratory pathogen in CF children. CF patients also experience frequent respiratory virus infections, and it has been hypothesized that virus coinfection increases the severity of S. aureus lung infections in CF. We investigated the relationship between S. aureus and the CF airway epithelium and observed that coinfection with respiratory syncytial virus (RSV) enhances S. aureus biofilm growth. However, iron, which was previously found to be a significant factor influencing Pseudomonas aeruginosa biofilms during virus coinfection, plays a minor role in S. aureus coinfections. Transcriptomic analyses provided new insight into how bacterial and viral pathogens alter host defense and suggest potential pathways by which dampening of host responses to one pathogen may favor persistence of another in the CF airways, highlighting complex interactions occurring between bacteria, viruses, and the host during polymicrobial infections.
format	article
author	Megan R. Kiedrowski Jordan R. Gaston Brian R. Kocak Stefanie L. Coburn Stella Lee Joseph M. Pilewski Michael M. Myerburg Jennifer M. Bomberger
author_facet	Megan R. Kiedrowski Jordan R. Gaston Brian R. Kocak Stefanie L. Coburn Stella Lee Joseph M. Pilewski Michael M. Myerburg Jennifer M. Bomberger
author_sort	Megan R. Kiedrowski
title	<italic toggle="yes">Staphylococcus aureus</italic> Biofilm Growth on Cystic Fibrosis Airway Epithelial Cells Is Enhanced during Respiratory Syncytial Virus Coinfection
title_short	<italic toggle="yes">Staphylococcus aureus</italic> Biofilm Growth on Cystic Fibrosis Airway Epithelial Cells Is Enhanced during Respiratory Syncytial Virus Coinfection
title_full	<italic toggle="yes">Staphylococcus aureus</italic> Biofilm Growth on Cystic Fibrosis Airway Epithelial Cells Is Enhanced during Respiratory Syncytial Virus Coinfection
title_fullStr	<italic toggle="yes">Staphylococcus aureus</italic> Biofilm Growth on Cystic Fibrosis Airway Epithelial Cells Is Enhanced during Respiratory Syncytial Virus Coinfection
title_full_unstemmed	<italic toggle="yes">Staphylococcus aureus</italic> Biofilm Growth on Cystic Fibrosis Airway Epithelial Cells Is Enhanced during Respiratory Syncytial Virus Coinfection
title_sort	<italic toggle="yes">staphylococcus aureus</italic> biofilm growth on cystic fibrosis airway epithelial cells is enhanced during respiratory syncytial virus coinfection
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/51d68d59419d4857a34322c5060ac47e
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<italic toggle="yes">Staphylococcus aureus</italic> Biofilm Growth on Cystic Fibrosis Airway Epithelial Cells Is Enhanced during Respiratory Syncytial Virus Coinfection

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