Interkingdom Signaling Induces <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> Biofilm Dispersion and Transition from Asymptomatic Colonization to Disease

ABSTRACT Streptococcus pneumoniae is a common human nasopharyngeal commensal colonizing 10% to 40% of healthy individuals, depending on age. Despite a low invasive disease rate, widespread carriage ensures that infection occurs often enough to make S. pneumoniae a leading bacterial cause of respirat...

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Autores principales:	Laura R. Marks, Bruce A. Davidson, Paul R. Knight, Anders P. Hakansson
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2013
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/fae1ba4b5154420583c0e91c64ac97ab
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spelling	oai:doaj.org-article:fae1ba4b5154420583c0e91c64ac97ab2021-11-15T15:43:09ZInterkingdom Signaling Induces <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> Biofilm Dispersion and Transition from Asymptomatic Colonization to Disease10.1128/mBio.00438-132150-7511https://doaj.org/article/fae1ba4b5154420583c0e91c64ac97ab2013-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00438-13https://doaj.org/toc/2150-7511ABSTRACT Streptococcus pneumoniae is a common human nasopharyngeal commensal colonizing 10% to 40% of healthy individuals, depending on age. Despite a low invasive disease rate, widespread carriage ensures that infection occurs often enough to make S. pneumoniae a leading bacterial cause of respiratory disease worldwide. However, the mechanisms behind transition from asymptomatic colonization to dissemination and disease in otherwise sterile sites remain poorly understood but are epidemiologically strongly linked to infection with respiratory viruses. In this report, we show that infection with influenza A virus and treatment with the resulting host signals (febrile-range temperatures, norepinephrine, extracytoplasmic ATP, and increased nutrient availability) induce the release of bacteria from biofilms in a newly developed biofilm model on live epithelial cells both in vitro and during in vivo colonization. These dispersed bacteria have distinct phenotypic properties different from those of both biofilm and broth-grown, planktonic bacteria, with the dispersed population showing differential virulence gene expression characteristics resulting in a significantly increased ability to disseminate and cause infection of otherwise sterile sites, such as the middle ear, lungs, and bloodstream. The results offer novel and important insights into the role of interkingdom signaling between microbe and host during biofilm dispersion and transition to acute disease. IMPORTANCE This report addresses the mechanisms involved in transition from pneumococcal asymptomatic colonization to disease. In this study, we determined that changes in the nasopharyngeal environment result in the release of bacteria from colonizing biofilms with a gene expression and virulence phenotype different not only from that of colonizing biofilm bacteria but also from that of the broth-grown planktonic bacteria commonly used for pathogenesis studies. The work importantly also identifies specific host factors responsible for the release of bacteria and their changed phenotype. We show that these interkingdom signals are recognized by bacteria and are induced by influenza virus infection, which is epidemiologically strongly associated with transition to secondary pneumococcal disease. As virus infection is a common inducer of transition to disease among species occupying the nasopharynx, the results of this study may provide a basis for better understanding of the signals involved in the transition from colonization to disease in the human nasopharynx.Laura R. MarksBruce A. DavidsonPaul R. KnightAnders P. HakanssonAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 4, Iss 4 (2013)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Laura R. Marks Bruce A. Davidson Paul R. Knight Anders P. Hakansson Interkingdom Signaling Induces <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> Biofilm Dispersion and Transition from Asymptomatic Colonization to Disease
description	ABSTRACT Streptococcus pneumoniae is a common human nasopharyngeal commensal colonizing 10% to 40% of healthy individuals, depending on age. Despite a low invasive disease rate, widespread carriage ensures that infection occurs often enough to make S. pneumoniae a leading bacterial cause of respiratory disease worldwide. However, the mechanisms behind transition from asymptomatic colonization to dissemination and disease in otherwise sterile sites remain poorly understood but are epidemiologically strongly linked to infection with respiratory viruses. In this report, we show that infection with influenza A virus and treatment with the resulting host signals (febrile-range temperatures, norepinephrine, extracytoplasmic ATP, and increased nutrient availability) induce the release of bacteria from biofilms in a newly developed biofilm model on live epithelial cells both in vitro and during in vivo colonization. These dispersed bacteria have distinct phenotypic properties different from those of both biofilm and broth-grown, planktonic bacteria, with the dispersed population showing differential virulence gene expression characteristics resulting in a significantly increased ability to disseminate and cause infection of otherwise sterile sites, such as the middle ear, lungs, and bloodstream. The results offer novel and important insights into the role of interkingdom signaling between microbe and host during biofilm dispersion and transition to acute disease. IMPORTANCE This report addresses the mechanisms involved in transition from pneumococcal asymptomatic colonization to disease. In this study, we determined that changes in the nasopharyngeal environment result in the release of bacteria from colonizing biofilms with a gene expression and virulence phenotype different not only from that of colonizing biofilm bacteria but also from that of the broth-grown planktonic bacteria commonly used for pathogenesis studies. The work importantly also identifies specific host factors responsible for the release of bacteria and their changed phenotype. We show that these interkingdom signals are recognized by bacteria and are induced by influenza virus infection, which is epidemiologically strongly associated with transition to secondary pneumococcal disease. As virus infection is a common inducer of transition to disease among species occupying the nasopharynx, the results of this study may provide a basis for better understanding of the signals involved in the transition from colonization to disease in the human nasopharynx.
format	article
author	Laura R. Marks Bruce A. Davidson Paul R. Knight Anders P. Hakansson
author_facet	Laura R. Marks Bruce A. Davidson Paul R. Knight Anders P. Hakansson
author_sort	Laura R. Marks
title	Interkingdom Signaling Induces <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> Biofilm Dispersion and Transition from Asymptomatic Colonization to Disease
title_short	Interkingdom Signaling Induces <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> Biofilm Dispersion and Transition from Asymptomatic Colonization to Disease
title_full	Interkingdom Signaling Induces <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> Biofilm Dispersion and Transition from Asymptomatic Colonization to Disease
title_fullStr	Interkingdom Signaling Induces <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> Biofilm Dispersion and Transition from Asymptomatic Colonization to Disease
title_full_unstemmed	Interkingdom Signaling Induces <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> Biofilm Dispersion and Transition from Asymptomatic Colonization to Disease
title_sort	interkingdom signaling induces <named-content content-type="genus-species">streptococcus pneumoniae</named-content> biofilm dispersion and transition from asymptomatic colonization to disease
publisher	American Society for Microbiology
publishDate	2013
url	https://doaj.org/article/fae1ba4b5154420583c0e91c64ac97ab
work_keys_str_mv	AT laurarmarks interkingdomsignalinginducesnamedcontentcontenttypegenusspeciesstreptococcuspneumoniaenamedcontentbiofilmdispersionandtransitionfromasymptomaticcolonizationtodisease AT bruceadavidson interkingdomsignalinginducesnamedcontentcontenttypegenusspeciesstreptococcuspneumoniaenamedcontentbiofilmdispersionandtransitionfromasymptomaticcolonizationtodisease AT paulrknight interkingdomsignalinginducesnamedcontentcontenttypegenusspeciesstreptococcuspneumoniaenamedcontentbiofilmdispersionandtransitionfromasymptomaticcolonizationtodisease AT andersphakansson interkingdomsignalinginducesnamedcontentcontenttypegenusspeciesstreptococcuspneumoniaenamedcontentbiofilmdispersionandtransitionfromasymptomaticcolonizationtodisease
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Interkingdom Signaling Induces <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> Biofilm Dispersion and Transition from Asymptomatic Colonization to Disease

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