Indirect Pathogenicity of <italic toggle="yes">Haemophilus influenzae</italic> and <italic toggle="yes">Moraxella catarrhalis</italic> in Polymicrobial Otitis Media Occurs via Interspecies Quorum Signaling

ABSTRACT Otitis media (OM) is among the leading diseases of childhood and is caused by opportunists that reside within the nasopharynx, such as Haemophilus influenzae and Moraxella catarrhalis. As with most airway infections, it is now clear that OM infections involve multiple organisms. This study...

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Autores principales:	Chelsie E. Armbruster, Wenzhou Hong, Bing Pang, Kristin E. D. Weimer, Richard A. Juneau, James Turner, W. Edward Swords
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2010
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/f30527172ea64d8b9284d4e64280f0f8
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spelling	oai:doaj.org-article:f30527172ea64d8b9284d4e64280f0f82021-11-15T15:38:15ZIndirect Pathogenicity of <italic toggle="yes">Haemophilus influenzae</italic> and <italic toggle="yes">Moraxella catarrhalis</italic> in Polymicrobial Otitis Media Occurs via Interspecies Quorum Signaling10.1128/mBio.00102-102150-7511https://doaj.org/article/f30527172ea64d8b9284d4e64280f0f82010-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00102-10https://doaj.org/toc/2150-7511ABSTRACT Otitis media (OM) is among the leading diseases of childhood and is caused by opportunists that reside within the nasopharynx, such as Haemophilus influenzae and Moraxella catarrhalis. As with most airway infections, it is now clear that OM infections involve multiple organisms. This study addresses the hypothesis that polymicrobial infection alters the course, severity, and/or treatability of OM disease. The results clearly show that coinfection with H. influenzae and M. catarrhalis promotes the increased resistance of biofilms to antibiotics and host clearance. Using H. influenzae mutants with known biofilm defects, these phenotypes were shown to relate to biofilm maturation and autoinducer-2 (AI-2) quorum signaling. In support of the latter mechanism, chemically synthesized AI-2 (dihydroxypentanedione [DPD]) promoted increased M. catarrhalis biofilm formation and resistance to antibiotics. In the chinchilla infection model of OM, polymicrobial infection promoted M. catarrhalis persistence beyond the levels seen in animals infected with M. catarrhalis alone. Notably, no such enhancement of M. catarrhalis persistence was observed in animals infected with M. catarrhalis and a quorum signaling-deficient H. influenzae luxS mutant strain. We thus conclude that H. influenzae promotes M. catarrhalis persistence within polymicrobial biofilms via interspecies quorum signaling. AI-2 may therefore represent an ideal target for disruption of chronic polymicrobial infections. Moreover, these results strongly imply that successful vaccination against the unencapsulated H. influenzae strains that cause airway infections may also significantly impact chronic M. catarrhalis disease by removing a reservoir of the AI-2 signal that promotes M. catarrhalis persistence within biofilm. IMPORTANCE Otitis media (OM) is one of the most common childhood infections and is a leading reason for antibiotic prescriptions to children. Chronic and recurrent OM involves persistence of bacteria within biofilm communities, a state in which they are highly resistant to immune clearance and antibiotic treatment. While it is clear that most of these infections involve multiple species, the vast majority of knowledge about OM infections has been derived from work involving single bacterial species. There is a pressing need for better understanding of the impact of polymicrobial infection on the course, severity, and treatability of OM disease. In this study, we show that communication between bacterial species promotes bacterial persistence and resistance to antibiotics, which are important considerations in the diagnosis, prevention, and treatment of OM. Moreover, the results of this study indicate that successful preventive measures against H. influenzae could reduce the levels of disease caused by M. catarrhalis.Chelsie E. ArmbrusterWenzhou HongBing PangKristin E. D. WeimerRichard A. JuneauJames TurnerW. Edward SwordsAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 1, Iss 3 (2010)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Chelsie E. Armbruster Wenzhou Hong Bing Pang Kristin E. D. Weimer Richard A. Juneau James Turner W. Edward Swords Indirect Pathogenicity of <italic toggle="yes">Haemophilus influenzae</italic> and <italic toggle="yes">Moraxella catarrhalis</italic> in Polymicrobial Otitis Media Occurs via Interspecies Quorum Signaling
description	ABSTRACT Otitis media (OM) is among the leading diseases of childhood and is caused by opportunists that reside within the nasopharynx, such as Haemophilus influenzae and Moraxella catarrhalis. As with most airway infections, it is now clear that OM infections involve multiple organisms. This study addresses the hypothesis that polymicrobial infection alters the course, severity, and/or treatability of OM disease. The results clearly show that coinfection with H. influenzae and M. catarrhalis promotes the increased resistance of biofilms to antibiotics and host clearance. Using H. influenzae mutants with known biofilm defects, these phenotypes were shown to relate to biofilm maturation and autoinducer-2 (AI-2) quorum signaling. In support of the latter mechanism, chemically synthesized AI-2 (dihydroxypentanedione [DPD]) promoted increased M. catarrhalis biofilm formation and resistance to antibiotics. In the chinchilla infection model of OM, polymicrobial infection promoted M. catarrhalis persistence beyond the levels seen in animals infected with M. catarrhalis alone. Notably, no such enhancement of M. catarrhalis persistence was observed in animals infected with M. catarrhalis and a quorum signaling-deficient H. influenzae luxS mutant strain. We thus conclude that H. influenzae promotes M. catarrhalis persistence within polymicrobial biofilms via interspecies quorum signaling. AI-2 may therefore represent an ideal target for disruption of chronic polymicrobial infections. Moreover, these results strongly imply that successful vaccination against the unencapsulated H. influenzae strains that cause airway infections may also significantly impact chronic M. catarrhalis disease by removing a reservoir of the AI-2 signal that promotes M. catarrhalis persistence within biofilm. IMPORTANCE Otitis media (OM) is one of the most common childhood infections and is a leading reason for antibiotic prescriptions to children. Chronic and recurrent OM involves persistence of bacteria within biofilm communities, a state in which they are highly resistant to immune clearance and antibiotic treatment. While it is clear that most of these infections involve multiple species, the vast majority of knowledge about OM infections has been derived from work involving single bacterial species. There is a pressing need for better understanding of the impact of polymicrobial infection on the course, severity, and treatability of OM disease. In this study, we show that communication between bacterial species promotes bacterial persistence and resistance to antibiotics, which are important considerations in the diagnosis, prevention, and treatment of OM. Moreover, the results of this study indicate that successful preventive measures against H. influenzae could reduce the levels of disease caused by M. catarrhalis.
format	article
author	Chelsie E. Armbruster Wenzhou Hong Bing Pang Kristin E. D. Weimer Richard A. Juneau James Turner W. Edward Swords
author_facet	Chelsie E. Armbruster Wenzhou Hong Bing Pang Kristin E. D. Weimer Richard A. Juneau James Turner W. Edward Swords
author_sort	Chelsie E. Armbruster
title	Indirect Pathogenicity of <italic toggle="yes">Haemophilus influenzae</italic> and <italic toggle="yes">Moraxella catarrhalis</italic> in Polymicrobial Otitis Media Occurs via Interspecies Quorum Signaling
title_short	Indirect Pathogenicity of <italic toggle="yes">Haemophilus influenzae</italic> and <italic toggle="yes">Moraxella catarrhalis</italic> in Polymicrobial Otitis Media Occurs via Interspecies Quorum Signaling
title_full	Indirect Pathogenicity of <italic toggle="yes">Haemophilus influenzae</italic> and <italic toggle="yes">Moraxella catarrhalis</italic> in Polymicrobial Otitis Media Occurs via Interspecies Quorum Signaling
title_fullStr	Indirect Pathogenicity of <italic toggle="yes">Haemophilus influenzae</italic> and <italic toggle="yes">Moraxella catarrhalis</italic> in Polymicrobial Otitis Media Occurs via Interspecies Quorum Signaling
title_full_unstemmed	Indirect Pathogenicity of <italic toggle="yes">Haemophilus influenzae</italic> and <italic toggle="yes">Moraxella catarrhalis</italic> in Polymicrobial Otitis Media Occurs via Interspecies Quorum Signaling
title_sort	indirect pathogenicity of <italic toggle="yes">haemophilus influenzae</italic> and <italic toggle="yes">moraxella catarrhalis</italic> in polymicrobial otitis media occurs via interspecies quorum signaling
publisher	American Society for Microbiology
publishDate	2010
url	https://doaj.org/article/f30527172ea64d8b9284d4e64280f0f8
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Indirect Pathogenicity of <italic toggle="yes">Haemophilus influenzae</italic> and <italic toggle="yes">Moraxella catarrhalis</italic> in Polymicrobial Otitis Media Occurs via Interspecies Quorum Signaling

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