Novel Role for the <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> Toxin Pneumolysin in the Assembly of Biofilms

ABSTRACT Streptococcus pneumoniae is an important commensal and pathogen responsible for almost a million deaths annually in children under five. The formation of biofilms by S. pneumoniae is important in nasopharyngeal colonization, pneumonia, and otitis media. Pneumolysin (Ply) is a toxin that con...

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Autores principales:	Joshua R. Shak, Herbert P. Ludewick, Kristen E. Howery, Fuminori Sakai, Hong Yi, Richard M. Harvey, James C. Paton, Keith P. Klugman, Jorge E. Vidal
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2013
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/cb7b494c6a8a40c1b8ae7c780fbb40da
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spelling	oai:doaj.org-article:cb7b494c6a8a40c1b8ae7c780fbb40da2021-11-15T15:42:47ZNovel Role for the <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> Toxin Pneumolysin in the Assembly of Biofilms10.1128/mBio.00655-132150-7511https://doaj.org/article/cb7b494c6a8a40c1b8ae7c780fbb40da2013-11-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00655-13https://doaj.org/toc/2150-7511ABSTRACT Streptococcus pneumoniae is an important commensal and pathogen responsible for almost a million deaths annually in children under five. The formation of biofilms by S. pneumoniae is important in nasopharyngeal colonization, pneumonia, and otitis media. Pneumolysin (Ply) is a toxin that contributes significantly to the virulence of S. pneumoniae and is an important candidate as a serotype-independent vaccine target. Having previously demonstrated that a luxS knockout mutant was unable to form early biofilms and expressed less ply mRNA than the wild type, we conducted a study to investigate the role of Ply in biofilm formation. We found that Ply was expressed in early phases of biofilm development and localized to cellular aggregates as early as 4 h postinoculation. S. pneumoniae ply knockout mutants in D39 and TIGR4 backgrounds produced significantly less biofilm biomass than wild-type strains at early time points, both on polystyrene and on human respiratory epithelial cells, cultured under static or continuous-flow conditions. Ply’s role in biofilm formation appears to be independent of its hemolytic activity, as S. pneumoniae serotype 1 strains, which produce a nonhemolytic variant of Ply, were still able to form biofilms. Transmission electron microscopy of biofilms grown on A549 lung cells using immunogold demonstrated that Ply was located both on the surfaces of pneumococcal cells and in the extracellular biofilm matrix. Altogether, our studies demonstrate a novel role for pneumolysin in the assembly of S. pneumoniae biofilms that is likely important during both carriage and disease and therefore significant for pneumolysin-targeting vaccines under development. IMPORTANCE The bacterium Streptococcus pneumoniae (commonly known as the pneumococcus) is commonly carried in the human nasopharynx and can spread to other body sites to cause disease. In the nasopharynx, middle ear, and lungs, the pneumococcus forms multicellular surface-associated structures called biofilms. Pneumolysin is an important toxin produced by almost all S. pneumoniae strains, extensively studied for its ability to cause damage to human tissue. In this paper, we demonstrate that pneumolysin has a previously unrecognized role in biofilm formation by showing that strains without pneumolysin are unable to form the same amount of biofilm on plastic and human cell substrates. Furthermore, we show that the role of pneumolysin in biofilm formation is separate from the hemolytic activity responsible for tissue damage during pneumococcal diseases. This novel role for pneumolysin suggests that pneumococcal vaccines directed against this protein should be investigated for their potential impact on biofilms formed during carriage and disease.Joshua R. ShakHerbert P. LudewickKristen E. HoweryFuminori SakaiHong YiRichard M. HarveyJames C. PatonKeith P. KlugmanJorge E. VidalAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 4, Iss 5 (2013)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Joshua R. Shak Herbert P. Ludewick Kristen E. Howery Fuminori Sakai Hong Yi Richard M. Harvey James C. Paton Keith P. Klugman Jorge E. Vidal Novel Role for the <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> Toxin Pneumolysin in the Assembly of Biofilms
description	ABSTRACT Streptococcus pneumoniae is an important commensal and pathogen responsible for almost a million deaths annually in children under five. The formation of biofilms by S. pneumoniae is important in nasopharyngeal colonization, pneumonia, and otitis media. Pneumolysin (Ply) is a toxin that contributes significantly to the virulence of S. pneumoniae and is an important candidate as a serotype-independent vaccine target. Having previously demonstrated that a luxS knockout mutant was unable to form early biofilms and expressed less ply mRNA than the wild type, we conducted a study to investigate the role of Ply in biofilm formation. We found that Ply was expressed in early phases of biofilm development and localized to cellular aggregates as early as 4 h postinoculation. S. pneumoniae ply knockout mutants in D39 and TIGR4 backgrounds produced significantly less biofilm biomass than wild-type strains at early time points, both on polystyrene and on human respiratory epithelial cells, cultured under static or continuous-flow conditions. Ply’s role in biofilm formation appears to be independent of its hemolytic activity, as S. pneumoniae serotype 1 strains, which produce a nonhemolytic variant of Ply, were still able to form biofilms. Transmission electron microscopy of biofilms grown on A549 lung cells using immunogold demonstrated that Ply was located both on the surfaces of pneumococcal cells and in the extracellular biofilm matrix. Altogether, our studies demonstrate a novel role for pneumolysin in the assembly of S. pneumoniae biofilms that is likely important during both carriage and disease and therefore significant for pneumolysin-targeting vaccines under development. IMPORTANCE The bacterium Streptococcus pneumoniae (commonly known as the pneumococcus) is commonly carried in the human nasopharynx and can spread to other body sites to cause disease. In the nasopharynx, middle ear, and lungs, the pneumococcus forms multicellular surface-associated structures called biofilms. Pneumolysin is an important toxin produced by almost all S. pneumoniae strains, extensively studied for its ability to cause damage to human tissue. In this paper, we demonstrate that pneumolysin has a previously unrecognized role in biofilm formation by showing that strains without pneumolysin are unable to form the same amount of biofilm on plastic and human cell substrates. Furthermore, we show that the role of pneumolysin in biofilm formation is separate from the hemolytic activity responsible for tissue damage during pneumococcal diseases. This novel role for pneumolysin suggests that pneumococcal vaccines directed against this protein should be investigated for their potential impact on biofilms formed during carriage and disease.
format	article
author	Joshua R. Shak Herbert P. Ludewick Kristen E. Howery Fuminori Sakai Hong Yi Richard M. Harvey James C. Paton Keith P. Klugman Jorge E. Vidal
author_facet	Joshua R. Shak Herbert P. Ludewick Kristen E. Howery Fuminori Sakai Hong Yi Richard M. Harvey James C. Paton Keith P. Klugman Jorge E. Vidal
author_sort	Joshua R. Shak
title	Novel Role for the <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> Toxin Pneumolysin in the Assembly of Biofilms
title_short	Novel Role for the <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> Toxin Pneumolysin in the Assembly of Biofilms
title_full	Novel Role for the <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> Toxin Pneumolysin in the Assembly of Biofilms
title_fullStr	Novel Role for the <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> Toxin Pneumolysin in the Assembly of Biofilms
title_full_unstemmed	Novel Role for the <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> Toxin Pneumolysin in the Assembly of Biofilms
title_sort	novel role for the <named-content content-type="genus-species">streptococcus pneumoniae</named-content> toxin pneumolysin in the assembly of biofilms
publisher	American Society for Microbiology
publishDate	2013
url	https://doaj.org/article/cb7b494c6a8a40c1b8ae7c780fbb40da
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Novel Role for the <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> Toxin Pneumolysin in the Assembly of Biofilms

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