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Streptococcus pyogenes Capsule Promotes Microcolony-Independent Biofilm Formation

Biofilms play an important role in the pathogenesis of group A streptococcus (GAS), a Gram-positive pathogen responsible for a wide range of infections and with a significant public health impact. Although most GAS serotypes are able to form biofilms, there is a large amount of heterogeneity between...

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Autores principales: Matysik, Artur, Kline, Kimberly A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6707922/
https://www.ncbi.nlm.nih.gov/pubmed/31085695
http://dx.doi.org/10.1128/JB.00052-19
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author Matysik, Artur
Kline, Kimberly A.
author_facet Matysik, Artur
Kline, Kimberly A.
author_sort Matysik, Artur
collection PubMed
description Biofilms play an important role in the pathogenesis of group A streptococcus (GAS), a Gram-positive pathogen responsible for a wide range of infections and with a significant public health impact. Although most GAS serotypes are able to form biofilms, there is a large amount of heterogeneity between individual strains in biofilm formation, as measured by standard crystal violet assays. It is generally accepted that biofilm formation includes the initial adhesion of bacterial cells to a surface followed by microcolony formation, biofilm maturation, and extensive production of extracellular matrix that links together proliferating cells and provides a scaffold for the three-dimensional (3D) biofilm structure. However, our studies show that for GAS strain JS95, microcolony formation is not an essential step in static biofilm formation, and instead, biofilm can be effectively formed from slow-growing or nonreplicating late-exponential- or early-stationary-phase planktonic cells via sedimentation and fixation of GAS chains. In addition, we show that the GAS capsule specifically contributes to the alternative sedimentation-initiated biofilms. Microcolony-independent sedimentation biofilms are similar in morphology and 3D structure to biofilms initiated by actively dividing planktonic bacteria. We conclude that GAS can form biofilms by an alternate noncanonical mechanism that does not require transition from microcolony formation to biofilm maturation and which may be obscured by biofilm phenotypes that arise via the classical biofilm maturation processes. IMPORTANCE The static biofilm assay is a common tool for easy biomass quantification of biofilm-forming bacteria. However, Streptococcus pyogenes biofilm formation as measured by the static assay is strain dependent and yields heterogeneous results for different strains of the same serotype. In this study, we show that two independent mechanisms, for which the protective capsule contributes opposing functions, may contribute to static biofilm formation. We propose that separation of these mechanisms for biofilm formation might uncover previously unappreciated biofilm phenotypes that may otherwise be masked in the classic static assay.
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spelling pubmed-67079222019-08-29 Streptococcus pyogenes Capsule Promotes Microcolony-Independent Biofilm Formation Matysik, Artur Kline, Kimberly A. J Bacteriol Meeting Presentation Biofilms play an important role in the pathogenesis of group A streptococcus (GAS), a Gram-positive pathogen responsible for a wide range of infections and with a significant public health impact. Although most GAS serotypes are able to form biofilms, there is a large amount of heterogeneity between individual strains in biofilm formation, as measured by standard crystal violet assays. It is generally accepted that biofilm formation includes the initial adhesion of bacterial cells to a surface followed by microcolony formation, biofilm maturation, and extensive production of extracellular matrix that links together proliferating cells and provides a scaffold for the three-dimensional (3D) biofilm structure. However, our studies show that for GAS strain JS95, microcolony formation is not an essential step in static biofilm formation, and instead, biofilm can be effectively formed from slow-growing or nonreplicating late-exponential- or early-stationary-phase planktonic cells via sedimentation and fixation of GAS chains. In addition, we show that the GAS capsule specifically contributes to the alternative sedimentation-initiated biofilms. Microcolony-independent sedimentation biofilms are similar in morphology and 3D structure to biofilms initiated by actively dividing planktonic bacteria. We conclude that GAS can form biofilms by an alternate noncanonical mechanism that does not require transition from microcolony formation to biofilm maturation and which may be obscured by biofilm phenotypes that arise via the classical biofilm maturation processes. IMPORTANCE The static biofilm assay is a common tool for easy biomass quantification of biofilm-forming bacteria. However, Streptococcus pyogenes biofilm formation as measured by the static assay is strain dependent and yields heterogeneous results for different strains of the same serotype. In this study, we show that two independent mechanisms, for which the protective capsule contributes opposing functions, may contribute to static biofilm formation. We propose that separation of these mechanisms for biofilm formation might uncover previously unappreciated biofilm phenotypes that may otherwise be masked in the classic static assay. American Society for Microbiology 2019-08-22 /pmc/articles/PMC6707922/ /pubmed/31085695 http://dx.doi.org/10.1128/JB.00052-19 Text en Copyright © 2019 Matysik and Kline. https://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Meeting Presentation
Matysik, Artur
Kline, Kimberly A.
Streptococcus pyogenes Capsule Promotes Microcolony-Independent Biofilm Formation
title Streptococcus pyogenes Capsule Promotes Microcolony-Independent Biofilm Formation
title_full Streptococcus pyogenes Capsule Promotes Microcolony-Independent Biofilm Formation
title_fullStr Streptococcus pyogenes Capsule Promotes Microcolony-Independent Biofilm Formation
title_full_unstemmed Streptococcus pyogenes Capsule Promotes Microcolony-Independent Biofilm Formation
title_short Streptococcus pyogenes Capsule Promotes Microcolony-Independent Biofilm Formation
title_sort streptococcus pyogenes capsule promotes microcolony-independent biofilm formation
topic Meeting Presentation
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6707922/
https://www.ncbi.nlm.nih.gov/pubmed/31085695
http://dx.doi.org/10.1128/JB.00052-19
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