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A role of epithelial cells and virulence factors in biofilm formation by Streptococcus pyogenes in vitro

Alamiri, Feiruz LU ; Chao, Yashuan LU ; Baumgarten, Maria LU ; Riesbeck, Kristian LU orcid and Hakansson, Anders P LU orcid (2020) In Infection and Immunity 88(10).
Abstract

Biofilm formation by Streptococcus pyogenes (GAS) in model systems mimicking the respiratory tract is poorly documented. Most studies have been conducted on abiotic surfaces, which poorly represent human tissues. We have previously shown that GAS forms mature and antibiotic-resistant biofilms on physiologically relevant epithelial cells. However, the role of the substratum, extracellular matrix (ECM) components, or GAS virulence factors for biofilm formation and structure is unclear. In this study, biofilm formation was measured on respiratory epithelial cells and keratinocytes by determining biomass and antibiotic resistance, and biofilm morphology was visualized using scanning electron microscopy. All GAS isolates tested formed... (More)

Biofilm formation by Streptococcus pyogenes (GAS) in model systems mimicking the respiratory tract is poorly documented. Most studies have been conducted on abiotic surfaces, which poorly represent human tissues. We have previously shown that GAS forms mature and antibiotic-resistant biofilms on physiologically relevant epithelial cells. However, the role of the substratum, extracellular matrix (ECM) components, or GAS virulence factors for biofilm formation and structure is unclear. In this study, biofilm formation was measured on respiratory epithelial cells and keratinocytes by determining biomass and antibiotic resistance, and biofilm morphology was visualized using scanning electron microscopy. All GAS isolates tested formed biofilms that had similar, albeit not identical, biomass and antibiotic resistance for both cell types. Interestingly, functionally mature biofilms formed more rapidly on keratinocytes but were structurally denser and coated with more ECM on respiratory epithelial cells. The ECM was crucial for biofilm integrity, as protein- and DNA-degrading enzymes induced bacterial release from biofilms. Abiotic surfaces supported biofilm formation, but these biofilms were structurally less dense and organized. No major role of M protein, capsule, or Streptolysin O was observed in biofilm formation on epithelial cells, although some morphological differences were detected. NAD-glycohydrolase was required for optimal biofilm formation, whereas Streptolysin S or cysteine protease SpeB impaired this process. Finally, no correlation was found between cell adherence or auto-aggregation and GAS biofilm formation. Combined, these results provide a better understanding of the role of biofilm formation in GAS pathogenesis and can potentially provide novel targets for future treatments against GAS infections.

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organization
publishing date
type
Contribution to journal
publication status
published
subject
in
Infection and Immunity
volume
88
issue
10
article number
e00133-20
publisher
American Society for Microbiology
external identifiers
  • pmid:32661124
  • scopus:85091324491
ISSN
1098-5522
DOI
10.1128/IAI.00133-20
language
English
LU publication?
yes
additional info
Copyright © 2020 American Society for Microbiology.
id
72357db2-2d89-421e-8108-673b54013b25
date added to LUP
2020-07-19 21:42:30
date last changed
2024-05-29 17:02:25
@article{72357db2-2d89-421e-8108-673b54013b25,
  abstract     = {{<p>Biofilm formation by Streptococcus pyogenes (GAS) in model systems mimicking the respiratory tract is poorly documented. Most studies have been conducted on abiotic surfaces, which poorly represent human tissues. We have previously shown that GAS forms mature and antibiotic-resistant biofilms on physiologically relevant epithelial cells. However, the role of the substratum, extracellular matrix (ECM) components, or GAS virulence factors for biofilm formation and structure is unclear. In this study, biofilm formation was measured on respiratory epithelial cells and keratinocytes by determining biomass and antibiotic resistance, and biofilm morphology was visualized using scanning electron microscopy. All GAS isolates tested formed biofilms that had similar, albeit not identical, biomass and antibiotic resistance for both cell types. Interestingly, functionally mature biofilms formed more rapidly on keratinocytes but were structurally denser and coated with more ECM on respiratory epithelial cells. The ECM was crucial for biofilm integrity, as protein- and DNA-degrading enzymes induced bacterial release from biofilms. Abiotic surfaces supported biofilm formation, but these biofilms were structurally less dense and organized. No major role of M protein, capsule, or Streptolysin O was observed in biofilm formation on epithelial cells, although some morphological differences were detected. NAD-glycohydrolase was required for optimal biofilm formation, whereas Streptolysin S or cysteine protease SpeB impaired this process. Finally, no correlation was found between cell adherence or auto-aggregation and GAS biofilm formation. Combined, these results provide a better understanding of the role of biofilm formation in GAS pathogenesis and can potentially provide novel targets for future treatments against GAS infections.</p>}},
  author       = {{Alamiri, Feiruz and Chao, Yashuan and Baumgarten, Maria and Riesbeck, Kristian and Hakansson, Anders P}},
  issn         = {{1098-5522}},
  language     = {{eng}},
  month        = {{09}},
  number       = {{10}},
  publisher    = {{American Society for Microbiology}},
  series       = {{Infection and Immunity}},
  title        = {{A role of epithelial cells and virulence factors in biofilm formation by Streptococcus pyogenes in vitro}},
  url          = {{http://dx.doi.org/10.1128/IAI.00133-20}},
  doi          = {{10.1128/IAI.00133-20}},
  volume       = {{88}},
  year         = {{2020}},
}