CdrA Interactions within the <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Biofilm Matrix Safeguard It from Proteolysis and Promote Cellular Packing

ABSTRACT Biofilms are robust multicellular aggregates of bacteria that are encased in an extracellular matrix. Different bacterial species have been shown to use a range of biopolymers to build their matrices. Pseudomonas aeruginosa is a model organism for the laboratory study of biofilms, and past...

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Autores principales: Courtney Reichhardt, Cynthis Wong, Daniel Passos da Silva, Daniel J. Wozniak, Matthew R. Parsek
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Publicado: American Society for Microbiology 2018
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spelling oai:doaj.org-article:64fae2abc88c4308beb2caab1749864b2021-11-15T15:58:21ZCdrA Interactions within the <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Biofilm Matrix Safeguard It from Proteolysis and Promote Cellular Packing10.1128/mBio.01376-182150-7511https://doaj.org/article/64fae2abc88c4308beb2caab1749864b2018-11-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01376-18https://doaj.org/toc/2150-7511ABSTRACT Biofilms are robust multicellular aggregates of bacteria that are encased in an extracellular matrix. Different bacterial species have been shown to use a range of biopolymers to build their matrices. Pseudomonas aeruginosa is a model organism for the laboratory study of biofilms, and past work has suggested that exopolysaccharides are a required matrix component. However, we found that expression of the matrix protein CdrA, in the absence of biofilm exopolysaccharides, allowed biofilm formation through the production of a CdrA-rich proteinaceous matrix. This represents a novel function for CdrA. Similar observations have been made for other species such as Escherichia coli and Staphylococcus aureus, which can utilize protein-dominant biofilm matrices. However, we found that these CdrA-containing matrices were susceptible to both exogenous and self-produced proteases. We previously reported that CdrA directly binds the biofilm matrix exopolysaccharide Psl. Now we have found that when CdrA bound to Psl, it was protected from proteolysis. Together, these results support the idea of the importance of multibiomolecular components in matrix stability and led us to propose a model in which CdrA-CdrA interactions can enhance cell-cell packing in an aggregate that is resistant to physical shear, while Psl-CdrA interactions enhance aggregate integrity in the presence of self-produced and exogenous proteases. IMPORTANCE Pseudomonas aeruginosa forms multicellular aggregates or biofilms using both exopolysaccharides and the CdrA matrix adhesin. We showed for the first time that P. aeruginosa can use CdrA to build biofilms that do not require known matrix exopolysaccharides. It is appreciated that biofilm growth is protective against environmental assaults. However, little is known about how the interactions between individual matrix components aid in this protection. We found that interactions between CdrA and the exopolysaccharide Psl fortify the matrix by preventing CdrA proteolysis. When both components—CdrA and Psl—are part of the matrix, robust aggregates form that are tightly packed and protease resistant. These findings provide insight into how biofilms persist in protease-rich host environments.Courtney ReichhardtCynthis WongDaniel Passos da SilvaDaniel J. WozniakMatthew R. ParsekAmerican Society for MicrobiologyarticleCdrAPseudomonas aeruginosaPslbiofilmelastaseexopolysaccharidesMicrobiologyQR1-502ENmBio, Vol 9, Iss 5 (2018)
institution DOAJ
collection DOAJ
language EN
topic CdrA
Pseudomonas aeruginosa
Psl
biofilm
elastase
exopolysaccharides
Microbiology
QR1-502
spellingShingle CdrA
Pseudomonas aeruginosa
Psl
biofilm
elastase
exopolysaccharides
Microbiology
QR1-502
Courtney Reichhardt
Cynthis Wong
Daniel Passos da Silva
Daniel J. Wozniak
Matthew R. Parsek
CdrA Interactions within the <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Biofilm Matrix Safeguard It from Proteolysis and Promote Cellular Packing
description ABSTRACT Biofilms are robust multicellular aggregates of bacteria that are encased in an extracellular matrix. Different bacterial species have been shown to use a range of biopolymers to build their matrices. Pseudomonas aeruginosa is a model organism for the laboratory study of biofilms, and past work has suggested that exopolysaccharides are a required matrix component. However, we found that expression of the matrix protein CdrA, in the absence of biofilm exopolysaccharides, allowed biofilm formation through the production of a CdrA-rich proteinaceous matrix. This represents a novel function for CdrA. Similar observations have been made for other species such as Escherichia coli and Staphylococcus aureus, which can utilize protein-dominant biofilm matrices. However, we found that these CdrA-containing matrices were susceptible to both exogenous and self-produced proteases. We previously reported that CdrA directly binds the biofilm matrix exopolysaccharide Psl. Now we have found that when CdrA bound to Psl, it was protected from proteolysis. Together, these results support the idea of the importance of multibiomolecular components in matrix stability and led us to propose a model in which CdrA-CdrA interactions can enhance cell-cell packing in an aggregate that is resistant to physical shear, while Psl-CdrA interactions enhance aggregate integrity in the presence of self-produced and exogenous proteases. IMPORTANCE Pseudomonas aeruginosa forms multicellular aggregates or biofilms using both exopolysaccharides and the CdrA matrix adhesin. We showed for the first time that P. aeruginosa can use CdrA to build biofilms that do not require known matrix exopolysaccharides. It is appreciated that biofilm growth is protective against environmental assaults. However, little is known about how the interactions between individual matrix components aid in this protection. We found that interactions between CdrA and the exopolysaccharide Psl fortify the matrix by preventing CdrA proteolysis. When both components—CdrA and Psl—are part of the matrix, robust aggregates form that are tightly packed and protease resistant. These findings provide insight into how biofilms persist in protease-rich host environments.
format article
author Courtney Reichhardt
Cynthis Wong
Daniel Passos da Silva
Daniel J. Wozniak
Matthew R. Parsek
author_facet Courtney Reichhardt
Cynthis Wong
Daniel Passos da Silva
Daniel J. Wozniak
Matthew R. Parsek
author_sort Courtney Reichhardt
title CdrA Interactions within the <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Biofilm Matrix Safeguard It from Proteolysis and Promote Cellular Packing
title_short CdrA Interactions within the <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Biofilm Matrix Safeguard It from Proteolysis and Promote Cellular Packing
title_full CdrA Interactions within the <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Biofilm Matrix Safeguard It from Proteolysis and Promote Cellular Packing
title_fullStr CdrA Interactions within the <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Biofilm Matrix Safeguard It from Proteolysis and Promote Cellular Packing
title_full_unstemmed CdrA Interactions within the <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Biofilm Matrix Safeguard It from Proteolysis and Promote Cellular Packing
title_sort cdra interactions within the <named-content content-type="genus-species">pseudomonas aeruginosa</named-content> biofilm matrix safeguard it from proteolysis and promote cellular packing
publisher American Society for Microbiology
publishDate 2018
url https://doaj.org/article/64fae2abc88c4308beb2caab1749864b
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