A Biofilm Matrix-Associated Protease Inhibitor Protects <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> from Proteolytic Attack

ABSTRACT Pseudomonas aeruginosa produces an extracellular biofilm matrix that consists of nucleic acids, exopolysaccharides, lipid vesicles, and proteins. In general, the protein component of the biofilm matrix is poorly defined and understudied relative to the other major matrix constituents. While...

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Autores principales: Boo Shan Tseng, Courtney Reichhardt, Gennifer E. Merrihew, Sophia A. Araujo-Hernandez, Joe J. Harrison, Michael J. MacCoss, Matthew R. Parsek
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Publicado: American Society for Microbiology 2018
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spelling oai:doaj.org-article:c73bbac4760e44f08cfcf26a00edf51a2021-11-15T15:53:26ZA Biofilm Matrix-Associated Protease Inhibitor Protects <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> from Proteolytic Attack10.1128/mBio.00543-182150-7511https://doaj.org/article/c73bbac4760e44f08cfcf26a00edf51a2018-05-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00543-18https://doaj.org/toc/2150-7511ABSTRACT Pseudomonas aeruginosa produces an extracellular biofilm matrix that consists of nucleic acids, exopolysaccharides, lipid vesicles, and proteins. In general, the protein component of the biofilm matrix is poorly defined and understudied relative to the other major matrix constituents. While matrix proteins have been suggested to provide many functions to the biofilm, only proteins that play a structural role have been characterized thus far. Here we identify proteins enriched in the matrix of P. aeruginosa biofilms. We then focused on a candidate matrix protein, the serine protease inhibitor ecotin (PA2755). This protein is able to inhibit neutrophil elastase, a bactericidal enzyme produced by the host immune system during P. aeruginosa biofilm infections. We show that ecotin binds to the key biofilm matrix exopolysaccharide Psl and that it can inhibit neutrophil elastase when associated with Psl. Finally, we show that ecotin protects both planktonic and biofilm P. aeruginosa cells from neutrophil elastase-mediated killing. This may represent a novel mechanism of protection for biofilms to increase their tolerance against the innate immune response. IMPORTANCE Proteins associated with the extracellular matrix of bacterial aggregates called biofilms have long been suggested to provide many important functions to the community. To date, however, only proteins that provide structural roles have been described, and few matrix-associated proteins have been identified. We developed a method to identify matrix proteins and characterized one. We show that this protein, when associated with the biofilm matrix, can inhibit a bactericidal enzyme produced by the immune system during infection and protect biofilm cells from death induced by the enzyme. This may represent a novel mechanism of protection for biofilms, further increasing their tolerance against the immune response. Together, our results are the first to show a nonstructural function for a confirmed matrix-interacting protein.Boo Shan TsengCourtney ReichhardtGennifer E. MerrihewSophia A. Araujo-HernandezJoe J. HarrisonMichael J. MacCossMatthew R. ParsekAmerican Society for MicrobiologyarticlePseudomonas aeruginosabiofilmsextracellular matrixMicrobiologyQR1-502ENmBio, Vol 9, Iss 2 (2018)
institution DOAJ
collection DOAJ
language EN
topic Pseudomonas aeruginosa
biofilms
extracellular matrix
Microbiology
QR1-502
spellingShingle Pseudomonas aeruginosa
biofilms
extracellular matrix
Microbiology
QR1-502
Boo Shan Tseng
Courtney Reichhardt
Gennifer E. Merrihew
Sophia A. Araujo-Hernandez
Joe J. Harrison
Michael J. MacCoss
Matthew R. Parsek
A Biofilm Matrix-Associated Protease Inhibitor Protects <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> from Proteolytic Attack
description ABSTRACT Pseudomonas aeruginosa produces an extracellular biofilm matrix that consists of nucleic acids, exopolysaccharides, lipid vesicles, and proteins. In general, the protein component of the biofilm matrix is poorly defined and understudied relative to the other major matrix constituents. While matrix proteins have been suggested to provide many functions to the biofilm, only proteins that play a structural role have been characterized thus far. Here we identify proteins enriched in the matrix of P. aeruginosa biofilms. We then focused on a candidate matrix protein, the serine protease inhibitor ecotin (PA2755). This protein is able to inhibit neutrophil elastase, a bactericidal enzyme produced by the host immune system during P. aeruginosa biofilm infections. We show that ecotin binds to the key biofilm matrix exopolysaccharide Psl and that it can inhibit neutrophil elastase when associated with Psl. Finally, we show that ecotin protects both planktonic and biofilm P. aeruginosa cells from neutrophil elastase-mediated killing. This may represent a novel mechanism of protection for biofilms to increase their tolerance against the innate immune response. IMPORTANCE Proteins associated with the extracellular matrix of bacterial aggregates called biofilms have long been suggested to provide many important functions to the community. To date, however, only proteins that provide structural roles have been described, and few matrix-associated proteins have been identified. We developed a method to identify matrix proteins and characterized one. We show that this protein, when associated with the biofilm matrix, can inhibit a bactericidal enzyme produced by the immune system during infection and protect biofilm cells from death induced by the enzyme. This may represent a novel mechanism of protection for biofilms, further increasing their tolerance against the immune response. Together, our results are the first to show a nonstructural function for a confirmed matrix-interacting protein.
format article
author Boo Shan Tseng
Courtney Reichhardt
Gennifer E. Merrihew
Sophia A. Araujo-Hernandez
Joe J. Harrison
Michael J. MacCoss
Matthew R. Parsek
author_facet Boo Shan Tseng
Courtney Reichhardt
Gennifer E. Merrihew
Sophia A. Araujo-Hernandez
Joe J. Harrison
Michael J. MacCoss
Matthew R. Parsek
author_sort Boo Shan Tseng
title A Biofilm Matrix-Associated Protease Inhibitor Protects <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> from Proteolytic Attack
title_short A Biofilm Matrix-Associated Protease Inhibitor Protects <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> from Proteolytic Attack
title_full A Biofilm Matrix-Associated Protease Inhibitor Protects <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> from Proteolytic Attack
title_fullStr A Biofilm Matrix-Associated Protease Inhibitor Protects <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> from Proteolytic Attack
title_full_unstemmed A Biofilm Matrix-Associated Protease Inhibitor Protects <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> from Proteolytic Attack
title_sort biofilm matrix-associated protease inhibitor protects <named-content content-type="genus-species">pseudomonas aeruginosa</named-content> from proteolytic attack
publisher American Society for Microbiology
publishDate 2018
url https://doaj.org/article/c73bbac4760e44f08cfcf26a00edf51a
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