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The structural role of bacterial eDNA in the formation of biofilm streamers

Across diverse habitats, bacteria are mainly found as biofilms, surface-attached communities embedded in a self-secreted matrix of extracellular polymeric substances (EPS), which enhance bacterial recalcitrance to antimicrobial treatment and mechanical stresses. In the presence of flow and geometric...

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Autores principales: Secchi, Eleonora, Savorana, Giovanni, Vitale, Alessandra, Eberl, Leo, Stocker, Roman, Rusconi, Roberto
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8944759/
https://www.ncbi.nlm.nih.gov/pubmed/35290120
http://dx.doi.org/10.1073/pnas.2113723119
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author Secchi, Eleonora
Savorana, Giovanni
Vitale, Alessandra
Eberl, Leo
Stocker, Roman
Rusconi, Roberto
author_facet Secchi, Eleonora
Savorana, Giovanni
Vitale, Alessandra
Eberl, Leo
Stocker, Roman
Rusconi, Roberto
author_sort Secchi, Eleonora
collection PubMed
description Across diverse habitats, bacteria are mainly found as biofilms, surface-attached communities embedded in a self-secreted matrix of extracellular polymeric substances (EPS), which enhance bacterial recalcitrance to antimicrobial treatment and mechanical stresses. In the presence of flow and geometric constraints such as corners or constrictions, biofilms can take the form of long, suspended filaments (streamers), which bear important consequences in industrial and clinical settings by causing clogging and fouling. The formation of streamers is thought to be driven by the viscoelastic nature of the biofilm matrix. Yet, little is known about the structural composition of streamers and how it affects their mechanical properties. Here, using a microfluidic platform that allows growing and precisely examining biofilm streamers, we show that extracellular DNA (eDNA) constitutes the backbone and is essential for the mechanical stability of Pseudomonas aeruginosa streamers. This finding is supported by the observations that DNA-degrading enzymes prevent the formation of streamers and clear already formed ones and that the antibiotic ciprofloxacin promotes their formation by increasing the release of eDNA. Furthermore, using mutants for the production of the exopolysaccharide Pel, an important component of P. aeruginosa EPS, we reveal an concurring role of Pel in tuning the mechanical properties of the streamers. Taken together, these results highlight the importance of eDNA and of its interplay with Pel in determining the mechanical properties of P. aeruginosa streamers and suggest that targeting the composition of streamers can be an effective approach to control the formation of these biofilm structures.
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spelling pubmed-89447592022-09-15 The structural role of bacterial eDNA in the formation of biofilm streamers Secchi, Eleonora Savorana, Giovanni Vitale, Alessandra Eberl, Leo Stocker, Roman Rusconi, Roberto Proc Natl Acad Sci U S A Physical Sciences Across diverse habitats, bacteria are mainly found as biofilms, surface-attached communities embedded in a self-secreted matrix of extracellular polymeric substances (EPS), which enhance bacterial recalcitrance to antimicrobial treatment and mechanical stresses. In the presence of flow and geometric constraints such as corners or constrictions, biofilms can take the form of long, suspended filaments (streamers), which bear important consequences in industrial and clinical settings by causing clogging and fouling. The formation of streamers is thought to be driven by the viscoelastic nature of the biofilm matrix. Yet, little is known about the structural composition of streamers and how it affects their mechanical properties. Here, using a microfluidic platform that allows growing and precisely examining biofilm streamers, we show that extracellular DNA (eDNA) constitutes the backbone and is essential for the mechanical stability of Pseudomonas aeruginosa streamers. This finding is supported by the observations that DNA-degrading enzymes prevent the formation of streamers and clear already formed ones and that the antibiotic ciprofloxacin promotes their formation by increasing the release of eDNA. Furthermore, using mutants for the production of the exopolysaccharide Pel, an important component of P. aeruginosa EPS, we reveal an concurring role of Pel in tuning the mechanical properties of the streamers. Taken together, these results highlight the importance of eDNA and of its interplay with Pel in determining the mechanical properties of P. aeruginosa streamers and suggest that targeting the composition of streamers can be an effective approach to control the formation of these biofilm structures. National Academy of Sciences 2022-03-15 2022-03-22 /pmc/articles/PMC8944759/ /pubmed/35290120 http://dx.doi.org/10.1073/pnas.2113723119 Text en Copyright © 2022 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Physical Sciences
Secchi, Eleonora
Savorana, Giovanni
Vitale, Alessandra
Eberl, Leo
Stocker, Roman
Rusconi, Roberto
The structural role of bacterial eDNA in the formation of biofilm streamers
title The structural role of bacterial eDNA in the formation of biofilm streamers
title_full The structural role of bacterial eDNA in the formation of biofilm streamers
title_fullStr The structural role of bacterial eDNA in the formation of biofilm streamers
title_full_unstemmed The structural role of bacterial eDNA in the formation of biofilm streamers
title_short The structural role of bacterial eDNA in the formation of biofilm streamers
title_sort structural role of bacterial edna in the formation of biofilm streamers
topic Physical Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8944759/
https://www.ncbi.nlm.nih.gov/pubmed/35290120
http://dx.doi.org/10.1073/pnas.2113723119
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