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Role of the flagellar hook in the structural development and antibiotic tolerance of Pseudomonas aeruginosa biofilms

Role of the flagellar hook in the structural development and antibiotic tolerance of Pseudomonas aeruginosa biofilms
Role of the flagellar hook in the structural development and antibiotic tolerance of Pseudomonas aeruginosa biofilms
Pseudomonas aeruginosa biofilms exhibit an intrinsic resistance to antibiotics and constitute a considerable clinical threat. In cystic fibrosis, a common feature of biofilms formed by P. aeruginosa in the airway is the occurrence of mutants deficient in flagellar motility. This study investigates the impact of flagellum deletion on the structure and antibiotic tolerance of P. aeruginosa biofilms, and highlights a role for the flagellum in adaptation and cell survival during biofilm development. Mutations in the flagellar hook protein FlgE influence greatly P. aeruginosa biofilm structuring and antibiotic tolerance. Phenotypic analysis of the flgE knockout mutant compared to the wild type (WT) reveal increased fitness under planktonic conditions, reduced initial adhesion but enhanced formation of microcolony aggregates in a microfluidic environment, and decreased expression of genes involved in exopolysaccharide formation. Biofilm cells of the flgE knock-out mutant display enhanced tolerance towards multiple antibiotics, whereas its planktonic cells show similar resistance to the WT. Confocal microscopy of biofilms demonstrates that gentamicin does not affect the viability of cells located in the inner part of the flgE knock-out mutant biofilms due to reduced penetration. These findings suggest that deficiency in flagellar proteins like FlgE in biofilms and in cystic fibrosis infections represent phenotypic and evolutionary adaptations that alter the structure of P. aeruginosa biofilms conferring increased antibiotic tolerance.
1751-7362
Valentin, Jules D.P.
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Straub, Hervé
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Pietsch, Franziska
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Lemare, Marion
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Ahrens, Christian H.
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Schreiber, Frank
996cc9b1-c439-4fae-8a46-43b94608d034
Webb, Jeremy
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Van der Mei, Henny C.
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Ren, Qun
fdc42b84-e0e0-4626-b7dd-0bd1d25619bf
Valentin, Jules D.P.
63941168-7e62-40a5-8ec8-c2053974ea12
Straub, Hervé
9e8235fd-65e9-4f96-91e8-f172f9f2f3d9
Pietsch, Franziska
0f11350d-36dd-4046-80f0-506593c97816
Lemare, Marion
e58ead6b-fb2b-4078-a637-7228e1b6183e
Ahrens, Christian H.
70789dbf-86c6-4725-beca-8dfa4b4e1323
Schreiber, Frank
996cc9b1-c439-4fae-8a46-43b94608d034
Webb, Jeremy
ec0a5c4e-86cc-4ae9-b390-7298f5d65f8d
Van der Mei, Henny C.
41a13fec-7b1c-41ce-b765-a53e30030662
Ren, Qun
fdc42b84-e0e0-4626-b7dd-0bd1d25619bf

Valentin, Jules D.P., Straub, Hervé, Pietsch, Franziska, Lemare, Marion, Ahrens, Christian H., Schreiber, Frank, Webb, Jeremy, Van der Mei, Henny C. and Ren, Qun (2021) Role of the flagellar hook in the structural development and antibiotic tolerance of Pseudomonas aeruginosa biofilms. The ISME Journal. (doi:10.1038/s41396-021-01157-9).

Record type: Article

Abstract

Pseudomonas aeruginosa biofilms exhibit an intrinsic resistance to antibiotics and constitute a considerable clinical threat. In cystic fibrosis, a common feature of biofilms formed by P. aeruginosa in the airway is the occurrence of mutants deficient in flagellar motility. This study investigates the impact of flagellum deletion on the structure and antibiotic tolerance of P. aeruginosa biofilms, and highlights a role for the flagellum in adaptation and cell survival during biofilm development. Mutations in the flagellar hook protein FlgE influence greatly P. aeruginosa biofilm structuring and antibiotic tolerance. Phenotypic analysis of the flgE knockout mutant compared to the wild type (WT) reveal increased fitness under planktonic conditions, reduced initial adhesion but enhanced formation of microcolony aggregates in a microfluidic environment, and decreased expression of genes involved in exopolysaccharide formation. Biofilm cells of the flgE knock-out mutant display enhanced tolerance towards multiple antibiotics, whereas its planktonic cells show similar resistance to the WT. Confocal microscopy of biofilms demonstrates that gentamicin does not affect the viability of cells located in the inner part of the flgE knock-out mutant biofilms due to reduced penetration. These findings suggest that deficiency in flagellar proteins like FlgE in biofilms and in cystic fibrosis infections represent phenotypic and evolutionary adaptations that alter the structure of P. aeruginosa biofilms conferring increased antibiotic tolerance.

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Accepted/In Press date: 16 November 2021
Published date: 8 December 2021

Identifiers

Local EPrints ID: 454762
URI: http://eprints.soton.ac.uk/id/eprint/454762
ISSN: 1751-7362
PURE UUID: f0434bd2-8b9e-4c35-ae9a-5d10cd54db5b
ORCID for Jeremy Webb: ORCID iD orcid.org/0000-0003-2068-8589

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Date deposited: 22 Feb 2022 17:42
Last modified: 17 Mar 2024 03:08

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Contributors

Author: Jules D.P. Valentin
Author: Hervé Straub
Author: Franziska Pietsch
Author: Marion Lemare
Author: Christian H. Ahrens
Author: Frank Schreiber
Author: Jeremy Webb ORCID iD
Author: Henny C. Van der Mei
Author: Qun Ren

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