Abstract

Pel exopolysaccharide biosynthetic loci are phylogenetically widespread biofilm matrix determinants in bacteria. In Pseudomonas aeruginosa, Pel is crucial for cell-to-cell interactions and reducing susceptibility to antibiotic and mucolytic treatments. While genes encoding glycoside hydrolases have long been linked to biofilm exopolysaccharide biosynthesis, their physiological role in biofilm development is unclear. Here we demonstrate that the glycoside hydrolase activity of P. aeruginosa PelA decreases adherent biofilm biomass and is responsible for generating the low molecular weight secreted form of the Pel exopolysaccharide. We show that the generation of secreted Pel contributes to the biomechanical properties of the biofilm and decreases the virulence of P. aeruginosa in Caenorhabditis elegans and Drosophila melanogaster. Our results reveal that glycoside hydrolases found in exopolysaccharide biosynthetic systems can help shape the soft matter attributes of a biofilm and propose that secreted matrix components be referred to as matrix associated to better reflect their influence.

Details

Title
Glycoside hydrolase processing of the Pel polysaccharide alters biofilm biomechanics and Pseudomonas aeruginosa virulence
Author
Razvi, Erum 1   VIAFID ORCID Logo  ; Whitfield, Gregory B. 2   VIAFID ORCID Logo  ; Reichhardt, Courtney 3 ; Dreifus, Julia E. 4 ; Willis, Alexandra R. 5 ; Gluscencova, Oxana B. 6 ; Gloag, Erin S. 7   VIAFID ORCID Logo  ; Awad, Tarek S. 8 ; Rich, Jacquelyn D. 9 ; da Silva, Daniel Passos 10 ; Bond, Whitney 4   VIAFID ORCID Logo  ; Le Mauff, François 11   VIAFID ORCID Logo  ; Sheppard, Donald C. 11   VIAFID ORCID Logo  ; Hatton, Benjamin D. 8   VIAFID ORCID Logo  ; Stoodley, Paul 12   VIAFID ORCID Logo  ; Reinke, Aaron W. 5   VIAFID ORCID Logo  ; Boulianne, Gabrielle L. 13 ; Wozniak, Daniel J. 14 ; Harrison, Joe J. 9   VIAFID ORCID Logo  ; Parsek, Matthew R. 4 ; Howell, P. Lynne 1   VIAFID ORCID Logo 

 The Hospital for Sick Children, Program in Molecular Medicine, Toronto, Canada (GRID:grid.42327.30) (ISNI:0000 0004 0473 9646); University of Toronto, Department of Biochemistry, Toronto, Canada (GRID:grid.17063.33) (ISNI:0000 0001 2157 2938) 
 The Hospital for Sick Children, Program in Molecular Medicine, Toronto, Canada (GRID:grid.42327.30) (ISNI:0000 0004 0473 9646); University of Toronto, Department of Biochemistry, Toronto, Canada (GRID:grid.17063.33) (ISNI:0000 0001 2157 2938); Faculté de Médecine Université de Montréal, Département de Microbiologie, Infectiologie, et Immunologie, Montréal, Canada (GRID:grid.14848.31) (ISNI:0000 0001 2292 3357) 
 University of Washington, Department of Microbiology, Seattle, USA (GRID:grid.34477.33) (ISNI:0000000122986657); Washington University, Department of Chemistry, St. Louis, USA (GRID:grid.4367.6) (ISNI:0000 0001 2355 7002) 
 University of Washington, Department of Microbiology, Seattle, USA (GRID:grid.34477.33) (ISNI:0000000122986657) 
 University of Toronto, Department of Molecular Genetics, Toronto, Canada (GRID:grid.17063.33) (ISNI:0000 0001 2157 2938) 
 The Hospital for Sick Children, Program in Developmental and Stem Cell Biology, Toronto, Canada (GRID:grid.42327.30) (ISNI:0000 0004 0473 9646) 
 The Ohio State University, Department of Microbial Infection and Immunity, Columbus, USA (GRID:grid.261331.4) (ISNI:0000 0001 2285 7943); VA-MD College of Veterinary Medicine, Department of Biomedical Sciences and Pathobiology, Virginia Tech, USA (GRID:grid.470073.7) (ISNI:0000 0001 2178 7701) 
 University of Toronto, Department of Materials Science and Engineering, Toronto, Canada (GRID:grid.17063.33) (ISNI:0000 0001 2157 2938) 
 University of Calgary, Department of Biological Sciences, Calgary, Canada (GRID:grid.22072.35) (ISNI:0000 0004 1936 7697) 
10  University of Washington, Department of Microbiology, Seattle, USA (GRID:grid.34477.33) (ISNI:0000000122986657); BioVectra Inc. 11 Aviation, Charlottetown, Canada (GRID:grid.34477.33) 
11  McGill University, Department of Microbiology and Immunology, Faculty of Medicine, Montreal, Canada (GRID:grid.14709.3b) (ISNI:0000 0004 1936 8649); Research Institute of the McGill University Health Centre, Infectious Disease and Immunity in Global Health, Montreal, Canada (GRID:grid.63984.30) (ISNI:0000 0000 9064 4811); McGill Interdisciplinary Initiative in Infection and Immunity, Montreal, Canada (GRID:grid.63984.30) 
12  The Ohio State University, Department of Microbial Infection and Immunity, Columbus, USA (GRID:grid.261331.4) (ISNI:0000 0001 2285 7943); The Ohio State University, Department of Orthopedics, Columbus, USA (GRID:grid.261331.4) (ISNI:0000 0001 2285 7943); University of Southampton, National Biofilm Innovation Centre (NBIC) and National Centre for Advanced Tribology at Southampton (nCATS), Southampton, UK (GRID:grid.5491.9) (ISNI:0000 0004 1936 9297); The Ohio State University, Department of Microbiology, Columbus, USA (GRID:grid.261331.4) (ISNI:0000 0001 2285 7943) 
13  University of Toronto, Department of Molecular Genetics, Toronto, Canada (GRID:grid.17063.33) (ISNI:0000 0001 2157 2938); The Hospital for Sick Children, Program in Developmental and Stem Cell Biology, Toronto, Canada (GRID:grid.42327.30) (ISNI:0000 0004 0473 9646) 
14  The Ohio State University, Department of Microbial Infection and Immunity, Columbus, USA (GRID:grid.261331.4) (ISNI:0000 0001 2285 7943); The Ohio State University, Department of Microbiology, Columbus, USA (GRID:grid.261331.4) (ISNI:0000 0001 2285 7943) 
Pages
7
Publication year
2023
Publication date
2023
Publisher
Nature Publishing Group
e-ISSN
20555008
Source type
Scholarly Journal
Language of publication
English
ProQuest document ID
2771822268
Copyright
© The Author(s) 2023. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.