Competition in Biofilms between Cystic Fibrosis Isolates of <italic toggle="yes">Pseudomonas aeruginosa</italic> Is Shaped by R-Pyocins

ABSTRACT Pseudomonas aeruginosa is an opportunistic pathogen and the leading cause of morbidity and mortality in cystic fibrosis (CF) patients. P. aeruginosa infections are difficult to treat due to a number of antibiotic resistance mechanisms and the organism’s propensity to form multicellular biof...

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Autores principales:	Olubukola Oluyombo, Christopher N. Penfold, Stephen P. Diggle
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	Pseudomonas aeruginosa bacteriocins biofilms cystic fibrosis pyocins Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/6136d509776247da8609f2a3de51967f
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spelling	oai:doaj.org-article:6136d509776247da8609f2a3de51967f2021-11-15T15:55:14ZCompetition in Biofilms between Cystic Fibrosis Isolates of <italic toggle="yes">Pseudomonas aeruginosa</italic> Is Shaped by R-Pyocins10.1128/mBio.01828-182150-7511https://doaj.org/article/6136d509776247da8609f2a3de51967f2019-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01828-18https://doaj.org/toc/2150-7511ABSTRACT Pseudomonas aeruginosa is an opportunistic pathogen and the leading cause of morbidity and mortality in cystic fibrosis (CF) patients. P. aeruginosa infections are difficult to treat due to a number of antibiotic resistance mechanisms and the organism’s propensity to form multicellular biofilms. Epidemic strains of P. aeruginosa often dominate within the lungs of individual CF patients, but how they achieve this is poorly understood. One way that strains of P. aeruginosa can compete is by producing chromosomally encoded bacteriocins, called pyocins. Three major classes of pyocin have been identified in P. aeruginosa: soluble pyocins (S types) and tailocins (R and F types). In this study, we investigated the distribution of S- and R-type pyocins in 24 clinical strains isolated from individual CF patients and then focused on understanding their roles in interstrain competition. We found that (i) each strain produced only one R-pyocin type, but the number of S-pyocins varied between strains, (ii) R-pyocins were generally important for strain dominance during competition assays in planktonic cultures and biofilm communities in strains with both disparate R- and S-pyocin subtypes, and (iii) purified R-pyocins demonstrated significant antimicrobial activity against established biofilms. Our work provides support for a role played by R-pyocins in the competition between P. aeruginosa strains and helps explain why certain strains and lineages of P. aeruginosa dominate and displace others during CF infection. Furthermore, we demonstrate the potential of exploiting R-pyocins for therapeutic gains in an era when antibiotic resistance is a global concern. IMPORTANCE A major clinical problem caused by Pseudomonas aeruginosa, is chronic biofilm infection of the lungs in individuals with cystic fibrosis (CF). Epidemic P. aeruginosa strains dominate and displace others during CF infection, but these intraspecies interactions remain poorly understood. Here we demonstrate that R-pyocins (bacteriocins) are important factors in driving competitive interactions in biofilms between P. aeruginosa strains isolated from different CF patients. In addition, we found that these phage-like pyocins are inhibitory against mature biofilms of susceptible strains. This highlights the potential of R-pyocins as antimicrobial and antibiofilm agents at a time when new antimicrobial therapies are desperately needed.Olubukola OluyomboChristopher N. PenfoldStephen P. DiggleAmerican Society for MicrobiologyarticlePseudomonas aeruginosabacteriocinsbiofilmscystic fibrosispyocinsMicrobiologyQR1-502ENmBio, Vol 10, Iss 1 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	Pseudomonas aeruginosa bacteriocins biofilms cystic fibrosis pyocins Microbiology QR1-502
spellingShingle	Pseudomonas aeruginosa bacteriocins biofilms cystic fibrosis pyocins Microbiology QR1-502 Olubukola Oluyombo Christopher N. Penfold Stephen P. Diggle Competition in Biofilms between Cystic Fibrosis Isolates of <italic toggle="yes">Pseudomonas aeruginosa</italic> Is Shaped by R-Pyocins
description	ABSTRACT Pseudomonas aeruginosa is an opportunistic pathogen and the leading cause of morbidity and mortality in cystic fibrosis (CF) patients. P. aeruginosa infections are difficult to treat due to a number of antibiotic resistance mechanisms and the organism’s propensity to form multicellular biofilms. Epidemic strains of P. aeruginosa often dominate within the lungs of individual CF patients, but how they achieve this is poorly understood. One way that strains of P. aeruginosa can compete is by producing chromosomally encoded bacteriocins, called pyocins. Three major classes of pyocin have been identified in P. aeruginosa: soluble pyocins (S types) and tailocins (R and F types). In this study, we investigated the distribution of S- and R-type pyocins in 24 clinical strains isolated from individual CF patients and then focused on understanding their roles in interstrain competition. We found that (i) each strain produced only one R-pyocin type, but the number of S-pyocins varied between strains, (ii) R-pyocins were generally important for strain dominance during competition assays in planktonic cultures and biofilm communities in strains with both disparate R- and S-pyocin subtypes, and (iii) purified R-pyocins demonstrated significant antimicrobial activity against established biofilms. Our work provides support for a role played by R-pyocins in the competition between P. aeruginosa strains and helps explain why certain strains and lineages of P. aeruginosa dominate and displace others during CF infection. Furthermore, we demonstrate the potential of exploiting R-pyocins for therapeutic gains in an era when antibiotic resistance is a global concern. IMPORTANCE A major clinical problem caused by Pseudomonas aeruginosa, is chronic biofilm infection of the lungs in individuals with cystic fibrosis (CF). Epidemic P. aeruginosa strains dominate and displace others during CF infection, but these intraspecies interactions remain poorly understood. Here we demonstrate that R-pyocins (bacteriocins) are important factors in driving competitive interactions in biofilms between P. aeruginosa strains isolated from different CF patients. In addition, we found that these phage-like pyocins are inhibitory against mature biofilms of susceptible strains. This highlights the potential of R-pyocins as antimicrobial and antibiofilm agents at a time when new antimicrobial therapies are desperately needed.
format	article
author	Olubukola Oluyombo Christopher N. Penfold Stephen P. Diggle
author_facet	Olubukola Oluyombo Christopher N. Penfold Stephen P. Diggle
author_sort	Olubukola Oluyombo
title	Competition in Biofilms between Cystic Fibrosis Isolates of <italic toggle="yes">Pseudomonas aeruginosa</italic> Is Shaped by R-Pyocins
title_short	Competition in Biofilms between Cystic Fibrosis Isolates of <italic toggle="yes">Pseudomonas aeruginosa</italic> Is Shaped by R-Pyocins
title_full	Competition in Biofilms between Cystic Fibrosis Isolates of <italic toggle="yes">Pseudomonas aeruginosa</italic> Is Shaped by R-Pyocins
title_fullStr	Competition in Biofilms between Cystic Fibrosis Isolates of <italic toggle="yes">Pseudomonas aeruginosa</italic> Is Shaped by R-Pyocins
title_full_unstemmed	Competition in Biofilms between Cystic Fibrosis Isolates of <italic toggle="yes">Pseudomonas aeruginosa</italic> Is Shaped by R-Pyocins
title_sort	competition in biofilms between cystic fibrosis isolates of <italic toggle="yes">pseudomonas aeruginosa</italic> is shaped by r-pyocins
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/6136d509776247da8609f2a3de51967f
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Competition in Biofilms between Cystic Fibrosis Isolates of <italic toggle="yes">Pseudomonas aeruginosa</italic> Is Shaped by R-Pyocins

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