Loss of social behaviours in populations of Pseudomonas aeruginosa infecting lungs of patients with cystic fibrosis.

Pseudomonas aeruginosa, is an opportunistic, bacterial pathogen causing persistent and frequently fatal infections of the lung in patients with cystic fibrosis. Isolates from chronic infections differ from laboratory and environmental strains in a range of traits and this is widely interpreted as th...

Full description

Bibliographic Details
Main Authors: Natalie Jiricny, Søren Molin, Kevin Foster, Stephen P Diggle, Pauline D Scanlan, Melanie Ghoul, Helle Krogh Johansen, Lorenzo A Santorelli, Roman Popat, Stuart A West, Ashleigh S Griffin
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2014-01-01
Series:PLoS ONE
Online Access:https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/24454693/?tool=EBI
_version_ 1818426210254848000
author Natalie Jiricny
Søren Molin
Kevin Foster
Stephen P Diggle
Pauline D Scanlan
Melanie Ghoul
Helle Krogh Johansen
Lorenzo A Santorelli
Roman Popat
Stuart A West
Ashleigh S Griffin
author_facet Natalie Jiricny
Søren Molin
Kevin Foster
Stephen P Diggle
Pauline D Scanlan
Melanie Ghoul
Helle Krogh Johansen
Lorenzo A Santorelli
Roman Popat
Stuart A West
Ashleigh S Griffin
author_sort Natalie Jiricny
collection DOAJ
description Pseudomonas aeruginosa, is an opportunistic, bacterial pathogen causing persistent and frequently fatal infections of the lung in patients with cystic fibrosis. Isolates from chronic infections differ from laboratory and environmental strains in a range of traits and this is widely interpreted as the result of adaptation to the lung environment. Typically, chronic strains carry mutations in global regulation factors that could effect reduced expression of social traits, raising the possibility that competitive dynamics between cooperative and selfish, cheating strains could also drive changes in P. aeruginosa infections. We compared the expression of cooperative traits - biofilm formation, secretion of exo-products and quorum sensing (QS) - in P. aeruginosa isolates that were estimated to have spent different lengths of time in the lung based on clinical information. All three exo-products involved in nutrient acquisition were produced in significantly smaller quantities with increased duration of infection, and patterns across four QS signal molecules were consistent with accumulation over time of mutations in lasR, which are known to disrupt the ability of cells to respond to QS signal. Pyocyanin production, and the proportion of cells in biofilm relative to motile, free-living cells in liquid culture, did not change. Overall, our results confirm that the loss of social behaviour is a consistent trend with time spent in the lung and suggest that social dynamics are potentially relevant to understanding the behaviour of P. aeruginosa in lung infections.
first_indexed 2024-12-14T14:26:12Z
format Article
id doaj.art-f91f498b41cd4b4c9bb09218f2299442
institution Directory Open Access Journal
issn 1932-6203
language English
last_indexed 2024-12-14T14:26:12Z
publishDate 2014-01-01
publisher Public Library of Science (PLoS)
record_format Article
series PLoS ONE
spelling doaj.art-f91f498b41cd4b4c9bb09218f22994422022-12-21T22:57:56ZengPublic Library of Science (PLoS)PLoS ONE1932-62032014-01-0191e8312410.1371/journal.pone.0083124Loss of social behaviours in populations of Pseudomonas aeruginosa infecting lungs of patients with cystic fibrosis.Natalie JiricnySøren MolinKevin FosterStephen P DigglePauline D ScanlanMelanie GhoulHelle Krogh JohansenLorenzo A SantorelliRoman PopatStuart A WestAshleigh S GriffinPseudomonas aeruginosa, is an opportunistic, bacterial pathogen causing persistent and frequently fatal infections of the lung in patients with cystic fibrosis. Isolates from chronic infections differ from laboratory and environmental strains in a range of traits and this is widely interpreted as the result of adaptation to the lung environment. Typically, chronic strains carry mutations in global regulation factors that could effect reduced expression of social traits, raising the possibility that competitive dynamics between cooperative and selfish, cheating strains could also drive changes in P. aeruginosa infections. We compared the expression of cooperative traits - biofilm formation, secretion of exo-products and quorum sensing (QS) - in P. aeruginosa isolates that were estimated to have spent different lengths of time in the lung based on clinical information. All three exo-products involved in nutrient acquisition were produced in significantly smaller quantities with increased duration of infection, and patterns across four QS signal molecules were consistent with accumulation over time of mutations in lasR, which are known to disrupt the ability of cells to respond to QS signal. Pyocyanin production, and the proportion of cells in biofilm relative to motile, free-living cells in liquid culture, did not change. Overall, our results confirm that the loss of social behaviour is a consistent trend with time spent in the lung and suggest that social dynamics are potentially relevant to understanding the behaviour of P. aeruginosa in lung infections.https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/24454693/?tool=EBI
spellingShingle Natalie Jiricny
Søren Molin
Kevin Foster
Stephen P Diggle
Pauline D Scanlan
Melanie Ghoul
Helle Krogh Johansen
Lorenzo A Santorelli
Roman Popat
Stuart A West
Ashleigh S Griffin
Loss of social behaviours in populations of Pseudomonas aeruginosa infecting lungs of patients with cystic fibrosis.
PLoS ONE
title Loss of social behaviours in populations of Pseudomonas aeruginosa infecting lungs of patients with cystic fibrosis.
title_full Loss of social behaviours in populations of Pseudomonas aeruginosa infecting lungs of patients with cystic fibrosis.
title_fullStr Loss of social behaviours in populations of Pseudomonas aeruginosa infecting lungs of patients with cystic fibrosis.
title_full_unstemmed Loss of social behaviours in populations of Pseudomonas aeruginosa infecting lungs of patients with cystic fibrosis.
title_short Loss of social behaviours in populations of Pseudomonas aeruginosa infecting lungs of patients with cystic fibrosis.
title_sort loss of social behaviours in populations of pseudomonas aeruginosa infecting lungs of patients with cystic fibrosis
url https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/24454693/?tool=EBI
work_keys_str_mv AT nataliejiricny lossofsocialbehavioursinpopulationsofpseudomonasaeruginosainfectinglungsofpatientswithcysticfibrosis
AT sørenmolin lossofsocialbehavioursinpopulationsofpseudomonasaeruginosainfectinglungsofpatientswithcysticfibrosis
AT kevinfoster lossofsocialbehavioursinpopulationsofpseudomonasaeruginosainfectinglungsofpatientswithcysticfibrosis
AT stephenpdiggle lossofsocialbehavioursinpopulationsofpseudomonasaeruginosainfectinglungsofpatientswithcysticfibrosis
AT paulinedscanlan lossofsocialbehavioursinpopulationsofpseudomonasaeruginosainfectinglungsofpatientswithcysticfibrosis
AT melanieghoul lossofsocialbehavioursinpopulationsofpseudomonasaeruginosainfectinglungsofpatientswithcysticfibrosis
AT hellekroghjohansen lossofsocialbehavioursinpopulationsofpseudomonasaeruginosainfectinglungsofpatientswithcysticfibrosis
AT lorenzoasantorelli lossofsocialbehavioursinpopulationsofpseudomonasaeruginosainfectinglungsofpatientswithcysticfibrosis
AT romanpopat lossofsocialbehavioursinpopulationsofpseudomonasaeruginosainfectinglungsofpatientswithcysticfibrosis
AT stuartawest lossofsocialbehavioursinpopulationsofpseudomonasaeruginosainfectinglungsofpatientswithcysticfibrosis
AT ashleighsgriffin lossofsocialbehavioursinpopulationsofpseudomonasaeruginosainfectinglungsofpatientswithcysticfibrosis