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Evolution of Quorum Sensing in <i>Pseudomonas aeruginosa</i> Can Occur via Loss of Function and Regulon Modulation


Jayakumar, Priyanikha; Figueiredo, Alexandre R T; Kümmerli, Rolf (2022). Evolution of Quorum Sensing in <i>Pseudomonas aeruginosa</i> Can Occur via Loss of Function and Regulon Modulation. mSystems, 7(5):e0035422.

Abstract

Pseudomonas aeruginosa populations evolving in cystic fibrosis lungs, animal hosts, natural environments and in vitro undergo extensive genetic adaption and diversification. A common mutational target is the quorum sensing (QS) system, a three-unit regulatory system that controls the expression of virulence factors and secreted public goods. Three evolutionary scenarios have been advocated to explain selection for QS mutants: (i) disuse of the regulon, (ii) cheating through the exploitation of public goods, or (ii) modulation of the QS regulon. Here, we examine these scenarios by studying a set of 61 QS mutants from an experimental evolution study. We observed nonsynonymous mutations in all three QS systems: Las, Rhl, and Pseudomonas Quinolone Signal (PQS). The majority of the Las mutants had large deletions of the Las regulon, resulting in loss of QS function and the inability to produce QS-regulated traits, thus supporting the first or second scenarios. Conversely, phenotypic and gene expression analyses of Rhl mutants support network modulation (third scenario), as these mutants overexpressed the Las and Rhl receptors and showed an altered QS-regulated trait production profile. PQS mutants also showed patterns of regulon modulation leading to strain diversification and phenotypic tradeoffs, where the upregulation of certain QS traits is associated with the downregulation of others. Overall, our results indicate that mutations in the different QS systems lead to diverging effects on the QS trait profile in P. aeruginosa populations. These mutations might not only affect the plasticity and diversity of evolved populations but could also impact bacterial fitness and virulence in infections.

Abstract

Pseudomonas aeruginosa populations evolving in cystic fibrosis lungs, animal hosts, natural environments and in vitro undergo extensive genetic adaption and diversification. A common mutational target is the quorum sensing (QS) system, a three-unit regulatory system that controls the expression of virulence factors and secreted public goods. Three evolutionary scenarios have been advocated to explain selection for QS mutants: (i) disuse of the regulon, (ii) cheating through the exploitation of public goods, or (ii) modulation of the QS regulon. Here, we examine these scenarios by studying a set of 61 QS mutants from an experimental evolution study. We observed nonsynonymous mutations in all three QS systems: Las, Rhl, and Pseudomonas Quinolone Signal (PQS). The majority of the Las mutants had large deletions of the Las regulon, resulting in loss of QS function and the inability to produce QS-regulated traits, thus supporting the first or second scenarios. Conversely, phenotypic and gene expression analyses of Rhl mutants support network modulation (third scenario), as these mutants overexpressed the Las and Rhl receptors and showed an altered QS-regulated trait production profile. PQS mutants also showed patterns of regulon modulation leading to strain diversification and phenotypic tradeoffs, where the upregulation of certain QS traits is associated with the downregulation of others. Overall, our results indicate that mutations in the different QS systems lead to diverging effects on the QS trait profile in P. aeruginosa populations. These mutations might not only affect the plasticity and diversity of evolved populations but could also impact bacterial fitness and virulence in infections.

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Item Type:Journal Article, refereed, original work
Communities & Collections:07 Faculty of Science > Department of Quantitative Biomedicine
Dewey Decimal Classification:610 Medicine & health
Scopus Subject Areas:Life Sciences > Microbiology
Life Sciences > Physiology
Life Sciences > Biochemistry
Life Sciences > Ecology, Evolution, Behavior and Systematics
Physical Sciences > Modeling and Simulation
Life Sciences > Molecular Biology
Life Sciences > Genetics
Physical Sciences > Computer Science Applications
Uncontrolled Keywords:Computer Science Applications, Genetics, Molecular Biology, Modeling and Simulation, Ecology, Evolution, Behavior and Systematics, Biochemistry, Physiology, Microbiology
Language:English
Date:26 October 2022
Deposited On:07 Feb 2023 18:50
Last Modified:28 Feb 2024 02:46
Publisher:American Society for Microbiology
ISSN:2379-5077
OA Status:Gold
Free access at:PubMed ID. An embargo period may apply.
Publisher DOI:https://doi.org/10.1128/msystems.00354-22
PubMed ID:36190124
Project Information:
  • : FunderH2020
  • : Grant ID681295
  • : Project TitleBactInd - Bacterial cooperation at the individual cell level
  • : FunderUniversity Research Priority Program
  • : Grant ID
  • : Project Title
  • Content: Published Version
  • Language: English
  • Licence: Creative Commons: Attribution 4.0 International (CC BY 4.0)