Selection of Functional Quorum Sensing Systems by Lysogenic Bacteriophages in Pseudomonas aeruginosa

Quorum sensing (QS) in Pseudomonas aeruginosa coordinates the expression of virulence factors, some of which are used as public goods. Since their production is a cooperative behavior, it is susceptible to social cheating in which non-cooperative QS deficient mutants use the resources without invest...

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Main Authors: Miguel A. Saucedo-Mora, Paulina Castañeda-Tamez, Adrián Cazares, Judith Pérez-Velázquez, Burkhard A. Hense, Daniel Cazares, Wendy Figueroa, Marco Carballo, Gabriel Guarneros, Berenice Pérez-Eretza, Nelby Cruz, Yoshito Nishiyama, Toshinari Maeda, Javier A. Belmont-Díaz, Thomas K. Wood, Rodolfo García-Contreras
Format: Article
Language:English
Published: Frontiers Media S.A. 2017-08-01
Series:Frontiers in Microbiology
Subjects:
Online Access:http://journal.frontiersin.org/article/10.3389/fmicb.2017.01669/full
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author Miguel A. Saucedo-Mora
Paulina Castañeda-Tamez
Adrián Cazares
Judith Pérez-Velázquez
Judith Pérez-Velázquez
Burkhard A. Hense
Daniel Cazares
Wendy Figueroa
Marco Carballo
Gabriel Guarneros
Berenice Pérez-Eretza
Nelby Cruz
Yoshito Nishiyama
Toshinari Maeda
Javier A. Belmont-Díaz
Thomas K. Wood
Rodolfo García-Contreras
author_facet Miguel A. Saucedo-Mora
Paulina Castañeda-Tamez
Adrián Cazares
Judith Pérez-Velázquez
Judith Pérez-Velázquez
Burkhard A. Hense
Daniel Cazares
Wendy Figueroa
Marco Carballo
Gabriel Guarneros
Berenice Pérez-Eretza
Nelby Cruz
Yoshito Nishiyama
Toshinari Maeda
Javier A. Belmont-Díaz
Thomas K. Wood
Rodolfo García-Contreras
author_sort Miguel A. Saucedo-Mora
collection DOAJ
description Quorum sensing (QS) in Pseudomonas aeruginosa coordinates the expression of virulence factors, some of which are used as public goods. Since their production is a cooperative behavior, it is susceptible to social cheating in which non-cooperative QS deficient mutants use the resources without investing in their production. Nevertheless, functional QS systems are abundant; hence, mechanisms regulating the amount of cheating should exist. Evidence that demonstrates a tight relationship between QS and the susceptibility of bacteria against the attack of lytic phages is increasing; nevertheless, the relationship between temperate phages and QS has been much less explored. Therefore, in this work, we studied the effects of having a functional QS system on the susceptibility to temperate bacteriophages and how this affects the bacterial and phage dynamics. We find that both experimentally and using mathematical models, that the lysogenic bacteriophages D3112 and JBD30 select QS-proficient P. aeruginosa phenotypes as compared to the QS-deficient mutants during competition experiments with mixed strain populations in vitro and in vivo in Galleria mellonella, in spite of the fact that both phages replicate better in the wild-type background. We show that this phenomenon restricts social cheating, and we propose that temperate phages may constitute an important selective pressure toward the conservation of bacterial QS.
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spelling doaj.art-66c04e7eb65b4ebc95ecade403fbc8d82022-12-22T00:59:10ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2017-08-01810.3389/fmicb.2017.01669289331Selection of Functional Quorum Sensing Systems by Lysogenic Bacteriophages in Pseudomonas aeruginosaMiguel A. Saucedo-Mora0Paulina Castañeda-Tamez1Adrián Cazares2Judith Pérez-Velázquez3Judith Pérez-Velázquez4Burkhard A. Hense5Daniel Cazares6Wendy Figueroa7Marco Carballo8Gabriel Guarneros9Berenice Pérez-Eretza10Nelby Cruz11Yoshito Nishiyama12Toshinari Maeda13Javier A. Belmont-Díaz14Thomas K. Wood15Rodolfo García-Contreras16Department of Microbiology and Parasitology, Faculty of Medicine, National Autonomous University of MexicoMexico City, MexicoDepartment of Microbiology and Parasitology, Faculty of Medicine, National Autonomous University of MexicoMexico City, MexicoDepartamento de Genética y Biología Molecular, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico NacionalMexico City, MexicoInstitute of Computational Biology, Helmholtz Zentrum München, Deutsches Forschungszentrum für Gesundheit und Umwelt (GmbH)Neuherberg, GermanyMathematical Modeling of Biological Systems, Zentrum Mathematik, Technical University of MunichGarching, GermanyInstitute of Computational Biology, Helmholtz Zentrum München, Deutsches Forschungszentrum für Gesundheit und Umwelt (GmbH)Neuherberg, GermanyCentro de Ciencias Genomicas, National Autonomous University of MexicoCuernavaca, MexicoDepartamento de Genética y Biología Molecular, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico NacionalMexico City, MexicoDepartamento de Genética y Biología Molecular, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico NacionalMexico City, MexicoDepartamento de Genética y Biología Molecular, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico NacionalMexico City, MexicoDepartment of Microbiology and Parasitology, Faculty of Medicine, National Autonomous University of MexicoMexico City, MexicoDepartamento de Genética y Biología Molecular, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico NacionalMexico City, MexicoDepartment of Biological Functions Engineering, Kyushu Institute of TechnologyKitakyushu, JapanDepartment of Biological Functions Engineering, Kyushu Institute of TechnologyKitakyushu, JapanDepartamento de Bioquímica, Instituto Nacional de CardiologíaMexico City, MexicoDepartment of Biochemistry and Molecular Biology, Pennsylvania State University, University ParkPA, United StatesDepartment of Microbiology and Parasitology, Faculty of Medicine, National Autonomous University of MexicoMexico City, MexicoQuorum sensing (QS) in Pseudomonas aeruginosa coordinates the expression of virulence factors, some of which are used as public goods. Since their production is a cooperative behavior, it is susceptible to social cheating in which non-cooperative QS deficient mutants use the resources without investing in their production. Nevertheless, functional QS systems are abundant; hence, mechanisms regulating the amount of cheating should exist. Evidence that demonstrates a tight relationship between QS and the susceptibility of bacteria against the attack of lytic phages is increasing; nevertheless, the relationship between temperate phages and QS has been much less explored. Therefore, in this work, we studied the effects of having a functional QS system on the susceptibility to temperate bacteriophages and how this affects the bacterial and phage dynamics. We find that both experimentally and using mathematical models, that the lysogenic bacteriophages D3112 and JBD30 select QS-proficient P. aeruginosa phenotypes as compared to the QS-deficient mutants during competition experiments with mixed strain populations in vitro and in vivo in Galleria mellonella, in spite of the fact that both phages replicate better in the wild-type background. We show that this phenomenon restricts social cheating, and we propose that temperate phages may constitute an important selective pressure toward the conservation of bacterial QS.http://journal.frontiersin.org/article/10.3389/fmicb.2017.01669/fullpublic goodssocial cheatingphage therapyquorum sensingvirulence
spellingShingle Miguel A. Saucedo-Mora
Paulina Castañeda-Tamez
Adrián Cazares
Judith Pérez-Velázquez
Judith Pérez-Velázquez
Burkhard A. Hense
Daniel Cazares
Wendy Figueroa
Marco Carballo
Gabriel Guarneros
Berenice Pérez-Eretza
Nelby Cruz
Yoshito Nishiyama
Toshinari Maeda
Javier A. Belmont-Díaz
Thomas K. Wood
Rodolfo García-Contreras
Selection of Functional Quorum Sensing Systems by Lysogenic Bacteriophages in Pseudomonas aeruginosa
Frontiers in Microbiology
public goods
social cheating
phage therapy
quorum sensing
virulence
title Selection of Functional Quorum Sensing Systems by Lysogenic Bacteriophages in Pseudomonas aeruginosa
title_full Selection of Functional Quorum Sensing Systems by Lysogenic Bacteriophages in Pseudomonas aeruginosa
title_fullStr Selection of Functional Quorum Sensing Systems by Lysogenic Bacteriophages in Pseudomonas aeruginosa
title_full_unstemmed Selection of Functional Quorum Sensing Systems by Lysogenic Bacteriophages in Pseudomonas aeruginosa
title_short Selection of Functional Quorum Sensing Systems by Lysogenic Bacteriophages in Pseudomonas aeruginosa
title_sort selection of functional quorum sensing systems by lysogenic bacteriophages in pseudomonas aeruginosa
topic public goods
social cheating
phage therapy
quorum sensing
virulence
url http://journal.frontiersin.org/article/10.3389/fmicb.2017.01669/full
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