Challenging the paradigm: non-canonical exoprotease cheating in clinical <i>Pseudomonas aeruginosa</i> isolates

Pseudomonas aeruginosa is a model organism for studying social behaviors in bacteria, such as the exploitation of exoprotease by social cheaters. The current paradigm holds that continuous culture of exoprotease-producing individuals with protein as the sole carbon source selects for exoprotease non-producers mutants with an impaired quorum-sensing regulator, LasR, which controls exoprotease expression. However, recent studies reveal that some isolates lacking functional LasR still produce exoproteases under the control of another regulator, RhlR. Here, we extended this study to two clinical strains, AUS 411 and AUS 531, isolated from cystic fibrosis patients and harboring functional LasR. Surprisingly, in AUS 411, exoprotease-non-producers appeared from the first growth passage, but most cells lost exoprotease production only transiently, with stable non-producers isolated only in late passages. In contrast, AUS 531 slowly selected stable non-producers with limited cheating ability, which neither accumulated to high proportions nor caused population collapses. Contrary to the paradigm, these non-producers had no inactivating mutations in lasR yet were more fit than laboratory-derived lasR deletion mutants in both casein and casamino acid media. Our findings demonstrate that social behavior can differ significantly from that in reference strains, suggesting that some P. aeruginosa strains evolve quorum-sensing networks with robust resistance to exploitation.

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Journal
FEMS Microbiology Ecology
Published
2025-10-13
DOI
https://doi.org/10.1093/femsec/fiaf106
Primary Topic
Academic integrity and plagiarism
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article
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article

Challenging the paradigm: non-canonical exoprotease cheating in clinical Pseudomonas aeruginosa isolates

Nicolas Fontaine, Frédéric Cadet, Diego Esquivel-Hernández, Shotaro Toya et al.
FEMS Microbiology Ecology
Academic integrity and plagiarism
article

Challenging the paradigm: non-canonical exoprotease cheating in clinical Pseudomonas aeruginosa isolates

Nicolas Fontaine, Frédéric Cadet, Diego Esquivel-Hernández, Shotaro Toya, Antonio Oliver, Selene García‐Reyes, Rodolfo García‐Contreras, Miguel Cocotl‐Yañez, María Tomás, Rafael Cantón, Alejandra Leonor Valdez, Timothy J. Kidd, Bernardo Franco, Bianca Rivera-Peña, Fohad Mabood Husain, Toshinari Maeda, Ángel Yahir Estrada-Velasco, Thomas K. Wood, Héctor Quezada, Joy Kirigo, Katya Dafne Guadarrama-Orozco, Mohammed Arshad, Altaf Khan, Lorena Paola Olvera-Falfan, Diana Ceapa, Miguel Ángel Islas-Tolentino, Diana Marroquin, María Guadalupe Lucero-Gil
article en

Abstract

Pseudomonas aeruginosa is a model organism for studying social behaviors in bacteria, such as the exploitation of exoprotease by social cheaters. The current paradigm holds that continuous culture of exoprotease-producing individuals with protein as the sole carbon source selects for exoprotease non-producers mutants with an impaired quorum-sensing regulator, LasR, which controls exoprotease expression. However, recent studies reveal that some isolates lacking functional LasR still produce exoproteases under the control of another regulator, RhlR. Here, we extended this study to two clinical strains, AUS 411 and AUS 531, isolated from cystic fibrosis patients and harboring functional LasR. Surprisingly, in AUS 411, exoprotease-non-producers appeared from the first growth passage, but most cells lost exoprotease production only transiently, with stable non-producers isolated only in late passages. In contrast, AUS 531 slowly selected stable non-producers with limited cheating ability, which neither accumulated to high proportions nor caused population collapses. Contrary to the paradigm, these non-producers had no inactivating mutations in lasR yet were more fit than laboratory-derived lasR deletion mutants in both casein and casamino acid media. Our findings demonstrate that social behavior can differ significantly from that in reference strains, suggesting that some P. aeruginosa strains evolve quorum-sensing networks with robust resistance to exploitation.

FEMS Microbiology EcologyVol. 101(11)
Universidade da Coruña (ES), Universidad de Guanajuato (MX), Queensland Health (AU), Pennsylvania State University (US), Universidad Autónoma Metropolitana (MX), Kyushu Institute of Technology (JP), King Saud Medical City (SA), Instituto de Salud Carlos III (ES), King Saud University (SA), Centro Médico Nacional La Raza (MX), Hospital Infantil de México Federico Gómez (MX), Instituto Nacional de Cardiologia (BR), Secretaría de Ciencia Tecnología e Innovación (MX), Centre for Artificial Intelligence and Robotics (IN), Planta Piloto de Procesos Industriales Microbiológicos (AR), Health Research Institute of the Balearic Islands (ES), Instituto Ramón y Cajal de Investigación Sanitaria (ES), Instituto de Tecnología Química (ES), Hospital de Especialidades (MX), Instituto de Biotecnología y Biología Molecular (AR), Instituto Nacional de Cardiología (MX), Instituto de Investigación Biomédica de A Coruña (ES), Universidad Nacional Autónoma de México (MX)
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Academic integrity and plagiarism
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