Exoprotease exploitation and social cheating in a Pseudomonas aeruginosa environmental lysogenic strain with a noncanonical quorum sensing system.

Carlos Eduardo Hernandez-Cuevas, Rodolfo García-Contreras, Thomas K Wood, Kota Kokila, Mohammed Arshad, Altaf Khan, Fohad Mabood Husain, Cristian Sadalis Santos-López, Reyna-Lara Martínez, Luis Felipe Jiménez-García, Karen González-García, Daniel Huelgas-Méndez, Aldo Limones-Martínez, Ana Lorena González-Vadillo, Oswaldo Tostado-Islas, Ana María Fernández-Presas, Toshinari Maeda, Toya Shotaro, Miguel Cocotl-Yañez, Corina Diana Ceapã, Luis David Alcaraz, Daniel Cazares

Journal: FEMS microbiology ecology 2023;99(9):fiad086

PMID: 37496200

Abstract

Social cheating is the exploitation of public goods that are costly metabolites, like exoproteases. Exoprotease exploitation in Pseudomonas aeruginosa has been studied in reference strains. Experimental evolution with reference strains during continuous growth in casein has demonstrated that nonexoprotease producers that are lasR mutants are selected while they behave as social cheaters. However, noncanonical quorum-sensing systems exist in P. aeruginosa strains, which are diverse. In this work, the exploitation of exoproteases in the environmental strain ID4365 was evaluated; ID4365 has a nonsense mutation that precludes expression of LasR. ID4365 produces exoproteases under the control of RhlR, and harbors an inducible prophage. As expected, rhlR mutants of ID4365 behave as social cheaters, and exoprotease-deficient individuals accumulate upon continuous growth in casein. Moreover, in all continuous cultures, population collapses occur. However, this also sometimes happens before cheaters dominate. Interestingly, during growth in casein, ID4565's native prophage is induced, suggesting that the metabolic costs imposed by social cheating may increase its induction, promoting population collapses. Accordingly, lysogenization of the PAO1 lasR mutant with this prophage accelerated its collapse. These findings highlight the influence of temperate phages in social cheating.

© The Author(s) 2023. Published by Oxford University Press on behalf of FEMS.

Address: Departamento de Microbiología y Parasitología, Facultad de Medicina, Universidad Nacional Autonoma de Mexico, Circuito Escolar 411A, Copilco Universidad, Coyoacán 04360, Mexico City, Mexico.; Department of Biology, University of Oxford, Broad St, Oxford OX1 3AZ, Oxford, United Kingdom.; Laboratorio de Genómica Ambiental, Departamento de Biología Celular, Facultad de Ciencias, UNAM, Circuito de la Investigación Científica, C.U., 04510, Mexico City, Mexico.; Microbiology Laboratory, Chemistry Institute, Universidad Nacional Autonoma de Mexico, Circuito de la Investigación Científica, C.U., 04510, Mexico City, Mexico.; Department of Biological Functions Engineering, Graduate School of Life Science and Systems Engineering, Kyushu Institute of Technology, 2-4 Hibikino, Wakamatsu-ku, Kitakyushu 808-0196, Japan.; Departamento de Biología Celular, Facultad de Ciencias, UNAM, Universidad Nacional Autónoma de México, Circuito de la Investigación Científica, C.U., 04510, Mexico City, Mexico.; Universidad Tec Milenio, Toluca de Lerdo, Calle Guadalupe Victoria 221, Las Jaras, Metepe 52166, Mexico.; Department of Food Science and Nutrition, King Saud University, Riyadh 11451, Saudi Arabia.; Department of Pharmacology, Central Laboratory, King Saud University, Riyadh 11451, Saudi Arabia.; Dental Biomaterials Research Chair, Dental Health Department, College of Applied Medical Sciences, King Saud University, Riyadh 11451, Saudi Arabia.; Department of Biology, Ramapo College of New Jersey, 505 Ramapo Valley Rd, Mahwah, NJ 07430, United States.; Department of Chemical Engineering, Pennsylvania State University, University Park, PA 16802-4400, United States.
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