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

Author:

Huelgas-Méndez Daniel1,Cazares Daniel2,Alcaraz Luis David3,Ceapã Corina Diana4,Cocotl-Yañez Miguel1,Shotaro Toya5,Maeda Toshinari5,Fernández-Presas Ana María1,Tostado-Islas Oswaldo1,González-Vadillo Ana Lorena1,Limones-Martínez Aldo1,Hernandez-Cuevas Carlos Eduardo1,González-García Karen1,Jiménez-García Luis Felipe6,Martínez Reyna-Lara6,Santos-López Cristian Sadalis17,Husain Fohad Mabood8,Khan Altaf9,Arshad Mohammed10,Kokila Kota11,Wood Thomas K12,García-Contreras Rodolfo1ORCID

Affiliation:

1. Departamento de Microbiología y Parasitología, Facultad de Medicina, Universidad Nacional Autonoma de Mexico , Circuito Escolar 411A, Copilco Universidad, Coyoacán 04360, Mexico City , Mexico

2. Department of Biology, University of Oxford , Broad St, Oxford OX1 3AZ, Oxford , United Kingdom

3. Laboratorio de Genómica Ambiental, Departamento de Biología Celular, Facultad de Ciencias, UNAM , Circuito de la Investigación Científica, C.U., 04510, Mexico City , Mexico

4. Microbiology Laboratory, Chemistry Institute, Universidad Nacional Autonoma de Mexico , Circuito de la Investigación Científica, C.U., 04510, Mexico City , Mexico

5. 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

6. Departamento de Biología Celular, Facultad de Ciencias, UNAM, Universidad Nacional Autónoma de México , Circuito de la Investigación Científica, C.U., 04510, Mexico City , Mexico

7. Universidad Tec Milenio, Toluca de Lerdo , Calle Guadalupe Victoria 221, Las Jaras, Metepe 52166 , Mexico

8. Department of Food Science and Nutrition, King Saud University , Riyadh 11451 , Saudi Arabia

9. Department of Pharmacology, Central Laboratory, King Saud University , Riyadh 11451 , Saudi Arabia

10. Dental Health Department, College of Applied Medical Sciences, King Saud University , Riyadh 11451 , Saudi Arabia

11. Department of Biology, Ramapo College of New Jersey , 505 Ramapo Valley Rd, Mahwah, NJ 07430 , United States

12. Department of Chemical Engineering, Pennsylvania State University , University Park, PA 16802-4400 , United States

Abstract

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.

Funder

DGAPA, UNAM

Consejo Nacional de Ciencia y Tecnología

King Saud University

Publisher

Oxford University Press (OUP)

Subject

Applied Microbiology and Biotechnology,Ecology,Microbiology

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