Filamentous prophage Pf4 promotes genetic exchange in Pseudomonas aeruginosa

Author:

Pei Tong-Tong12,Luo Han1,Wang Yuanyuan3,Li Hao12,Wang Xing-Yu12,Zhang Yi-Qiu2,An Ying2,Wu Li-Li1,Ma Junhua1,Liang Xiaoye2,Yan Aixin4,Yang Liang5,Chen Changbin36,Dong Tao2

Affiliation:

1. State Key Laboratory of Microbial Metabolism, Joint International Research Laboratory of Metabolic & Developmental Sciences, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University , Shanghai 200240 , China

2. Department of Immunology and Microbiology, School of Life Sciences, Southern University of Science and Technology , Shenzhen 518055 , China

3. Unit of Pathogenic Fungal Infection and Host Immunity, Key Laboratory of Molecular Virology and Immunology, Institute of Immunity and Infection, Chinese Academy of Sciences , Shanghai 200031 , China

4. School of Biological Sciences, The University of Hong Kong, Hong Kong Special Administrative Region 999077 , China

5. School of Medicine, Southern University of Science and Technology , Shenzhen 518055 , China

6. Nanjing Advanced Academy of Life and Health , Nanjing 211135 , China

Abstract

Abstract Filamentous prophages are widespread among bacteria and play crucial functions in virulence, antibiotic resistance, and biofilm structures. The filamentous Pf4 particles, extruded by an important pathogen Pseudomonas aeruginosa, can protect producing cells from adverse conditions. Contrary to the conventional belief that the Pf4-encoding cells resist reinfection, we herein report that the Pf4 prophage is reciprocally and commonly exchanged within P. aeruginosa colonies, which can repair defective Pf4 within the community. By labeling the Pf4 locus with antibiotic resistance and fluorescence markers, we demonstrate that the Pf4 locus is frequently exchanged within colony biofilms, in artificial sputum media, and in infected mouse lungs. We further show that Pf4 trafficking is a rapid process and capable of rescuing Pf4-defective mutants. The Pf4 phage is highly adaptable and can package additional DNA doubling its genome size. We also report that two clinical P. aeruginosa isolates are susceptible to the Pf4-mediated exchange, and the Pf5 prophage can be exchanged between cells as well. These findings suggest that the genetic exchanging interactions by filamentous prophages may facilitate defect rescue and the sharing of prophage-dependent benefits and costs within the P. aeruginosa community.

Funder

National Key Research and Development Program of China

National Natural Science Foundation of China

Innovation Capacity Building Project of Jiangsu Province

Guangdong Natural Science Foundation for Distinguished Young Scholar

Publisher

Oxford University Press (OUP)

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