A reverse transcriptase controls prophage genome reduction to promote phage dissemination in Pseudomonas aeruginosa biofilms
Yunxue Guo,
Shituan Lin,
Ran Chen,
Jiayu Gu,
Kaihao Tang,
Zhaolong Nie,
Zixian Huang,
Juehua Weng,
Jianzhong Lin,
Tianlang Liu,
Matthew K. Waldor,
Xiaoxue Wang
Affiliations
Yunxue Guo
Key Laboratory of Tropical Marine Bio-resources and Ecology, Guangdong Key Laboratory of Marine Materia Medica, Innovation Academy of South China Sea Ecology and Environmental Engineering, South China Sea Institute of Oceanology, Chinese Academy of Sciences, No. 1119 Haibin Road, Nansha District, Guangzhou 511458, China; Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou), No. 1119 Haibin Road, Nansha District, Guangzhou 511458, China; University of Chinese Academy of Sciences, Beijing 100049, China
Shituan Lin
Key Laboratory of Tropical Marine Bio-resources and Ecology, Guangdong Key Laboratory of Marine Materia Medica, Innovation Academy of South China Sea Ecology and Environmental Engineering, South China Sea Institute of Oceanology, Chinese Academy of Sciences, No. 1119 Haibin Road, Nansha District, Guangzhou 511458, China; University of Chinese Academy of Sciences, Beijing 100049, China
Ran Chen
Key Laboratory of Tropical Marine Bio-resources and Ecology, Guangdong Key Laboratory of Marine Materia Medica, Innovation Academy of South China Sea Ecology and Environmental Engineering, South China Sea Institute of Oceanology, Chinese Academy of Sciences, No. 1119 Haibin Road, Nansha District, Guangzhou 511458, China; Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou), No. 1119 Haibin Road, Nansha District, Guangzhou 511458, China
Jiayu Gu
Key Laboratory of Tropical Marine Bio-resources and Ecology, Guangdong Key Laboratory of Marine Materia Medica, Innovation Academy of South China Sea Ecology and Environmental Engineering, South China Sea Institute of Oceanology, Chinese Academy of Sciences, No. 1119 Haibin Road, Nansha District, Guangzhou 511458, China; University of Chinese Academy of Sciences, Beijing 100049, China
Kaihao Tang
Key Laboratory of Tropical Marine Bio-resources and Ecology, Guangdong Key Laboratory of Marine Materia Medica, Innovation Academy of South China Sea Ecology and Environmental Engineering, South China Sea Institute of Oceanology, Chinese Academy of Sciences, No. 1119 Haibin Road, Nansha District, Guangzhou 511458, China; Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou), No. 1119 Haibin Road, Nansha District, Guangzhou 511458, China
Zhaolong Nie
Key Laboratory of Tropical Marine Bio-resources and Ecology, Guangdong Key Laboratory of Marine Materia Medica, Innovation Academy of South China Sea Ecology and Environmental Engineering, South China Sea Institute of Oceanology, Chinese Academy of Sciences, No. 1119 Haibin Road, Nansha District, Guangzhou 511458, China
Zixian Huang
Key Laboratory of Tropical Marine Bio-resources and Ecology, Guangdong Key Laboratory of Marine Materia Medica, Innovation Academy of South China Sea Ecology and Environmental Engineering, South China Sea Institute of Oceanology, Chinese Academy of Sciences, No. 1119 Haibin Road, Nansha District, Guangzhou 511458, China; University of Chinese Academy of Sciences, Beijing 100049, China
Juehua Weng
Key Laboratory of Tropical Marine Bio-resources and Ecology, Guangdong Key Laboratory of Marine Materia Medica, Innovation Academy of South China Sea Ecology and Environmental Engineering, South China Sea Institute of Oceanology, Chinese Academy of Sciences, No. 1119 Haibin Road, Nansha District, Guangzhou 511458, China; University of Chinese Academy of Sciences, Beijing 100049, China
Jianzhong Lin
Key Laboratory of Tropical Marine Bio-resources and Ecology, Guangdong Key Laboratory of Marine Materia Medica, Innovation Academy of South China Sea Ecology and Environmental Engineering, South China Sea Institute of Oceanology, Chinese Academy of Sciences, No. 1119 Haibin Road, Nansha District, Guangzhou 511458, China; University of Chinese Academy of Sciences, Beijing 100049, China
Tianlang Liu
Key Laboratory of Tropical Marine Bio-resources and Ecology, Guangdong Key Laboratory of Marine Materia Medica, Innovation Academy of South China Sea Ecology and Environmental Engineering, South China Sea Institute of Oceanology, Chinese Academy of Sciences, No. 1119 Haibin Road, Nansha District, Guangzhou 511458, China; University of Chinese Academy of Sciences, Beijing 100049, China
Matthew K. Waldor
Department of Microbiology, Harvard Medical School, 77 Avenue Louis Pasteur, Boston, MA 02115, USA; Division of Infectious Diseases, Brigham and Women’s Hospital, 15 Francis Street, Boston, MA 02115, USA; Howard Hughes Medical Institute, 181 Longwood Avenue, Boston, MA 02115, USA
Xiaoxue Wang
Key Laboratory of Tropical Marine Bio-resources and Ecology, Guangdong Key Laboratory of Marine Materia Medica, Innovation Academy of South China Sea Ecology and Environmental Engineering, South China Sea Institute of Oceanology, Chinese Academy of Sciences, No. 1119 Haibin Road, Nansha District, Guangzhou 511458, China; Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou), No. 1119 Haibin Road, Nansha District, Guangzhou 511458, China; University of Chinese Academy of Sciences, Beijing 100049, China; Corresponding author
Summary: Filamentous bacteriophages play a critical role in biofilm formation and virulence in the opportunistic pathogen Pseudomonas aeruginosa. Here, studies of the filamentous Pf4 prophage life cycle within P. aeruginosa biofilms revealed that the prophage-encoded reverse transcriptase (RT) regulates phage genome dynamics. The RT and the non-coding RNA PhrD collaborate to edit the Pf4 phage genome to generate superinfective Pf4 variants capable of rapid propagation within biofilms by preserving genes essential for virion assembly and reconstituting a promoter for the phage excisionase gene. Mutant cells emerge in biofilms where intact Pf4 prophages are replaced by these reduced-genome phage variants, further enhancing virion production. The discovery of RT’s role in phage genome reduction expands understanding of RT functions and of the versatility of phage biology and its impact on microbial community dynamics within biofilms.
