Insertion sequence transposition activates antimycobacteriophage immunity through an lsr2‐silenced lipid metabolism gene island
Yakun Li,
Yuyun Wei,
Xiao Guo,
Xiaohui Li,
Lining Lu,
Lihua Hu,
Zheng‐Guo He
Affiliations
Yakun Li
State Key Laboratory for Conservation and Utilization of Subtropical Agro‐Bioresources, Guangxi Research Center for Microbial and Enzyme Engineering Technology, College of Life Science and Technology Guangxi University Nanning China
Yuyun Wei
State Key Laboratory for Conservation and Utilization of Subtropical Agro‐Bioresources, Guangxi Research Center for Microbial and Enzyme Engineering Technology, College of Life Science and Technology Guangxi University Nanning China
Xiao Guo
State Key Laboratory for Conservation and Utilization of Subtropical Agro‐Bioresources, Guangxi Research Center for Microbial and Enzyme Engineering Technology, College of Life Science and Technology Guangxi University Nanning China
Xiaohui Li
State Key Laboratory for Conservation and Utilization of Subtropical Agro‐Bioresources, Guangxi Research Center for Microbial and Enzyme Engineering Technology, College of Life Science and Technology Guangxi University Nanning China
Lining Lu
State Key Laboratory for Conservation and Utilization of Subtropical Agro‐Bioresources, Guangxi Research Center for Microbial and Enzyme Engineering Technology, College of Life Science and Technology Guangxi University Nanning China
Lihua Hu
State Key Laboratory for Conservation and Utilization of Subtropical Agro‐Bioresources, Guangxi Research Center for Microbial and Enzyme Engineering Technology, College of Life Science and Technology Guangxi University Nanning China
Zheng‐Guo He
State Key Laboratory for Conservation and Utilization of Subtropical Agro‐Bioresources, Guangxi Research Center for Microbial and Enzyme Engineering Technology, College of Life Science and Technology Guangxi University Nanning China
Abstract Insertion sequences (ISs) exist widely in bacterial genomes, but their roles in the evolution of bacterial antiphage defense remain to be clarified. Here, we report that, under the pressure of phage infection, the IS1096 transposition of Mycobacterium smegmatis into the lsr2 gene can occur at high frequencies, which endows the mutant mycobacterium with a broad‐spectrum antiphage ability. Lsr2 functions as a negative regulator and directly silences expression of a gene island composed of 11 lipid metabolism‐related genes. The complete or partial loss of the gene island leads to a significant decrease of bacteriophage adsorption to the mycobacterium, thus defending against phage infection. Strikingly, a phage that has evolved mutations in two tail‐filament genes can re‐escape from the lsr2 inactivation‐triggered host defense. This study uncovered a new signaling pathway for activating antimycobacteriophage immunity by IS transposition and provided insight into the natural evolution of bacterial antiphage defense.