ORF4 of the temperate archaeal virus SNJ1 governs the lysis-lysogeny switch and superinfection immunity

Beibei Chen (1) , Zhao Chen (1) , Yuchen Wang (1) , Han Gong (1) , Linshan Sima (1) , Jiao Wang (1) , Shushan Ouyang (1) , Wenqiang Gan (1) , Mart Krupovic (2) , Xiangdong Chen (1) , Shishen Du (1)

1 State Key Laboratory of Virology
2 Virologie des archées - Archaeal Virology

Recent environmental and metagenomic studies have considerably increased the repertoire of archaeal viruses and suggested that they play important roles in nutrient cycling in the biosphere. However, very little is known about how they regulate their life cycles and interact with their hosts. Here, we report that the life cycle of the temperate haloarchaeal virus SNJ1 is controlled by the product ORF4, a small protein belonging to the antitoxin MazE superfamily. We show that ORF4 controls the lysis-lysogeny switch of SNJ1 and mediates superinfection immunity by repression of genomic DNA replication of the superinfecting viruses. Bioinformatic analysis shows that ORF4 is highly conserved in two SNJ1-like proviruses, suggesting that the mechanisms for lysis-lysogeny switch and superinfection immunity are conserved in this group of viruses. As lysis-lysogeny switch and superinfection immunity of archaeal viruses are poorly studied, we suggest that SNJ1 could serve as a model system to study these processes. IMPORTANCE Archaeal viruses are important parts of the virosphere. Understanding how they regulate their life cycles and interact with host cells provide crucial insights into their biological functions and the evolutionary histories of viruses. However, mechanistic studies of the life cycle of archaeal viruses are scarce due to a lack of genetic tools and demanding cultivation conditions. Here, we discover that the temperate haloarchaeal virus SNJ1, which infects Natrinema sp. J7, employs a lysis-lysogeny switch and establishes superinfection immunity like bacteriophages. We show that its ORF4 is critical for both processes and acts as a repressor of the replication of SNJ1.These results establish ORF4 as a master regulator of SNJ1 life cycle and provides novel insights on the regulation of life cycles by temperate archaeal viruses and on their interactions with host cells.

Mots clés: temperate virus; lysis-lysogeny switch; superinfection immunity; Archaea; SNJ1

Domaines: Microbiologie et Parasitologie; Virologie

Beibei Chen, Zhao Chen, Yuchen Wang, Han Gong, Linshan Sima, et al.. ORF4 of the temperate archaeal virus SNJ1 governs the lysis-lysogeny switch and superinfection immunity. Journal of Virology, 2020, 94 (16), pp.e00841-20. ⟨10.1128/JVI.00841-20⟩. ⟨pasteur-02909667⟩