Combined actions of bacteriophage-encoded genes in Wolbachia-induced male lethality

• Published in: iScience Vol. 26; no. 6; p. 106842
• Main Authors: Arai, Hiroshi, Anbutsu, Hisashi, Nishikawa, Yohei, Kogawa, Masato, Ishii, Kazuo, Hosokawa, Masahito, Lin, Shiou-Ruei, Ueda, Masatoshi, Nakai, Madoka, Kunimi, Yasuhisa, Harumoto, Toshiyuki, Kageyama, Daisuke, Takeyama, Haruko, Inoue, Maki N.
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 16.06.2023; Elsevier
• Subjects: Evolutionary biology; Genetics; Microbiology; Virology; Genetics; Microbiology; Evolutionary biology; Virology
• ISSN: 2589-0042; 2589-0042
• DOI: 10.1016/j.isci.2023.106842

Some Wolbachia endosymbionts induce male killing, whereby male offspring of infected females are killed during development; however, the origin and diversity of the underlying mechanisms remain unclear. In this study, we identified a 76 kbp prophage region specific to male-killing Wolbachia hosted by the moth Homona magnanima. The prophage encoded a homolog of the male-killing gene oscar in Ostrinia moths and the wmk gene that induces various toxicities in Drosophila melanogaster. Upon overexpressing these genes in D. melanogaster, wmk-1 and wmk-3 killed all males and most females, whereas Hm-oscar, wmk-2, and wmk-4 had no impact on insect survival. Strikingly, co-expression of tandemly arrayed wmk-3 and wmk-4 killed 90% of males and restored 70% of females, suggesting their conjugated functions for male-specific lethality. While the male-killing gene in the native host remains unknown, our findings highlight the role of bacteriophages in male-killing evolution and differences in male-killing mechanisms among insects. [Display omitted] •The origin and diversity of the male-killing mechanisms of Wolbachia were studied•Bacteriophages are involved in evolution and differences in male-killing mechanisms•Combinations of wmk genes induce multiple MK mechanisms and lethality variations Virology; Genetics; Microbiology; Evolutionary biology