Combined actions of bacteriophage-encoded genes in Wolbachia-induced male lethality
Hiroshi Arai,
Hisashi Anbutsu,
Yohei Nishikawa,
Masato Kogawa,
Kazuo Ishii,
Masahito Hosokawa,
Shiou-Ruei Lin,
Masatoshi Ueda,
Madoka Nakai,
Yasuhisa Kunimi,
Toshiyuki Harumoto,
Daisuke Kageyama,
Haruko Takeyama,
Maki N. Inoue
Affiliations
Hiroshi Arai
United Graduate School of Agricultural Science, Tokyo University of Agriculture and Technology, 3-5-8 Saiwai, Fuchu, Tokyo 183-8509, Japan; National Agriculture and Food Research Organization (NARO), 1-2 Owashi, Tsukuba, Ibaraki 305-0851, Japan; Corresponding author
Hisashi Anbutsu
Computational Bio Big-Data Open Innovation Laboratory (CBBD-OIL), National Institute of Advanced Industrial Science and Technology (AIST), 3-4-1 Okubo, Shinjuku-ku, Tokyo 169-8555, Japan; Bioproduction Research Institute, AIST, 1-1-1 Higashi, Tsukuba, Ibaraki 305-8566, Japan; Research Organization for Nano and Life Innovation, Waseda University, 513 Wasedatsurumaki-cho, Shinjuku-ku, Tokyo 162-0041, Japan
Yohei Nishikawa
Computational Bio Big-Data Open Innovation Laboratory (CBBD-OIL), National Institute of Advanced Industrial Science and Technology (AIST), 3-4-1 Okubo, Shinjuku-ku, Tokyo 169-8555, Japan; Research Organization for Nano and Life Innovation, Waseda University, 513 Wasedatsurumaki-cho, Shinjuku-ku, Tokyo 162-0041, Japan
Masato Kogawa
Research Organization for Nano and Life Innovation, Waseda University, 513 Wasedatsurumaki-cho, Shinjuku-ku, Tokyo 162-0041, Japan
Kazuo Ishii
United Graduate School of Agricultural Science, Tokyo University of Agriculture and Technology, 3-5-8 Saiwai, Fuchu, Tokyo 183-8509, Japan
Masahito Hosokawa
Computational Bio Big-Data Open Innovation Laboratory (CBBD-OIL), National Institute of Advanced Industrial Science and Technology (AIST), 3-4-1 Okubo, Shinjuku-ku, Tokyo 169-8555, Japan; Research Organization for Nano and Life Innovation, Waseda University, 513 Wasedatsurumaki-cho, Shinjuku-ku, Tokyo 162-0041, Japan; Institute for Advanced Research of Biosystem Dynamics, Waseda Research Institute for Science and Engineering, Graduate School of Advanced Science and Engineering, Waseda University, 3-4-1 Okubo, Shinjuku-ku, Tokyo 169-8555, Japan; Department of Life Science and Medical Bioscience, Graduate School of Advanced Science and Engineering, Waseda University, 2-2 Wakamatsucho, Shinjuku-ku, Tokyo 162-8480, Japan
Shiou-Ruei Lin
Tea Research and Extension Station, 326011 Chung-Hsing RD, Yangmei, Taoyuan, Taiwan, R.O.C
Masatoshi Ueda
United Graduate School of Agricultural Science, Tokyo University of Agriculture and Technology, 3-5-8 Saiwai, Fuchu, Tokyo 183-8509, Japan
Madoka Nakai
United Graduate School of Agricultural Science, Tokyo University of Agriculture and Technology, 3-5-8 Saiwai, Fuchu, Tokyo 183-8509, Japan
Yasuhisa Kunimi
United Graduate School of Agricultural Science, Tokyo University of Agriculture and Technology, 3-5-8 Saiwai, Fuchu, Tokyo 183-8509, Japan
Toshiyuki Harumoto
Hakubi Center for Advanced Research, Kyoto University. Yoshida-honmachi, Sakyo-ku, Kyoto 606-8501, Japan; Graduate School of Biostudies, Kyoto University, Yoshida-Konoe-cho, Sakyo-ku, Kyoto 606-8501, Japan
Daisuke Kageyama
National Agriculture and Food Research Organization (NARO), 1-2 Owashi, Tsukuba, Ibaraki 305-0851, Japan
Haruko Takeyama
Computational Bio Big-Data Open Innovation Laboratory (CBBD-OIL), National Institute of Advanced Industrial Science and Technology (AIST), 3-4-1 Okubo, Shinjuku-ku, Tokyo 169-8555, Japan; Research Organization for Nano and Life Innovation, Waseda University, 513 Wasedatsurumaki-cho, Shinjuku-ku, Tokyo 162-0041, Japan; Institute for Advanced Research of Biosystem Dynamics, Waseda Research Institute for Science and Engineering, Graduate School of Advanced Science and Engineering, Waseda University, 3-4-1 Okubo, Shinjuku-ku, Tokyo 169-8555, Japan; Department of Life Science and Medical Bioscience, Graduate School of Advanced Science and Engineering, Waseda University, 2-2 Wakamatsucho, Shinjuku-ku, Tokyo 162-8480, Japan; Corresponding author
Maki N. Inoue
United Graduate School of Agricultural Science, Tokyo University of Agriculture and Technology, 3-5-8 Saiwai, Fuchu, Tokyo 183-8509, Japan; Corresponding author
Summary: 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.
