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

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 b...

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Published iniScience 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
LanguageEnglish
Published United States Elsevier Inc 16.06.2023
Elsevier
Subjects
Evolutionary biology
Genetics
Microbiology
Virology
Genetics
Microbiology
Evolutionary biology
Virology
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Abstract 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
AbstractList 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.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.
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.
Some 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 hosted by the moth . The prophage encoded a homolog of the male-killing gene in moths and the gene that induces various toxicities in . Upon overexpressing these genes in , and killed all males and most females, whereas and had no impact on insect survival. Strikingly, co-expression of tandemly arrayed and 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.
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. • 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
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
ArticleNumber 106842
Author Kunimi, Yasuhisa
Hosokawa, Masahito
Anbutsu, Hisashi
Lin, Shiou-Ruei
Takeyama, Haruko
Ishii, Kazuo
Kogawa, Masato
Ueda, Masatoshi
Harumoto, Toshiyuki
Arai, Hiroshi
Kageyama, Daisuke
Inoue, Maki N.
Nishikawa, Yohei
Nakai, Madoka
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  surname: Arai
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  organization: United Graduate School of Agricultural Science, Tokyo University of Agriculture and Technology, 3-5-8 Saiwai, Fuchu, Tokyo 183-8509, Japan
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  organization: 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
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  fullname: Nishikawa, Yohei
  organization: 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
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  organization: United Graduate School of Agricultural Science, Tokyo University of Agriculture and Technology, 3-5-8 Saiwai, Fuchu, Tokyo 183-8509, Japan
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  givenname: Masahito
  surname: Hosokawa
  fullname: Hosokawa, Masahito
  organization: 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
– sequence: 7
  givenname: Shiou-Ruei
  surname: Lin
  fullname: Lin, Shiou-Ruei
  organization: Tea Research and Extension Station, 326011 Chung-Hsing RD, Yangmei, Taoyuan, Taiwan, R.O.C
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  givenname: Masatoshi
  surname: Ueda
  fullname: Ueda, Masatoshi
  organization: United Graduate School of Agricultural Science, Tokyo University of Agriculture and Technology, 3-5-8 Saiwai, Fuchu, Tokyo 183-8509, Japan
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  givenname: Madoka
  surname: Nakai
  fullname: Nakai, Madoka
  organization: United Graduate School of Agricultural Science, Tokyo University of Agriculture and Technology, 3-5-8 Saiwai, Fuchu, Tokyo 183-8509, Japan
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  givenname: Yasuhisa
  surname: Kunimi
  fullname: Kunimi, Yasuhisa
  organization: United Graduate School of Agricultural Science, Tokyo University of Agriculture and Technology, 3-5-8 Saiwai, Fuchu, Tokyo 183-8509, Japan
– sequence: 11
  givenname: Toshiyuki
  surname: Harumoto
  fullname: Harumoto, Toshiyuki
  organization: Hakubi Center for Advanced Research, Kyoto University. Yoshida-honmachi, Sakyo-ku, Kyoto 606-8501, Japan
– sequence: 12
  givenname: Daisuke
  surname: Kageyama
  fullname: Kageyama, Daisuke
  organization: National Agriculture and Food Research Organization (NARO), 1-2 Owashi, Tsukuba, Ibaraki 305-0851, Japan
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  givenname: Haruko
  surname: Takeyama
  fullname: Takeyama, Haruko
  email: haruko-takeyama@waseda.jp
  organization: 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
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  givenname: Maki N.
  surname: Inoue
  fullname: Inoue, Maki N.
  email: makimaki@cc.tuat.ac.jp
  organization: United Graduate School of Agricultural Science, Tokyo University of Agriculture and Technology, 3-5-8 Saiwai, Fuchu, Tokyo 183-8509, Japan
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Keywords Genetics
Microbiology
Evolutionary biology
Virology
Language English
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Snippet Some Wolbachia endosymbionts induce male killing, whereby male offspring of infected females are killed during development; however, the origin and diversity...
Some endosymbionts induce male killing, whereby male offspring of infected females are killed during development; however, the origin and diversity of the...
Some Wolbachia endosymbionts induce male killing, whereby male offspring of infected females are killed during development; however, the origin and diversity...
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SubjectTerms Evolutionary biology
Genetics
Microbiology
Virology
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Title Combined actions of bacteriophage-encoded genes in Wolbachia-induced male lethality
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