Male-killing-associated bacteriophage WO identified from comparisons of Wolbachia endosymbionts of Homona magnanima

Arai, H.; Anbutsu, H.; Nishikawa, Y.; Kogawa, M.; Ishii, K.; Hosokawa, M.; Lin, S.-R.; Ueda, M.; Nakai, M.; Kunimi, Y.; Harumoto, T.; Kageyama, D.; Takeyama, H.; INOUE, M. N.

doi:10.1101/2022.06.12.495854

bioRxiv · 10.1101/2022.06.12.495854

Male-killing-associated bacteriophage WO identified from comparisons of Wolbachia endosymbionts of Homona magnanima

Arai, H.·Anbutsu, H.·Nishikawa, Y.·Kogawa, M.·Ishii, K.·Hosokawa, M.·Lin, S.-R.·Ueda, M.·Nakai, M.·Kunimi, Y.·Harumoto, T.·Kageyama, D.·Takeyama, H.·INOUE, M. N.

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Abstract

The origin and mechanism of male-killing, an advantageous strategy employed by maternally transmitted symbionts such as Wolbachia, remain unclear. We compared genomes of four Wolbachia strains derived from Homona magnanima, a male-killing strain wHm-t (1.5 Mb), and three non-male-killing strains, wHm-a (1.1 Mb), wHm-b (1.3 Mb), and wHm-c (1.4 Mb). A wHm-t-specific 76-kbp prophage region harboured two tandemly arrayed WO-mediated killing (wmk) gene homologs (wmk-1/wmk-2 and wmk-3/wmk-4). Of these, wmk-1 or wmk-3 killed almost all Drosophila melanogaster individuals when transgenically overexpressed. Dual expression of wmk-3 and wmk-4 killed all males and rescued females. We propose a novel hypothesis wherein horizontally transmitted proto-Wolbachia with a single wmk killed both sexes, and tandem duplication of wmk allowed an evolutionary transition to a vertically transmitted symbiont, causing male-killing. Our study highlights the bacteriophage as a critical driver of the evolution of male-killing and argues for a conserved male-killing mechanism in diverse insects.

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Arai, H., Anbutsu, H., Nishikawa, Y., Kogawa, M., Ishii, K., Hosokawa, M., Lin, S.-R., Ueda, M., Nakai, M., Kunimi, Y., Harumoto, T., Kageyama, D., Takeyama, H., INOUE, M. N.. 2022-06-13. Male-killing-associated bacteriophage WO identified from comparisons of Wolbachia endosymbionts of Homona magnanima. https://doi.org/10.1101/2022.06.12.495854

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