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Data from: Experimental horizontal transfer of phage-derived genes to Drosophila confers innate immunity to parasitoids

Tarnopol, Rebecca1; Tamsil, Josephine1; Cinege, Gyöngyi2; Ha, Ji Heon1; Verster, Kirsten3; Ábrahám, Edit2; Magyar, Lilla2; Kim, Bernard3; Bernstein, Susan1; Lipinszki, Zoltán2; Andó, István2; Whiteman, Noah1

Published Jan 02, 2025 on Dryad. https://doi.org/10.5061/dryad.q573n5tsh

Data files

Jan 02, 2025 version files 5.07 GB

Abstract

Metazoan parasites have played an outsized role in shaping innate immunity in animals. Insects are excellent models for illuminating the strategies that animals evolved to neutralize such enemies, including nematodes and parasitoid wasps. One such strategy relies on endosymbioses between insects and bacteria that express phage-encoded toxins as well as horizontal transfer of the genes that encode the toxins to insects. Here, we used genome editing in Drosophila melanogaster to recapitulate the evolution of two of these toxin genes — cytolethal distending toxin B (cdtB) and apoptosis inducing protein of 56kDa (aip56) — that were horizontally transferred likely from phages of endosymbiotic bacteria to insects millions of years ago. We found that a cdtB::aip56 fusion gene (fusionB), which is conserved in D. ananassae subgroup species, dramatically promoted fly survival and suppressed parasitoid wasp development when heterologously expressed in D. melanogaster immune tissues. We found that FusionB was a functional nuclease and was secreted into the host hemolymph where it targeted the parasitoid embryo’s serosal tissue. Although the killing mechanism remains unknown, when expressed ubiquitously, fusionB resulted in delayed development of late stage fly larvae and eventually killed pupating flies. These results point to the salience of regulatory constraint in mitigating autoimmunity during the domestication process following horizontal transfer. Our findings demonstrate how horizontal gene transfer can instantly provide new, potent innate immune modules in animals.