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

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.