Toxin cargo genes are often horizontally transferred by phages between bacterial species
and are known to play an important role in the evolution of bacterial pathogenesis.
Here, we show how these same genes have been horizontally transferred from phage or
bacteria to animals and have resulted in novel adaptations. We discovered that two
widespread bacterial genes encoding toxins of animal cells, cytolethal distending
toxin subunit B ( cdtB ) and apoptosis-inducing protein of 56 kDa ( aip56) , were
captured by insect genomes through horizontal gene transfer from bacteria or phages.
To study the function of these genes in insects, we focused on Drosophila ananassae
as a model. In the D. ananassae subgroup species, cdtB and aip56 are present as singular
( cdtB ) or fused copies ( cdtB::aip56 ) on the second chromosome. We found that cdtB
and aip56 genes and encoded proteins were expressed by immune cells, some proteins
were localized to the wasp embryo’s serosa, and their expression increased following
parasitoid wasp infection. Species of the ananassae subgroup are highly resistant
to parasitoid wasps, and we observed that D. ananassae lines carrying null mutations
in cdtB and aip56 toxin genes were more susceptible to parasitoids than the wild type.
We conclude that toxin cargo genes were captured by these insects millions of years
ago and integrated as novel modules into their innate immune system. These modules
now represent components of a heretofore undescribed defense response and are important
for resistance to parasitoid wasps. Phage or bacterially derived eukaryotic toxin
genes serve as macromutations that can spur the instantaneous evolution of novelty
in animals.
