Evolution of insect innate immunity through domestication of bacterial toxins

Verster, Kirsten I. and Cinege, Gyöngyi and Lipinszki, Zoltán and Magyar, Lilla B. and Kurucz, Éva and Tarnopol, Rebecca L. and Ábrahám, Edit and Darula, Zsuzsanna and Karageorgi, Marianthi and Tamsil, Josephine A. and Akalu, Saron M. and Andó, István and Whiteman, Noah K. (2023) Evolution of insect innate immunity through domestication of bacterial toxins. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 120 (16). ArtNo: e2218334120. ISSN 0027-8424

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Abstract

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.

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