Experimental horizontal transfer of phage-derived genes to Drosophila confers innate immunity to parasitoids.

IF 8.1 1区 生物学 Q1 BIOCHEMISTRY & MOLECULAR BIOLOGY Current Biology Pub Date : 2024-12-17 DOI:10.1016/j.cub.2024.11.071
Rebecca L Tarnopol, Josephine A Tamsil, Gyöngyi Cinege, Ji Heon Ha, Kirsten I Verster, Edit Ábrahám, Lilla B Magyar, Bernard Y Kim, Susan L Bernstein, Zoltán Lipinszki, István Andó, Noah K Whiteman
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Abstract

Metazoan parasites have played a major role in shaping innate immunity in animals. Insect hosts and parasitoid wasps are excellent models for illuminating how animal innate immune systems have evolved to neutralize these enemies. One such strategy relies on symbioses between insects and intracellular bacteria that express phage-encoded toxins. In some cases, the genes that encode these toxins have been horizontally transferred to the genomes of the insects. Here, we used genome editing in Drosophila melanogaster to recapitulate the evolution of two 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 mechanism of toxicity 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.

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来源期刊
Current Biology
Current Biology 生物-生化与分子生物学
CiteScore
11.80
自引率
2.20%
发文量
869
审稿时长
46 days
期刊介绍: Current Biology is a comprehensive journal that showcases original research in various disciplines of biology. It provides a platform for scientists to disseminate their groundbreaking findings and promotes interdisciplinary communication. The journal publishes articles of general interest, encompassing diverse fields of biology. Moreover, it offers accessible editorial pieces that are specifically designed to enlighten non-specialist readers.
期刊最新文献
A recurrent neural circuit in Drosophila temporally sharpens visual inputs. The Fat-Dachsous planar polarity pathway competes with hinge contraction to orient polarized cell behaviors during Drosophila wing morphogenesis. Experimental horizontal transfer of phage-derived genes to Drosophila confers innate immunity to parasitoids. Visual identification of conspecifics shapes social behavior in mice. Form, function, and evolutionary origins of architectural symmetry in honey bee nests.
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