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

Autor:	Tarnopol RL; Department of Plant and Microbial Biology, University of California, Berkeley, Berkeley, CA 94720, USA. Electronic address: tarnopol@berkeley.edu., Tamsil JA; Department of Molecular & Cell Biology, University of California, Berkeley, Berkeley, CA 94720, USA., Cinege G; Innate Immunity Group, Institute of Genetics, HUN-REN Biological Research Centre, Szeged 6726, Hungary., Ha JH; Department of Molecular & Cell Biology, University of California, Berkeley, Berkeley, CA 94720, USA., Verster KI; Department of Integrative Biology, University of California, Berkeley, Berkeley, CA 94720, USA; Department of Biology, Stanford University, Palo Alto, CA 94305, USA., Ábrahám E; Synthetic and Systems Biology Unit, Institute of Biochemistry, HUN-REN Biological Research Centre, Szeged 6726, Hungary; National Laboratory for Biotechnology Institute of Genetics, HUN-REN Biological Research Centre, Szeged 6726, Hungary., Magyar LB; Innate Immunity Group, Institute of Genetics, HUN-REN Biological Research Centre, Szeged 6726, Hungary., Kim BY; Department of Biology, Stanford University, Palo Alto, CA 94305, USA., Bernstein SL; Department of Molecular & Cell Biology, University of California, Berkeley, Berkeley, CA 94720, USA; Department of Integrative Biology, University of California, Berkeley, Berkeley, CA 94720, USA., Lipinszki Z; Synthetic and Systems Biology Unit, Institute of Biochemistry, HUN-REN Biological Research Centre, Szeged 6726, Hungary; National Laboratory for Biotechnology Institute of Genetics, HUN-REN Biological Research Centre, Szeged 6726, Hungary., Andó I; Innate Immunity Group, Institute of Genetics, HUN-REN Biological Research Centre, Szeged 6726, Hungary. Electronic address: ando@brc.hu., Whiteman NK; Department of Molecular & Cell Biology, University of California, Berkeley, Berkeley, CA 94720, USA; Department of Integrative Biology, University of California, Berkeley, Berkeley, CA 94720, USA; Essig Museum of Entomology, University of California, Berkeley, Berkeley, CA 94720, USA. Electronic address: whiteman@berkeley.edu.
Jazyk:	angličtina
Zdroj:	Current biology : CB [Curr Biol] 2024 Dec 17. Date of Electronic Publication: 2024 Dec 17.
DOI:	10.1016/j.cub.2024.11.071
Abstrakt:	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. Competing Interests: Declaration of interests The authors declare no competing interests. (Copyright © 2024 The Author(s). Published by Elsevier Inc. All rights reserved.)
Databáze:	MEDLINE
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