Transcriptomic response during wasp parasitism in the Drosophila-Spiroplasma interaction
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abstract
AbstractSeveral facultative bacterial symbionts of insects protect their hosts against natural enemies.Spiroplasma poulsoniistrainsMel, a male-killing heritable symbiont ofDrosophila melanogaster, confers protection against some species of parasitic wasps. Several lines of evidence suggest thatSpiroplasma-encoded ribosome inactivating proteins (RIPs) are involved in the protection mechanism, but the potential contribution of the fly-encoded functions has not been deeply explored. Here we used RNA-seq to evaluate the response ofD. melanogasterto infection bySpiroplasmaand parasitism by theSpiroplasma-susceptible waspLeptopilina heterotoma, and theSpiroplasma-resistant waspGanaspis hookeri. In the absence ofSpiroplasmainfection, we found evidence ofDrosophilaimmune activation byG. hookeri, but not byL. heterotoma, which in turn negatively influenced functions associated with male gonad development. As expected for a symbiont that kills males, we detected extensive downregulation in theSpiroplasma-infected treatments of genes known to have male-biased expression. We detected very few genes whose expression was influenced by theSpiroplasma-L. heterotomainteraction, and they do not appear to be related to immune response. For most of them, parasitism byL. heterotoma(in the absence ofSpiroplasma) caused an expression change that was at least partly reversed whenSpiroplasmawas also present. It is unclear whether such genes are involved in theSpiroplasma-mediated mechanism that leads to wasp death or fly rescue. Nonetheless, the expression pattern of some of these genes, which reportedly undergo expression shifts during the larva-to-pupa transition, is suggestive of an influence ofSpiroplasmaon the development time ofL. heterotoma-parasitized flies. In addition, we used the RNAseq data and quantitative (q)PCR to evaluate the transcript levels of theSpiroplasma-encoded RIP genes. One of the five RIP genes (RIP2) was consistently highly expressed independently of wasp parasitism, in two substrains ofsMel. Finally, the RNAseq data revealed evidence consistent with RIP-induced damage in the ribosomal (r)RNA of theSpiroplasma-susceptible, but not theSpiroplasma-resistant, wasp. We conclude that immune priming is unlikely to contribute to theSpiroplasma-mediated protection against wasps, and that the mechanism by whichG. hookeriresists/toleratesSpiroplasmadoes not involve inhibition of RIP transcription.
