Foreign Ribosome Inactivating Proteins as immune effectors in insects

Abstract

Ribosome inactivating proteins (RIPs) are RNA N-glycosidases that depurinate an adenine residue in the conserved alpha-sarcin/ricin loop (SRL) of rRNA. This ribosomal modification inhibits protein synthesis. During the last years, we have reported the existence of these toxins in insects, where their presence is restricted to mosquitoes from the Culicinae subfamily (e.g. Aedes aegypti) and whiteflies from Aleyrodidae family (e.g. Bemisia tabaci). Combination of phylogeny and synteny analyses showed that both groups of genes are derived from two independent horizontal gene transfer (HGT) events. Interestingly, we found that RIP encoding genes have been evolving under purifying selection, indicating that they have a positive impact on fitness of host organisms. We also demonstrated that A. aegypti RIP genes are transcribed and their transcripts are polyadenylated. Although the biological roles of these toxins remain open to speculation, defense activities have been postulated for plant and bacterial RIPs. Based on these pieces of evidence, we hypothesize that RIPs play a similar protective role in insects. In this work, we report the occurrence of a third HGT event in Sciaroidea superfamily, supporting that RIP genes fulfill an important functional niche in insects. Analysis on transcriptomic experiments from the three groups of insects indicate a convergence in expression profiles which are compatible with immune effectors. Finally, we show the induction in RIP expression after infection with pathogens. Moreover, we show transcriptomic evidence of parasite SRL depurination. Altogether, our results strongly support the role of these foreign genes as immune effectors that confer fitness advantage to host insects.