Evidence For Long-Lasting Transgenerational Antiviral Immunity in Insects

Abstract

Summary Transgenerational immune priming (TGIP) allows memory-like immune responses to be transmitted from parents to offspring in many invertebrates. Despite increasing evidence for TGIP in insects, the mechanisms involved in the transfer of information remain largely unknown. Here, we show that Drosophila melanogaster and Aedes aegypti transmit antiviral immunological memory to their progeny that lasts throughout generations. We observe that TGIP, which is virus and sequence specific but RNAi independent, is initiated by a single exposure to disparate RNA viruses and also by inoculation of a fragment of viral double-stranded RNA. The progeny, which inherit a viral DNA that is only a fragment of the viral RNA used to infect the parents, display enriched expression of genes related to chromatin and DNA binding. These findings represent a demonstration of TGIP for RNA viruses in invertebrates, broadly increasing our understanding of the immune response, host genome plasticity, and antiviral memory of the germline.

Between virus correlations in the outcome of infection across host species: Evidence of virus by host species interactions

“… 2017 ; Mondotte et al. 2020 ). Three of the viruses tested here are isolates of Drosophila C virus (DCV‐C, DCV‐EB, and DCV‐M), a well‐studied virus isolated from Drosophila melanogaster (Johnson and Christian 1999 ), and represent the most divergent available isolates of this virus species.…”

Profile of Small RNAs, vDNA Forms and Viral Integrations in Late Chikungunya Virus Infection of Aedes albopictus Mosquitoes

“…A total of 30 and 534 transcripts displayed significant differential abundance (SDA) of siRNAs in CHIKV-infected ovaries and carcasses, respectively, representing six over-represented GO terms, including “DNA helicase activity”, “DNA recombination”, and “DNA repair” ( Table S4 ). Interestingly, transcriptional regulation of genes associated with DNA repair and chromatin function has been recently linked to ovaries and carcasses, respectively [ 93 ] ( Figure 4 A,B, Table S3 ).…”

“…GO enrichment analyses reveled an over representation representation of 6 terms, including “DNA helicase activity”, “DNA recombination”, and “DNA repair” ( Table S4 ). Interestingly, transcriptional regulation of genes associated with DNA repair and chromatin function has been recently linked to transgenerational immunopriming (TGIP) in D. melanogaster after infection with Sindbis virus, an Alphavirus-like CHIKV, which was clearly demonstrated only in females [ 93 ]. Thus, it is tempting to speculate that during persistent infection of female mosquitoes, there is transcriptional regulation of functions that not only helps with maintenance of infection, but also prepares to TGIP.…”

Exposure to Inactivated Deformed Wing Virus Leads to Trans-Generational Costs but Not Immune Priming in Honeybees (Apis mellifera)

“…Although TGIP with viruses have been studied less, recently the existence of antiviral TGIP in fruit flies and mosquitoes was shown, lasting for multiple generations (Mondotte et al, 2020). The mechanism was found to be virus specific, RNAi independent and was shown with multiple positive strand RNAviruses, which the DWV also is.…”

“…Further, if antiviral TGIP can persist for multiple generations, exposure to DWV in prior generations may have already primed the queens, explaining the lack of further priming effects. Future studies could investigate whether viral derived DNA fragments are present in offspring of honeybee queens challenged with live virus or viral dsRNA, as was seen in the fruit flies by Mondotte et al (2020).…”