The Iflaviruses Sacbrood virus and Deformed wing virus evoke different transcriptional responses in the honeybee which may facilitate their horizontal or vertical transmission

Abstract

Sacbrood virus (SBV) and Deformed wing virus (DWV) are evolutionarily related positive-strand RNA viruses, members of the Iflavirus group. They both infect the honeybee Apis mellifera but have strikingly different levels of virulence when transmitted orally. Honeybee larvae orally infected with SBV usually accumulate high levels of the virus, which halts larval development and causes insect death. In contrast, oral DWV infection at the larval stage usually causes asymptomatic infection with low levels of the virus, although high doses of ingested DWV could lead to DWV replicating to high levels. We investigated effects of DWV and SBV infection on the transcriptome of honeybee larvae and pupae using global RNA-Seq and real-time PCR analysis. This showed that high levels of SBV replication resulted in down-regulation of the genes involved in cuticle and muscle development, together with changes in expression of putative immune-related genes. In particular, honeybee larvae with high levels of SBV replication, with and without high levels of DWV replication, showed concerted up-regulated expression of antimicrobial peptides (AMPs), and down-regulated expression of the prophenoloxidase activating enzyme (PPAE) together with up-regulation of the expression of a putative serpin, which could lead to the suppression of the melanisation pathway. The effects of high SBV levels on expression of these immune genes were unlikely to be a consequence of SBV-induced developmental changes, because similar effects were observed in honeybee pupae infected by injection. In the orally infected larvae with high levels of DWV replication alone we observed no changes of AMPs or of gene expression in the melanisation pathway. In the injected pupae, high levels of DWV alone did not alter expression of the tested melanisation pathway genes, but resulted in up-regulation of the AMPs, which could be attributed to the effect of DWV on the regulation of AMP expression in response to wounding. We propose that the difference in expression of the honeybee immune genes induced by SBV and DWV may be an evolutionary adaptation to the different predominant transmission routes used by these viruses.

Decoupling the effects of nutrition, age and behavioral caste on honey bee physiology and immunity

“…Thus, it is either possible that the higher expression of the immune genes observed in foragers can be a response to increased DWV infection, or that this immune expression occurs before the increase in viral infection. Still, the close association observed between ppo expression and DWV titers, which has been documented in winter bees (Steinman 2015) is remarkable and consistent with the association between the cellular immune response and viral infections reported previously in honey bees and other insects [110–113].…”

Virus and dsRNA-triggered transcriptional responses reveal key components of honey bee antiviral defense

“…The DEGs identified in SINV-GFP-infected bees 72 hpi were compared to those identified in naturally IAPV-infected bees (Chen et al . 2014, orange) 9 , bees infected with IAPV via oral inoculation (Galbraith et al ., 2015, green) 24 , SBV and DWV-infected bees (Ryabov et al ., 2016, pink) 25 , and a common DEG list that was compiled from 19 gene expression data sets including Varroa destructor -parasitized and virus-infected bees (Doublet et al ., 2017) 92 (purple). Lists of DEGs from all studies that were used to generate the Venn diagram 131 are provided in Supplementary Tables S14 and Venn diagram results are listed in S15. …”

Viral transmission in honey bees and native bees, supported by a global black queen cell virus phylogeny

“…The Kenyan clade of honey bee adults and brood share related BQCV strains with their Varroa mites. The mite Varroa destructor vectors several viruses (McMenamin and Genersch, ; Ryabov et al ., ). Additionally, we found that BQCV isolated from the fungus Ascosphaera apis from honey bees in Maryland clustered with our New York honey bee and native bee samples, illustrating the close relatedness of the virus and potential for virus crossover between fungal and bee species.…”

“…While the virus can be detected in honey bee workers, it is not typically a lethal infection in this caste. DWV is often asymptomatic and found at low levels in a honey bee colony, however, direct injection by the Varroa mite causes high pathogenicity (Ryabov et al, 2016). This is the most common virus found in non-Apis hosts, present in 19 species (Tehel et al, 2016).…”