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.
Highlights
The Western honeybee, Apis mellifera, is the most important managed insect pollinator worldwide
The analysis was carried out using whole-body RNA extracted from individual honeybee pupae sampled at 9 dpi
Our results indicate that evolutionarily-related Iflaviruses Sacbrood virus (SBV) and Deformed wing virus (DWV), evoke markedly different transcriptional responses in their honeybee host, including effects on the expression of immune-related genes
Summary
The Western honeybee, Apis mellifera, is the most important managed insect pollinator worldwide. In recent decades a global decline in the number of honeybee colonies was reported, threatening security of the global food supply (Vanbergen et al, 2013), with pathogens—in particular viruses—contributing significantly to these declines. These viral pathogens are predominantly single-stranded, positive sense RNA viruses of the families Dicistroviridae and Iflaviridae, and may exhibit differing virulence levels, causing infections ranging from asymptomatic to acute and resulting in rapid insect death (McMenamin & Genersch, 2015). It is likely that SBV is transmitted from the larvae killed by SBV to in-hive worker honeybees, which subsequently transmit the virus to young larvae (Bailey, 1969)
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