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Parallel Epigenomic and Transcriptomic Responses to Viral Infection in Honey Bees (Apis mellifera)
Populations of honey bees are declining throughout the world, with US beekeepers losing 30% of their colonies each winter. Though multiple factors are driving these colony losses, it is increasingly clear that viruses play a major role. However, information about the molecular mechanisms mediating antiviral immunity in honey bees is surprisingly limited. Here, we examined the transcriptional and epigenetic (DNA methylation) responses to viral infection in honey bee workers. One-day old worker honey bees were fed solutions containing Israeli Acute Paralysis Virus (IAPV), a virus which causes muscle paralysis and death and has previously been associated with colony loss. Uninfected control and infected, symptomatic bees were collected within 20–24 hours after infection. Worker fat bodies, the primary tissue involved in metabolism, detoxification and immune responses, were collected for analysis. We performed transcriptome- and bisulfite-sequencing of the worker fat bodies to identify genome-wide gene expression and DNA methylation patterns associated with viral infection. There were 753 differentially expressed genes (FDR<0.05) in infected versus control bees, including several genes involved in epigenetic and antiviral pathways. DNA methylation status of 156 genes (FDR<0.1) changed significantly as a result of the infection, including those involved in antiviral responses in humans. There was no significant overlap between the significantly differentially expressed and significantly differentially methylated genes, and indeed, the genomic characteristics of these sets of genes were quite distinct. Our results indicate that honey bees have two distinct molecular pathways, mediated by transcription and methylation, that modulate protein levels and/or function in response to viral infections.
Author Summary
Honey bees are a critical pollinator of a wide variety of agricultural crops, but beekeepers experience heavy annual losses of honey bee colonies. Several factors are associated with colony losses, in particular infection with Israeli Acute Paralysis Virus (IAPV). Despite the importance of viruses to honey bee health, our understanding of the molecular mechanisms mediating host-pathogen interactions is limited. Here, we characterized the epigenomic and transcriptomic responses of honey bees to short term (<24 hour) IAPV infection. We found significant expression differences in 753 genes between infected and control bees, including genes involved in immune and epigenetic pathways. However, IAPV-regulated genes did not overlap significantly with genes that respond to bacterial or microsporidian infection, suggesting that honey bees utilize distinct pathways for different immune challenges. Additionally, DNA methylation status of 156 genes changed significantly, including several genes that have been linked to antiviral immune responses in humans. Interestingly, there was no significant overlap between the differentially methylated and differentially expressed genes, suggesting that honey bees may possess a parallel genomic mechanisms to respond to viral infection.
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