Parallel Epigenomic and Transcriptomic Responses to Viral Infection in Honey Bees (Apis mellifera)

Abstract

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.

Dynamic changes in host–virus interactions associated with colony founding and social environment in fire ant queens (Solenopsis invicta)

“…2015). There were 11 genes in common between the two studies (Table S5): this overlap was larger than expected of two independent groups but not statistically significant (hypergeometric test: representation factor: 1.3, P  =   0.249).…”

“…These biological functions have been linked to the antiviral response of honeybees to Israeli Acute Paralysis Virus in a recent study (Galbraith et al. 2015). Additionally, genes associated with diet and fat body metabolism ( CdsA , Hr96 , Cul1 , bgm , schlank ) and reproductive activation ( CkIIα , nos , retn , fz2 ) were differentially regulated in SINV‐1 and SINV‐2 infected queens.…”

“…2013), and similar results were found in honey bees infected with Israeli Acute Paralysis Virus (Galbraith et al. 2015). However, genes up‐regulated by these different viruses are not the same.…”

“…Clustering analyses, pairwise comparisons and gene ontology analysis were performed (see Data S2) and we compared results of our study to a suite of genes identified as differentially expressed in response to Israeli Acute Paralysis Virus infection in the honey bee Apis mellifera (Galbraith et al. 2015). …”

Israeli acute paralysis virus associated paralysis symptoms, viral tissue distribution and Dicer-2 induction in bumblebee workers (Bombus terrestris)

“…The nomenclature of this virus is largely based on its symptoms that are similar to ABPV. Both viruses can induce abnormal body trembling (Galbraith et al, 2015;Li et al, 2013;Maori et al, 2009). In bumblebees, injection of a low dose of IAPV particles into healthy workers could induce rapid mortality (Niu et al, 2014a).…”