A Diverse Range of Novel RNA Viruses in Geographically Distinct Honey Bee Populations

Abstract

Understanding the diversity and consequences of viruses present in honey bees is critical for maintaining pollinator health and managing the spread of disease. The viral landscape of honey bees (Apis mellifera) has changed dramatically since the emergence of the parasitic mite Varroa destructor, which increased the spread of virulent variants of viruses such as deformed wing virus. Previous genomic studies have focused on colonies suffering from infections by Varroa and virulent viruses, which could mask other viral species present in honey bees, resulting in a distorted view of viral diversity. To capture the viral diversity within colonies that are exposed to mites but do not suffer the ultimate consequences of the infestation, we examined populations of honey bees that have evolved naturally or have been selected for resistance to Varroa. This analysis revealed seven novel viruses isolated from honey bees sampled globally, including the first identification of negative-sense RNA viruses in honey bees. Notably, two rhabdoviruses were present in three geographically diverse locations and were also present in Varroa mites parasitizing the bees. To characterize the antiviral response, we performed deep sequencing of small RNA populations in honey bees and mites. This provided evidence of a Dicer-mediated immune response in honey bees, while the viral small RNA profile in Varroa mites was novel and distinct from the response observed in bees. Overall, we show that viral diversity in honey bee colonies is greater than previously thought, which encourages additional studies of the bee virome on a global scale and which may ultimately improve disease management.IMPORTANCE Honey bee populations have become increasingly susceptible to colony losses due to pathogenic viruses spread by parasitic Varroa mites. To date, 24 viruses have been described in honey bees, with most belonging to the order Picornavirales. Collapsing Varroa-infected colonies are often overwhelmed with high levels of picornaviruses. To examine the underlying viral diversity in honey bees, we employed viral metatranscriptomics analyses on three geographically diverse Varroa-resistant populations from Europe, Africa, and the Pacific. We describe seven novel viruses from a range of diverse viral families, including two viruses that are present in all three locations. In honey bees, small RNA sequences indicate that these viruses are processed by Dicer and the RNA interference pathway, whereas Varroa mites produce strikingly novel small RNA patterns. This work increases the number and diversity of known honey bee viruses and will ultimately contribute to improved disease management in our most important agricultural pollinator.

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

“…Eleven viruses have been found in wild bees, less than half of the number reported from Apis mellifera (>26; reviewed in Tehel et al, 2016;Remnant et al, 2017), and data show there is cross-species transmission (Bailey and Gibbs, 1964). Managed bees are found to frequently have a negative effect on wild bees due to their pathogens (Mallinger et al, 2017), and the presence of managed bees can alter pathogen loads in native bees by a number of different mechanisms including facilitation, spillover and spill back (Graystock et al, 2016).…”

Investigating the viral ecology of global bee communities with high-throughput metagenomics

“…Sequence homology analyses of these 29 novel virus contigs revealed 9 different viral families among these bee associated viruses, including 6 viral families that had not been heretofore observed in bees (noted in Supplementary Table 3). Of these, one virus from the family Rhaboviridae (BRV) was recently described in A. mellifera populations in the United States, Israel, South Africa, Tonga and the Netherlands, and B. impatiens populations in the United States [6,55]. Of the 29 novel virus contigs, 6 were found to contain a putative RdRp that could be used for phylogenetic analyses.…”

“…Only recently have negative sense RNA ((-)ssRNA) viruses been identified in bees [6,29]. One of these, Apis mellifera Rhabdovirus 1 (ARV-1), from the family Rhabdoviridae [6], was detected in A. mellifera populations in South Africa, Tonga, and the Netherlands. It was also recently identified in bee populations in Israel and the United States [55].…”

“…Populations of bees around the world are exhibiting declines, which are the result of multiple interacting factors, including pressure from pathogens [1]. To date, more than 24 viruses have been identified in western honey bees (Apis mellifera) [2][3][4][5][6][7]. These viral infections can result in a range of symptoms, from no obvious phenotype to rapid death and colony loss, depending on the viral species, viral strain, physiological state of the host, and presence of other stressors (reviewed in [8]).…”

“…Using this approach, several recent studies have identified novel viruses in populations of bees (A. mellifera, Bombus terrestris, Bombus pascuorum, Osmia cornuta, and Andrena vaga) collected from sites in the Netherlands, South Africa, Tonga, Israel and Belgium [6,29,34]. However, while these studies have provided valuable information about viral communities within particular species or regions, they are limited in scope, in that they focus on a single bee species in multiple locations (A. mellifera populations in Israel [34] or the Netherlands, South Africa, and Tonga [6]) or a selection of wild bees in a single region (Belgium [29]). Furthermore, two of these studies [6,29] did not purify viral particles prior to sequencing, and thus had samples with a high percentage of reads corresponding to the host bee species, which can limit detection of rare viral species.…”