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

Abstract

Bee viral ecology is a fascinating emerging area of research: viruses exert a range of effects on their hosts, exacerbate the impacts of other environmental stressors, and, importantly, are readily shared across multiple bee species in a community. However, our understanding of bee viral communities is limited, as it is primarily derived from studies of North American and European Apis mellifera populations. Here, we examined viruses in populations of A. mellifera and 11 other bee species from 9 countries, across 5 continents and Oceania. We developed a novel pipeline to rapidly, inexpensively, and robustly screen for bee viruses. This pipeline includes purification of encapsulated RNA/DNA viruses, sequence-independent amplification, high throughput sequencing, integrated assembly of contigs, and filtering to identify contigs specifically corresponding to viral sequences. We identified sequences corresponding to (+)ssRNA, (-)ssRNA, dsRNA, and ssDNA viruses. Overall, we found 127 contigs corresponding to novel viruses (i.e. previously not observed in bees), with 29 represented by >0.1 % of the reads in a given sample. These viruses and viral families were distributed across multiple regions and species. This study provides a robust pipeline for metagenomics analysis of viruses, and greatly expands our understanding of the diversity of viruses found in bee communities.

Hymenoptera associated eukaryotic virome lacks host specificity

“…Recent advancements in sequencing technologies and metagenomics have accelerated virus discovery in bees and a number of studies have attempted to describe the viral diversity associated with bees. These studies were able to expand the range of known honey bee viruses significantly and aside from numerous viruses belonging to the order Picornavirales, numerous other RNA viruses have been discovered belonging to the orders Bunyavirales, Mononegavirales (containing the family Rhabdoviridae) and Articulavirales (containing the family Orthomyxoviridae), and several unclassified RNA viruses such as LSV (33)(34)(35)(36)(37). DNA viruses have also been described, such as Apis mellifera Filamentous virus (AmFV) (38), and numerous single-stranded DNA viruses (39).…”

Metatranscriptome Analysis of Sympatric Bee Species Identifies Bee Virus Variants and a New Virus, Andrena-Associated Bee Virus-1

“…Most of the characterized bee-infecting viruses are positive-sense, single-stranded RNA viruses (+ssRNA) in the Picornaviridae family including Dicistroviruses (acute bee paralysis virus (ABPV), black queen cell virus (BQCV), Israeli acute paralysis virus (IAPV), and Kashmir bee virus (KBV)); the Iflaviruses (deformed wing virus (DWV), Kakugo virus, Varroa destructor virus-1/DWV-B, sacbrood virus (SBV), and slow bee paralysis virus (SBPV)); and taxonomically unclassified viruses (chronic bee paralysis virus (CBPV) and the Lake Sinai viruses (LSVs)) (reviewed in [42,45]). There are very few identified bee-infecting viruses with DNA genomes, which include Apis mellifera filamentous virus (AmFV) [46,47] and Osmia cornuta nudivirus [48,49]. Several honey bee-associated viruses have been detected in wild bee species including BQCV, LSV, SBV, and AmFV in Andrena vaga, and LSV and AmFV in Andrena ventralis in Belgium [50], and DWV, BQCV, and SBV in Andrena spp.…”

“…Several honey bee-associated viruses have been detected in wild bee species including BQCV, LSV, SBV, and AmFV in Andrena vaga, and LSV and AmFV in Andrena ventralis in Belgium [50], and DWV, BQCV, and SBV in Andrena spp. sampled in the eastern United States [48,51,52,53,54,55,56]. It is unclear whether virus detections in most of these studies were indicative of active infections in mining bees since viral replication was not assessed by negative strand-specific RT-PCR or inferred by quantitative PCR, though DWV replication was detected in Andrena haemorrhoa in Germany [57].…”

“…Recent high-throughput sequencing studies identified additional honey bee-infecting +ssRNA viruses including Bee macula-like virus (BeeMLV) in the Tymoviridae family, Apis mellifera flavivirus, and Apis mellifera nora virus 1 [58,59], as well as the first negative-sense single-stranded RNA viruses (-ssRNA) including Apis mellifera rhabdovirus-1 (ARV-1) [59], also known as Bee rhabdovirus (BRV-1) [60] and Apis mellifera rhabdovirus-2 (ARV-2) (reviewed in [43]). To date, the majority of sequencing efforts aimed at identifying bee-associated viruses have utilized honey bee and the ectoparasitic mite (Varroa destructor) samples [48,59,60,61,62,63] (reviewed in [43]). Sequencing a greater variety of bee and other insect species indicates that many honey bee-infecting viruses have a broader host range that includes bumble bees (Bombus spp.…”

Prevalence of bee viruses in Apis cerana cerana populations from different locations in the Fujian Province of China

“…Honeybee viral diseases are creating a major problem in the beekeeping industry in most regions around the globe, causing economic losses worldwide (Gisder & Genersch, , ; Martinello et al., ). The number of RNA and DNA viruses that have impacted bee species as investigated by metagenomics and applied next‐generation sequencing technologies are increasing; at present, 27 honeybee viruses have been identified (Galbraith et al., ; McMenamin & Flenniken, ; Schoonvaere, Smagghe, Francis, & de Graaf, ). The seven most common and destructive bee viruses are sacbrood virus (SBV), deformed wing virus (DWV), black queen cell virus (BQCV), Israeli acute paralysis virus (IAPV), chronic bee paralysis virus (CBPV), acute bee paralysis virus (ABPV), and Kashmir bee virus (KBV) (Ai, Yan, & Han, ).…”