Study of the Metatranscriptome of Eight Social and Solitary Wild Bee Species Reveals Novel Viruses and Bee Parasites

Abstract

Bees are associated with a remarkable diversity of microorganisms, including unicellular parasites, bacteria, fungi, and viruses. The application of next-generation sequencing approaches enables the identification of this rich species composition as well as the discovery of previously unknown associations. Using high-throughput polyadenylated ribonucleic acid (RNA) sequencing, we investigated the metatranscriptome of eight wild bee species (Andrena cineraria, Andrena fulva, Andrena haemorrhoa, Bombus terrestris, Bombus cryptarum, Bombus pascuorum, Osmia bicornis, and Osmia cornuta) sampled from four different localities in Belgium. Across the RNA sequencing libraries, 88–99% of the taxonomically informative reads were of the host transcriptome. Four viruses with homology to insect pathogens were found including two RNA viruses (belonging to the families Iflaviridae and Tymoviridae that harbor already viruses of honey bees), a double stranded DNA virus (family Nudiviridae) and a single stranded DNA virus (family Parvoviridae). In addition, we found genomic sequences of 11 unclassified arthropod viruses (related to negeviruses, sobemoviruses, totiviruses, rhabdoviruses, and mononegaviruses), seven plant pathogenic viruses, and one fungal virus. Interestingly, nege-like viruses appear to be widespread, host-specific, and capable of attaining high copy numbers inside bees. Next to viruses, three novel parasite associations were discovered in wild bees, including Crithidia pragensis and a tubulinosematid and a neogregarine parasite. Yeasts of the genus Metschnikowia were identified in solitary bees. This study gives a glimpse of the microorganisms and viruses associated with social and solitary wild bees and demonstrates that their diversity exceeds by far the subset of species first discovered in honey bees.

An ancient lineage of highly divergent parvoviruses infects both vertebrate and invertebrate hosts

“…Interestingly, another endogenous element of parvoviral origin was detected at the same locus. This element encodes an intact, potentially fully-expressible NS gene, homologous to the NS1 of ambidensoviruses (genus Ambidensovirus ) and discloses similarity to a recently reported ambidensovirus species, detected only at cDNA level in the transcriptome of two bumble bee species ( Bombus cryptarum and B. terrestris ) (22). An additional ORF was present in this ambidensoviral element, overlapping the reputative NS1 gene, which harboured no significant similarity to any sequences deposited to GenBank to date.…”

Diversity and Global Distribution of Viruses of the Western Honey Bee, Apis mellifera

“…This avalanche of virus discoveries covers all organisms and environments, surpassing the capacity of the existing taxonomic structures to catalogue and organize this data, while the discoveries themselves add resolution and power to the bioinformatics tools for further discoveries, in new or old datasets. For bees, this process started in earnest with the mass screening for possible virological links to colony collapse disorder (CCD) [43], with each subsequent effort adding to the virus diversity in bees or its ectoparasite Varroa destructor [32][33][34][44][45][46][47][48], culminating in the list in Table 1. However, this is almost certainly a vast underestimate of the true total virus diversity in bees, judging by the rate of new discoveries [49], not only of virus species and genera [50] but also of families and orders [23].…”

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).…”