Abstract

The ectoparasitic mite, Varroa destructor, feeds directly on honey bees and serves as a vector for transmitting viruses among them. The Varroa mite causes relatively little damage to its natural host, the Eastern honey bee (Apis cerana) but it is the most devastating pest for the Western honey bee (Apis mellifera). Using Illumina HiSeq sequencing technology, we conducted a metatranscriptome analysis of the microbial community associated with Varroa mites. This study led to the identification of a new Chinese strain of Varroa destructor virus-2 (VDV-2), which is a member of the Iflaviridae family and was previously reported to be specific to Varroa mites. A subsequent epidemiological investigation of Chinese strain of VDV-2 (VDV-2-China) showed that the virus was highly prevalent among Varroa populations and was not identified in any of the adult workers from both A. mellifera and A. cerana colonies distributed in six provinces in China, clearly indicating that VDV-2-China is predominantly a Varroa-adapted virus. While A. mellifera worker pupae exposed to less than two Varroa mites tested negative for VDV-2-China, VDV-2-China was detected in 12.5% of the A. mellifera worker pupae that were parasitized by more than 10 Varroa mites, bringing into play the possibility of a new scenario where VDV-2 could be transmitted to the honey bees during heavy Varroa infestations. Bioassay for the VDV-2-China infectivity showed that A. cerana was not a permissive host for VDV-2-China, yet A. mellifera could be a biological host that supports VDV-2-China’s replication. The different replication dynamics of the virus between the two host species reflect their variation in terms of susceptibility to the virus infection, posing a potential threat to the health of the Western honey bee. The information gained from this study contributes to the knowledge concerning genetic variabilities and evolutionary dynamics of Varroa-borne viruses, thereby enhancing our understanding of underlying molecular mechanisms governing honey bee Varroosis.

Highlights

  • The ectoparasitic mite, Varroa destructor [1], is the world’s most detrimental pest of the Western honey bee, Apis mellifera, which is the primary managed pollinator in agricultural systems and natural ecosystems

  • The open reading frame (ORF) encoding a polyprotein of 2995 amino acid residues is flanked by approximately 413 nt of 5 -UTR and 147 nt of 3 -UTR, which is typical for the genome organization of Iflaviridae

  • The ORF encoding a polyprotein of 2995 amino acid residues is flanked by approximately 413 nt of 5′-UTR and 147 nt of 3′-UTR, which is typical for the genome organization of Iflaviridae

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Summary

Introduction

The ectoparasitic mite, Varroa destructor (hereafter referred to as the Varroa mite) [1], is the world’s most detrimental pest of the Western honey bee, Apis mellifera, which is the primary managed pollinator in agricultural systems and natural ecosystems. Since its host expansion from the Eastern honey bee Apis cerana to A. mellifera in the mid-1900s, the Varroa mite has spread to every region where honey bees are kept with the exception of Australia, and has been catastrophic for the beekeeping industry worldwide [2,3,4]. A. cerana, they inflict profound damage on the A. mellifera hosts through the intake of their fat body tissue and hemolymph from immature brood and adult honey bees [5,6]. Varroa mite infestations in A. mellifera colonies have been cited as strong predictive markers for honey bee colony mortality during winter [14,15,16,17,18]. The massive Varroa mite infestation causes a devastating honey bee disease called Varroosis and has destroyed millions of A. mellifera colonies since its establishment in various parts of the world [19]

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