Virion Structure of Black Queen Cell Virus, a Common Honeybee Pathogen

Abstract

Viral diseases are a major threat to honeybee (Apis mellifera) populations worldwide and therefore an important factor in reliable crop pollination and food security. Black queen cell virus (BQCV) is the etiological agent of a fatal disease of honeybee queen larvae and pupae. The virus belongs to the genus Triatovirus from the family Dicistroviridae, which is part of the order Picornavirales. Here we present a crystal structure of BQCV determined to a resolution of 3.4 Å. The virion is formed by 60 copies of each of the major capsid proteins VP1, VP2, and VP3; however, there is no density corresponding to a 75-residue-long minor capsid protein VP4 encoded by the BQCV genome. We show that the VP4 subunits are present in the crystallized virions that are infectious. This aspect of the BQCV virion is similar to that of the previously characterized triatoma virus and supports the recent establishment of the separate genus Triatovirus within the family Dicistroviridae. The C terminus of VP1 and CD loops of capsid proteins VP1 and VP3 of BQCV form 34-Å-tall finger-like protrusions at the virion surface. The protrusions are larger than those of related dicistroviruses.IMPORTANCE The western honeybee is the most important pollinator of all, and it is required to sustain the agricultural production and biodiversity of wild flowering plants. However, honeybee populations worldwide are suffering from virus infections that cause colony losses. One of the most common, and least known, honeybee pathogens is black queen cell virus (BQCV), which at high titers causes queen larvae and pupae to turn black and die. Here we present the three-dimensional virion structure of BQCV, determined by X-ray crystallography. The structure of BQCV reveals large protrusions on the virion surface. Capsid protein VP1 of BQCV does not contain a hydrophobic pocket. Therefore, the BQCV virion structure provides evidence that capsid-binding antiviral compounds that can prevent the replication of vertebrate picornaviruses may be ineffective against honeybee virus infections.

Cryo-electron Microscopy Structures of Novel Viruses from Mud Crab Scylla paramamosain with Multiple Infections

“…Virus-receptor binding and genome release can be prevented when inhibitors bind to this pocket (33,34). Considering the lack of the hydrophobic pocket in VP1, similar to other reported dicistroviruses (7,8,11,12), MCDV shall have different receptor binding sites. A previous report has revealed that the finger-like protuberance of TrV plays roles in virus-host interactions (8), whereas the C terminus of MCDV VP3 occupies the location of finger-like protuberance.…”

“…Besides MCDV, structures of four other viruses from the family Dicistroviridae have been determined to date ( Fig. 3): Israeli acute bee paralysis virus (IAPV) (11), triatoma virus (TrV) (8), black queen cell virus (BQCV) (12), and cricket paralysis virus (CrPV) (7). Among these, a stable VP4 disk-like structure was seen only in IAPV and CrPV, while atomic models could not be built for TrV and BQCV.…”

“…In BQCV, the finger-like protuberances near the 5-fold axes are composed of the short C-terminal regions of VP1 and the CD loops of VP1 and VP3. These density features are most obvious in BQCV, less prominent in TrV and IAPV, and almost invisible in CrPV (12). The finger-like protuberances of TrV were speculated to play a role in virus-host interactions, in particular those involved in binding to the entry receptor (8).…”

“…injection of MCTV (10 4 copies/g of body weight), whereas the controls received PBS. Nine crabs were selected randomly at each time point (4,12,24,48,72, and 96 h postinoculation), and total RNA was extracted according to the manufacturer's instructions. Reverse transcription was performed using the PrimeScript RT reagent kit (TaKaRa, Japan) according to the manufacturer's instructions.…”

Virucides in apiculture: persistence of surrogate enterovirus under simulated field conditions

“…Physicochemical properties of both f. Iflaviridae and f. Dicistroviridae have not been fully established . However, phylogenetic analyses based on the virion structure comparing honeybee iflaviruses and dicistroviruses to picornaviruses showed that DWV and BQCV are structurally related to vertebrate picornaviruses (f. Picornaviridae ) . In general, picornaviruses are considered to be relatively resistant to chemical germicides, mainly as a consequence of the absence of the lipid envelope of virions .…”