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. 2016 Jul 27;90(16):7444-7455.
doi: 10.1128/JVI.00680-16. Print 2016 Aug 15.

Virion Structure of Iflavirus Slow Bee Paralysis Virus at 2.6-Angstrom Resolution

Sergei Kalynych  1 , Antonín Přidal  2 , Lenka Pálková  1 , Yevgen Levdansky  1 , Joachim R de Miranda  3 , Pavel Plevka  4
Affiliations

Virion Structure of Iflavirus Slow Bee Paralysis Virus at 2.6-Angstrom Resolution

Sergei Kalynych et al. J Virol. .

Abstract

The western honeybee (Apis mellifera) is the most important commercial insect pollinator. However, bees are under pressure from habitat loss, environmental stress, and pathogens, including viruses that can cause lethal epidemics. Slow bee paralysis virus (SBPV) belongs to the Iflaviridae family of nonenveloped single-stranded RNA viruses. Here we present the structure of the SBPV virion determined from two crystal forms to resolutions of 3.4 Å and 2.6 Å. The overall structure of the virion resembles that of picornaviruses, with the three major capsid proteins VP1 to 3 organized into a pseudo-T3 icosahedral capsid. However, the SBPV capsid protein VP3 contains a C-terminal globular domain that has not been observed in other viruses from the order Picornavirales The protruding (P) domains form "crowns" on the virion surface around each 5-fold axis in one of the crystal forms. However, the P domains are shifted 36 Å toward the 3-fold axis in the other crystal form. Furthermore, the P domain contains the Ser-His-Asp triad within a surface patch of eight conserved residues that constitutes a putative catalytic or receptor-binding site. The movements of the domain might be required for efficient substrate cleavage or receptor binding during virus cell entry. In addition, capsid protein VP2 contains an RGD sequence that is exposed on the virion surface, indicating that integrins might be cellular receptors of SBPV.

Importance: Pollination by honeybees is needed to sustain agricultural productivity as well as the biodiversity of wild flora. However, honeybee populations in Europe and North America have been declining since the 1950s. Honeybee viruses from the Iflaviridae family are among the major causes of honeybee colony mortality. We determined the virion structure of an Iflavirus, slow bee paralysis virus (SBPV). SBPV exhibits unique structural features not observed in other picorna-like viruses. The SBPV capsid protein VP3 has a large C-terminal domain, five of which form highly prominent protruding "crowns" on the virion surface. However, the domains can change their positions depending on the conditions of the environment. The domain includes a putative catalytic or receptor binding site that might be important for SBPV cell entry.

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Figures

FIG 1
FIG 1
Structure of SBPV virion and icosahedral asymmetric unit. Surface representations of SBPV virions determined in crystal form 1 (A) and crystal form 2 (B) show differences in the positioning of the P domains. The surfaces of the particles are rainbow-colored based on the distance from the particle center. Depressions are shown in blue and peaks in red. (C) Cartoon representation of SBPV icosahedral asymmetric unit. VP1 is shown in blue, VP2 in green, and VP3 in red. The P domain positioned as in crystal form 1 is shown in yellow and in crystal form 2 in orange. Locations of 5-fold, 3-fold, and 2-fold icosahedral symmetry axes are indicated by a pentagon, triangle, and oval, respectively. The RGD motif found in the GH loop of VP2 subunit is shown as space-filling model in magenta. The position of the RGD motif in FMDV is indicated with a dotted black oval. The cyan oval indicates the position of rotation axis relating the two P domain positions. (D) Cartoon representation of P domain rainbow colored from the N terminus in blue to the C terminus in red. Names of secondary structure elements are indicated. (E) Diagram of SBPV genome organization. Capsid proteins VP1, VP2, and VP3 were identified based on their location in the capsid according to the picornavirus convention. Predicted molecular masses of capsid proteins are specified. The location of the P domain of VP3 is indicated. VPg, viral protein, genome linked; L, leader peptide; IRES, internal ribosome entry site; UTR, untranslated region; 3CPRO, 3C protease; RdRP, RNA-dependent RNA polymerase.
FIG 2
FIG 2
Interactions of P domain with the core of the SBPV capsid. (A and B) P domain footprints on the SBPV surface in crystal forms 1 (A) and 2 (B). The images show two-dimensional projections of the SBPV virion surface without the P domains. Residues of capsid proteins VP1, VP2, and VP3 are outlined in blue, green, and red, respectively. Residues involved in interaction with the P domain are shown in yellow. The P domain footprints are outlined by white lines. The border of one VP2-VP3-VP1 protomer is indicated by a light blue line. RGD residues of VP2 are indicated by a magenta line. (C and D) Inner surfaces of P domains in crystal forms 1 (C) and 2 (D), viewed from inside the particle. Residues interacting with the core of the capsid are shown in yellow and the remaining residues in red. Positions of 2-fold, 3-fold, and 5-fold icosahedral symmetry axes are shown as ovals, triangles, and pentagons, respectively. One icosahedral asymmetric unit is outlined by a triangle.
FIG 3
FIG 3
The P domain contains a putative Ser-His-Asp active site that is part of a patch of residues that are conserved among iflaviruses. The conserved residues are highlighted in gray in pentamers of capsid protein protomers in the conformation from crystal form 1 (A) and crystal form 2 (B). Detail of the putative active site with electron density contoured at 2σ (C). A sequence alignment of residues forming the conserved patch in the P domain is also shown (D). HEI, heliconius erato iflavirus; API, antherae pernyi iflavirus. Uniprot accession numbers of the sequences used in the alignment are provided.
FIG 4
FIG 4
Protruding domains of viruses identified in a DALI search based on similarity to SBPV P domain. (A) SBPV; (B) human astrovirus outer coat protein (5EWN) (55); (C) grouper nervous necrosis virus (4RFU) (56); (D) orsay virus (4NWW) (57); (E) P1 domain of human hepatitis E virus (3HAG) (76); (F) P1 domain of human calcivirus (2GH8) (77). Protruding domain of tomato bushy stunt virus (2TBV) (78) is shown for comparison, however, it was not identified in the DALI server search. β-Strands are shown in light gray, helices in orange, and loops in black.
FIG 5
FIG 5
Comparison of SBPV structure to that of dicistrovirus TrV. (A and B) Cartoon representations of icosahedral asymmetric units of SBPV (A) and TrV (B). VP1 subunits are shown in blue, VP2 in green, and VP3 in red. The GH loop of VP2 is highlighted in magenta, the GH loop of VP3 is in cyan, and the N-terminal arms of VP2 are in yellow. (C and D) Domain swapping between SBPV (C) and TrV (D) N-terminal arms of VP2 subunits that mediate interpentamer interactions. The insets show details of hydrogen bonds between β2 of VP2 and βF of VP3. (E and F) Location of DDF sequences, which might be involved in the cleavage of VP0 to VP4 and VP3, on the inside of the capsid of SBPV (E) and TrV (F).
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