Capsid structure of a fungal dsRNA megabirnavirus reveals its previously unidentified surface architecture

Abstract

Rosellinia necatrix megabirnavirus 1-W779 (RnMBV1) is a non-enveloped icosahedral double-stranded (ds)RNA virus that infects the ascomycete fungus Rosellinia necatrix, a causative agent that induces a lethal plant disease white root rot. Herein, we have first resolved the atomic structure of the RnMBV1 capsid at 3.2 Å resolution using cryo-electron microscopy (cryo-EM) single-particle analysis. Compared with other non-enveloped icosahedral dsRNA viruses, the RnMBV1 capsid protein structure exhibits an extra-long C-terminal arm and a surface protrusion domain. In addition, the previously unrecognized crown proteins are identified in a symmetry-expanded cryo-EM model and are present over the 3-fold axes. These exclusive structural features of the RnMBV1 capsid could have been acquired for playing essential roles in transmission and/or particle assembly of the megabirnaviruses. Our findings, therefore, will reinforce the understanding of how the structural and molecular machineries of the megabirnaviruses influence the virulence of the disease-related ascomycete fungus.

High-resolution comparative atomic structures of two Giardiavirus prototypes infectingG. duodenalisparasite

“…The electropositive capsid surface could have a role in recruiting negatively charged NTPs to the pores, as previously suggested for icosahedral dsRNA viruses [23,25]. A capsid of the human immunodeficiency virus (HIV) also has negatively charged pores for recruiting deoxynucleotide triphosphates (dNTPs) for its intraparticle genome synthesis [48,49].…”

“…The extracellular transmission mechanism of Totiviridae and toti-like viruses is still unclear; however, these surface loops could have profound roles in extracellular cell-to-cell transmission, such as budding, membrane penetration, and receptor-binding cell entry. The toti-like virus OmRV and IMNV and the megabirnavirus RnMBV-1 also possess additional CrP on their surface, which may facilitate extracellular or horizontal cell-to-cell transmission in multicellular hosts [23,24,43]. Considering that the GLV capsid does not express and has no extra surface CrP structurally (Fig.…”

“…These positive and negative surface properties are constantly observed in other Totiviridae viruses [25,35,40], which implies their essential functions. The dsRNA viruses infecting multicellular hosts possess similar pores composed of two consecutive arginine residues (RR motif); however, they are obstructed [23,25,34,38]. In human picobirnavirus and toti-like viruses, simple conformational changes on the pore assist them in opening [25,38].…”

“…Intraparticle genome synthesis and the RdRp/pore are thought to be fundamental requirements of non-enveloped icosahedral dsRNA viruses for sequestering the host's innate immune system that could be triggered by viral dsRNAs [25,37]. However, the pores of some icosahedral dsRNA viruses that infect multicellular hosts (e.g., toti-like viruses) are obstructed [23,25,38]. Considering the unique phylogenetic clade of GLV in evolution, the surface and pore structure of GLV are key to deeply elucidating the infection and intraparticle genome synthesis mechanisms in the transmission steps of Totiviridae and toti-like viruses.…”

“…Totivirdiae viruses, which hints at an understanding of the evolutionary relevance of Totiviridae viruses and toti-like viruses [16,20]. Almost all Totiviridae viruses infecting unicellular yeast and protists merely adopt intracellular transmission by frequent mating of cell division and cell fusion in yeasts and protists [17,21,22], while the toti-like viruses infecting multicellular hosts have acquired an extracellular phase and likely transmit adjacent cells using membranepenetration and/or receptor-binding mechanisms [23][24][25][26]. Intriguingly, although GLV infects a unicellular protozoa, it can be efficiently transmitted extracellularly [15,27].…”