The structure and evolution of the major capsid protein of a large, lipid-containing DNA virus

Abstract

Paramecium bursaria Chlorella virus type 1 (PBCV-1) is a very large, icosahedral virus containing an internal membrane enclosed within a glycoprotein coat consisting of pseudohexagonal arrays of trimeric capsomers. Each capsomer is composed of three molecules of the major capsid protein, Vp54, the 2.0-Å resolution structure of which is reported here. Four N-linked and two O-linked glycosylation sites were identified. The N-linked sites are associated with nonstandard amino acid motifs as a result of glycosylation by virus-encoded enzymes. Each monomer of the trimeric structure consists of two eight-stranded, antiparallel ␤-barrel, ''jelly-roll'' domains related by a pseudo-sixfold rotation. The fold of the monomer and the pseudo-sixfold symmetry of the capsomer resembles that of the major coat proteins in the double-stranded DNA bacteriophage PRD1 and the double-stranded DNA human adenoviruses, as well as the viral proteins VP2-VP3 of picornaviruses. The structural similarities among these diverse groups of viruses, whose hosts include bacteria, unicellular eukaryotes, plants, and mammals, make it probable that their capsid proteins have evolved from a common ancestor that had already acquired a pseudo-sixfold organization. The trimeric capsid protein structure was used to produce a quasi-atomic model of the 1,900-Å diameter PBCV-1 outer shell, based on fitting of the Vp54 crystal structure into a three-dimensional cryoelectron microscopy image reconstruction of the virus.

Rubella virus capsid protein structure and its role in virus assembly and infection

“…Of particular relevance to RV is the nucleocapsid of Sindbis virus (9) and Ross River virus (11), alphaviruses whose nucleocapsid surface is positively charged and surrounded by lipid membranes. A second example is the double-stranded DNA containing Paramecium bursaria Chlorella virus-1 whose capsid protein hugs the exterior of the internal lipid membrane (19). A third example is the matrix protein of the pleomorphic Newcastle disease virus, which is closely associated with the interior of the viral lipid envelope (20).…”

Subcellular localization of bacteriophage PRD1 proteins in Escherichia coli

“…The PRD1 virion is formed by an icosahedral protein capsid surrounding a protein-rich membrane which, in turn, encloses the linear dsDNA genome and Olsen et al, 1974. Based on X-ray crystallographic analyses, PRD1 belongs to a certain structure based viral lineage with several other viruses such as: adenovirus, Paramecium bursaria chlorella virus 1 (PBCV-1) and Sulfolobus turreted icosahedral virus (STIV) ( Abrescia et al, 2012, Benson et al, 1999, Khayat et al, 2005and Nandhagopal et al, 2002. All these viruses have a major capsid protein with a double -barrel fold and similar virion architecture.…”

An icosahedral algal virus has a complex unique vertex decorated by a spike

“…PBCV-1 has a multilayer structure, with an outer glycoprotein capsid that surrounds a lipid bilayer membrane and a dsDNA genome (4,6). The 331-kbp PBCV-1 genome codes for 11 tRNAs and Ϸ365 putative proteins (7), of which more than 100 are present in the mature virion.…”

“…The crystal structure of Vp54 showed that the subunit consists of two 8-stranded, antiparallel ␤-barrel, ''jelly-roll'' domains. The monomeric Vp54 forms a trimeric capsomer (a ''major capsomer''), which has pseudo-6-fold symmetry, relating the jelly-roll structures (6).…”

“…The triangulation number (9) (T) is 169d (h ϭ 7, k ϭ 8), where T represents the number of jelly rolls in the icosahedral asymmetric unit. The crystal structure of PBCV-1 Vp54 had been fitted into the 26-Å-resolution cryoEM density map (6,10) to generate a pseudoatomic structure of the capsid. However, the 5 jelly rolls surrounding each pentameric vertex form a special capsomer in which, presumably, the monomers contain only 1 jelly roll.…”