Three-dimensional structure of the enveloped bacteriophage Φ12: An incomplete T = 13 lattice is superposed on an enclosed T = 1 shell

Hui Wei, R. Holland Cheng, John Berriman, William J. Rice, David L. Stokes, A. Katz, David Gene Morgan, Paul Gottlieb

Research output: Contribution to journalArticle

18 Citations (Scopus)

Abstract

Background: Bacteriophage φ12 is a member of the Cystoviridae, a unique group of lipid containing membrane enveloped bacteriophages that infect the bacterial plant pathogen Pseudomonas syringae pv. phaseolicola. The genomes of the virus species contain three double-stranded (dsRNA) segments, and the virus capsid itself is organized in multiple protein shells. The segmented dsRNA genome, the multi-layered arrangement of the capsid and the overall viral replication scheme make the Cystoviridae similar to the Reoviridae. Methodology/Principal Findings: We present structural studies of cystovirus φ12 obtained using cryo-electron microscopy and image processing techniques. We have collected images of isolated φ12 virions and generated reconstructions of both the entire particles and the polymerase complex (PC). We find that in the nucleocapsid (NC), the φ12 P8 protein is organized on an incomplete T = 13 icosahedral lattice where the symmetry axes of the T = 13 layer and the enclosed T = 1 layer of the PC superpose. This is the same general protein-component organization found in φ6 NC's but the detailed structure of the entire φ12 P8 layer is distinct from that found in the best classified cystovirus species φ6. In the reconstruction of the NC, the P8 layer includes protein density surrounding the hexamers of P4 that sit at the 5-fold vertices of the icosahedral lattice. We believe these novel features correspond to dimers of protein P7. Conclusions/Significance: In conclusion, we have determined that the φ12 NC surface is composed of an incomplete T = 13 P8 layer forming a net-like configuration. The significance of this finding in regard to cystovirus assembly is that vacancies in the lattice could have the potential to accommodate additional viral proteins that are required for RNA packaging and synthesis.

Original languageEnglish (US)
Article numbere6850
JournalPLoS One
Volume4
Issue number9
DOIs
StatePublished - Sep 3 2009

Fingerprint

Cystoviridae
Bacteriophages
Cystovirus
bacteriophages
Nucleocapsid
nucleocapsid
capsid
Capsid
double-stranded RNA
Proteins
Viruses
proteins
Genes
Reoviridae
Pseudomonas syringae pv. phaseolicola
Genome
Pseudomonas syringae
Cryoelectron Microscopy
viruses
genome

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Medicine(all)

Cite this

Three-dimensional structure of the enveloped bacteriophage Φ12 : An incomplete T = 13 lattice is superposed on an enclosed T = 1 shell. / Wei, Hui; Cheng, R. Holland; Berriman, John; Rice, William J.; Stokes, David L.; Katz, A.; Morgan, David Gene; Gottlieb, Paul.

In: PLoS One, Vol. 4, No. 9, e6850, 03.09.2009.

Research output: Contribution to journalArticle

Wei, Hui ; Cheng, R. Holland ; Berriman, John ; Rice, William J. ; Stokes, David L. ; Katz, A. ; Morgan, David Gene ; Gottlieb, Paul. / Three-dimensional structure of the enveloped bacteriophage Φ12 : An incomplete T = 13 lattice is superposed on an enclosed T = 1 shell. In: PLoS One. 2009 ; Vol. 4, No. 9.
@article{9888ae9536994650b6f8399e5493aea6,
title = "Three-dimensional structure of the enveloped bacteriophage Φ12: An incomplete T = 13 lattice is superposed on an enclosed T = 1 shell",
abstract = "Background: Bacteriophage φ12 is a member of the Cystoviridae, a unique group of lipid containing membrane enveloped bacteriophages that infect the bacterial plant pathogen Pseudomonas syringae pv. phaseolicola. The genomes of the virus species contain three double-stranded (dsRNA) segments, and the virus capsid itself is organized in multiple protein shells. The segmented dsRNA genome, the multi-layered arrangement of the capsid and the overall viral replication scheme make the Cystoviridae similar to the Reoviridae. Methodology/Principal Findings: We present structural studies of cystovirus φ12 obtained using cryo-electron microscopy and image processing techniques. We have collected images of isolated φ12 virions and generated reconstructions of both the entire particles and the polymerase complex (PC). We find that in the nucleocapsid (NC), the φ12 P8 protein is organized on an incomplete T = 13 icosahedral lattice where the symmetry axes of the T = 13 layer and the enclosed T = 1 layer of the PC superpose. This is the same general protein-component organization found in φ6 NC's but the detailed structure of the entire φ12 P8 layer is distinct from that found in the best classified cystovirus species φ6. In the reconstruction of the NC, the P8 layer includes protein density surrounding the hexamers of P4 that sit at the 5-fold vertices of the icosahedral lattice. We believe these novel features correspond to dimers of protein P7. Conclusions/Significance: In conclusion, we have determined that the φ12 NC surface is composed of an incomplete T = 13 P8 layer forming a net-like configuration. The significance of this finding in regard to cystovirus assembly is that vacancies in the lattice could have the potential to accommodate additional viral proteins that are required for RNA packaging and synthesis.",
author = "Hui Wei and Cheng, {R. Holland} and John Berriman and Rice, {William J.} and Stokes, {David L.} and A. Katz and Morgan, {David Gene} and Paul Gottlieb",
year = "2009",
month = "9",
day = "3",
doi = "10.1371/journal.pone.0006850",
language = "English (US)",
volume = "4",
journal = "PLoS One",
issn = "1932-6203",
publisher = "Public Library of Science",
number = "9",

}

TY - JOUR

T1 - Three-dimensional structure of the enveloped bacteriophage Φ12

T2 - An incomplete T = 13 lattice is superposed on an enclosed T = 1 shell

AU - Wei, Hui

AU - Cheng, R. Holland

AU - Berriman, John

AU - Rice, William J.

AU - Stokes, David L.

AU - Katz, A.

AU - Morgan, David Gene

AU - Gottlieb, Paul

PY - 2009/9/3

Y1 - 2009/9/3

N2 - Background: Bacteriophage φ12 is a member of the Cystoviridae, a unique group of lipid containing membrane enveloped bacteriophages that infect the bacterial plant pathogen Pseudomonas syringae pv. phaseolicola. The genomes of the virus species contain three double-stranded (dsRNA) segments, and the virus capsid itself is organized in multiple protein shells. The segmented dsRNA genome, the multi-layered arrangement of the capsid and the overall viral replication scheme make the Cystoviridae similar to the Reoviridae. Methodology/Principal Findings: We present structural studies of cystovirus φ12 obtained using cryo-electron microscopy and image processing techniques. We have collected images of isolated φ12 virions and generated reconstructions of both the entire particles and the polymerase complex (PC). We find that in the nucleocapsid (NC), the φ12 P8 protein is organized on an incomplete T = 13 icosahedral lattice where the symmetry axes of the T = 13 layer and the enclosed T = 1 layer of the PC superpose. This is the same general protein-component organization found in φ6 NC's but the detailed structure of the entire φ12 P8 layer is distinct from that found in the best classified cystovirus species φ6. In the reconstruction of the NC, the P8 layer includes protein density surrounding the hexamers of P4 that sit at the 5-fold vertices of the icosahedral lattice. We believe these novel features correspond to dimers of protein P7. Conclusions/Significance: In conclusion, we have determined that the φ12 NC surface is composed of an incomplete T = 13 P8 layer forming a net-like configuration. The significance of this finding in regard to cystovirus assembly is that vacancies in the lattice could have the potential to accommodate additional viral proteins that are required for RNA packaging and synthesis.

AB - Background: Bacteriophage φ12 is a member of the Cystoviridae, a unique group of lipid containing membrane enveloped bacteriophages that infect the bacterial plant pathogen Pseudomonas syringae pv. phaseolicola. The genomes of the virus species contain three double-stranded (dsRNA) segments, and the virus capsid itself is organized in multiple protein shells. The segmented dsRNA genome, the multi-layered arrangement of the capsid and the overall viral replication scheme make the Cystoviridae similar to the Reoviridae. Methodology/Principal Findings: We present structural studies of cystovirus φ12 obtained using cryo-electron microscopy and image processing techniques. We have collected images of isolated φ12 virions and generated reconstructions of both the entire particles and the polymerase complex (PC). We find that in the nucleocapsid (NC), the φ12 P8 protein is organized on an incomplete T = 13 icosahedral lattice where the symmetry axes of the T = 13 layer and the enclosed T = 1 layer of the PC superpose. This is the same general protein-component organization found in φ6 NC's but the detailed structure of the entire φ12 P8 layer is distinct from that found in the best classified cystovirus species φ6. In the reconstruction of the NC, the P8 layer includes protein density surrounding the hexamers of P4 that sit at the 5-fold vertices of the icosahedral lattice. We believe these novel features correspond to dimers of protein P7. Conclusions/Significance: In conclusion, we have determined that the φ12 NC surface is composed of an incomplete T = 13 P8 layer forming a net-like configuration. The significance of this finding in regard to cystovirus assembly is that vacancies in the lattice could have the potential to accommodate additional viral proteins that are required for RNA packaging and synthesis.

UR - http://www.scopus.com/inward/record.url?scp=70149112989&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=70149112989&partnerID=8YFLogxK

U2 - 10.1371/journal.pone.0006850

DO - 10.1371/journal.pone.0006850

M3 - Article

C2 - 19727406

AN - SCOPUS:70149112989

VL - 4

JO - PLoS One

JF - PLoS One

SN - 1932-6203

IS - 9

M1 - e6850

ER -