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Title: Structure of faustovirus, a large dsDNA virus

Abstract

Many viruses protect their genome with a combination of a protein shell with or without a membrane layer. In this paper, we describe the structure of faustovirus, the first DNA virus (to our knowledge) that has been found to use two protein shells to encapsidate and protect its genome. The crystal structure of the major capsid protein, in combination with cryo-electron microscopy structures of two different maturation stages of the virus, shows that the outer virus shell is composed of a double jelly-roll protein that can be found in many double-stranded DNA viruses. The structure of the repeating hexameric unit of the inner shell is different from all other known capsid proteins. In addition to the unique architecture, the region of the genome that encodes the major capsid protein stretches over 17,000 bp and contains a large number of introns and exons. Finally, this complexity might help the virus to rapidly adapt to new environments or hosts.

Authors:
 [1];  [2];  [2];  [3];  [2];  [2];  [1]
  1. Purdue Univ., West Lafayette, IN (United States). Dept. of Biological Sciences
  2. Aix-Marseille Univ., Marseille (France). Research Inst. for Development. Dept. of Research on Emerging Infectious and Tropical Diseases (URMITE)
  3. Purdue Univ., West Lafayette, IN (United States). Dept. of Chemistry
Publication Date:
Research Org.:
Purdue Univ., West Lafayette, IN (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES); National Inst. of Health (NIH) (United States)
Contributing Org.:
Aix-Marseille Univ., Marseille (France)
OSTI Identifier:
1258668
Grant/Contract Number:  
AC02-06CH11357; AI011219
Resource Type:
Accepted Manuscript
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 113; Journal Issue: 22; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)
Country of Publication:
United States
Language:
ENGLISH
Subject:
60 APPLIED LIFE SCIENCES; 59 BASIC BIOLOGICAL SCIENCES; faustovirus; structure; double-protein shell; major capsid protein

Citation Formats

Klose, Thomas, Reteno, Dorine G., Benamar, Samia, Hollerbach, Adam, Colson, Philippe, La Scola, Bernard, and Rossmann, Michael G. Structure of faustovirus, a large dsDNA virus. United States: N. p., 2016. Web. doi:10.1073/pnas.1523999113.
Klose, Thomas, Reteno, Dorine G., Benamar, Samia, Hollerbach, Adam, Colson, Philippe, La Scola, Bernard, & Rossmann, Michael G. Structure of faustovirus, a large dsDNA virus. United States. https://doi.org/10.1073/pnas.1523999113
Klose, Thomas, Reteno, Dorine G., Benamar, Samia, Hollerbach, Adam, Colson, Philippe, La Scola, Bernard, and Rossmann, Michael G. Mon . "Structure of faustovirus, a large dsDNA virus". United States. https://doi.org/10.1073/pnas.1523999113. https://www.osti.gov/servlets/purl/1258668.
@article{osti_1258668,
title = {Structure of faustovirus, a large dsDNA virus},
author = {Klose, Thomas and Reteno, Dorine G. and Benamar, Samia and Hollerbach, Adam and Colson, Philippe and La Scola, Bernard and Rossmann, Michael G.},
abstractNote = {Many viruses protect their genome with a combination of a protein shell with or without a membrane layer. In this paper, we describe the structure of faustovirus, the first DNA virus (to our knowledge) that has been found to use two protein shells to encapsidate and protect its genome. The crystal structure of the major capsid protein, in combination with cryo-electron microscopy structures of two different maturation stages of the virus, shows that the outer virus shell is composed of a double jelly-roll protein that can be found in many double-stranded DNA viruses. The structure of the repeating hexameric unit of the inner shell is different from all other known capsid proteins. In addition to the unique architecture, the region of the genome that encodes the major capsid protein stretches over 17,000 bp and contains a large number of introns and exons. Finally, this complexity might help the virus to rapidly adapt to new environments or hosts.},
doi = {10.1073/pnas.1523999113},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 22,
volume = 113,
place = {United States},
year = {Mon May 16 00:00:00 EDT 2016},
month = {Mon May 16 00:00:00 EDT 2016}
}

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Cited by: 59 works
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Works referenced in this record:

LMSD: LIPID MAPS structure database
journal, January 2007

  • Sud, M.; Fahy, E.; Cotter, D.
  • Nucleic Acids Research, Vol. 35, Issue Database
  • DOI: 10.1093/nar/gkl838

Electrostatics of nanosystems: Application to microtubules and the ribosome
journal, August 2001

  • Baker, N. A.; Sept, D.; Joseph, S.
  • Proceedings of the National Academy of Sciences, Vol. 98, Issue 18, p. 10037-10041
  • DOI: 10.1073/pnas.181342398

Physical Principles in the Construction of Regular Viruses
journal, January 1962


PHENIX: a comprehensive Python-based system for macromolecular structure solution.
text, January 2010

  • Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor
  • Apollo - University of Cambridge Repository
  • DOI: 10.17863/cam.45787

Viruses and viruslike particles of eukaryotic algae.
journal, January 1991


Dali server: conservation mapping in 3D
journal, May 2010

  • Holm, Liisa; Rosenstr�m, P�ivi
  • Nucleic Acids Research, Vol. 38, Issue suppl_2
  • DOI: 10.1093/nar/gkq366

Herpesvirus assembly: An update
journal, August 2009


Electrospray ionization/tandem quadrupole mass spectrometric studies on phosphatidylcholines: The fragmentation processes
journal, April 2003


Automated molecular microscopy: The new Leginon system
journal, July 2005

  • Suloway, Christian; Pulokas, James; Fellmann, Denis
  • Journal of Structural Biology, Vol. 151, Issue 1
  • DOI: 10.1016/j.jsb.2005.03.010

Towards automated crystallographic structure refinement with phenix.refine
journal, March 2012

  • Afonine, Pavel V.; Grosse-Kunstleve, Ralf W.; Echols, Nathaniel
  • Acta Crystallographica Section D Biological Crystallography, Vol. 68, Issue 4
  • DOI: 10.1107/S0907444912001308

On-Demand Ambient Ionization of Picoliter Samples Using Charge Pulses
journal, April 2015

  • Li, Anyin; Hollerbach, Adam; Luo, Qingjie
  • Angewandte Chemie International Edition, Vol. 54, Issue 23
  • DOI: 10.1002/anie.201501895

Insights into assembly from structural analysis of bacteriophage PRD1
journal, November 2004

  • Abrescia, Nicola G. A.; Cockburn, Joseph J. B.; Grimes, Jonathan M.
  • Nature, Vol. 432, Issue 7013
  • DOI: 10.1038/nature03056

A Giant Virus in Amoebae
journal, March 2003


Analysis of the Complete Nucleotide Sequence of African Swine Fever Virus
journal, April 1995

  • Yáñez, Rafael J.; Rodrı́guez, Javier M.; Nogal, Maria L.
  • Virology, Vol. 208, Issue 1
  • DOI: 10.1006/viro.1995.1149

The Marine Algal Virus PpV01 Has an Icosahedral Capsid with T=219 Quasisymmetry
journal, June 2005


The Capsid Proteins of a Large, Icosahedral dsDNA Virus
journal, January 2009


Three-dimensional structure and function of the Paramecium bursaria chlorella virus capsid
journal, August 2011

  • Zhang, X.; Xiang, Y.; Dunigan, D. D.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 36
  • DOI: 10.1073/pnas.1107847108

XDS
journal, January 2010

  • Kabsch, Wolfgang
  • Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2
  • DOI: 10.1107/S0907444909047337

A PRD1 by Another Name?
journal, December 2005


UCSF Chimera?A visualization system for exploratory research and analysis
journal, January 2004

  • Pettersen, Eric F.; Goddard, Thomas D.; Huang, Conrad C.
  • Journal of Computational Chemistry, Vol. 25, Issue 13
  • DOI: 10.1002/jcc.20084

Computational studies of polyurethanases from Pseudomonas
journal, January 2021

  • do Canto, Vanessa Petry; Thompson, Claudia Elizabeth; Netz, Paulo Augusto
  • Journal of Molecular Modeling, Vol. 27, Issue 2
  • DOI: 10.1007/s00894-021-04671-x

African swine fever virus morphogenesis
journal, April 2013


An Electron Microscope Study of the Structure of Sericesthis Iridescent Virus
journal, July 1969


Maturation in Action: CryoEM Study of a Viral Capsid Caught during Expansion
journal, August 2012


Structures and organization of adenovirus cement proteins provide insights into the role of capsid maturation in virus entry and infection
journal, July 2014

  • Reddy, V. S.; Nemerow, G. R.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 32
  • DOI: 10.1073/pnas.1408462111

Membrane Remodeling by the Double-Barrel Scaffolding Protein of Poxvirus
journal, September 2011


Combined EM/X-Ray Imaging Yields a Quasi-Atomic Model of the Adenovirus-Related Bacteriophage PRD1 and Shows Key Capsid and Membrane Interactions
journal, October 2001


EMAN2: An extensible image processing suite for electron microscopy
journal, January 2007

  • Tang, Guang; Peng, Liwei; Baldwin, Philip R.
  • Journal of Structural Biology, Vol. 157, Issue 1
  • DOI: 10.1016/j.jsb.2006.05.009

A tale of two symmetrons: Rules for construction of icosahedral capsids from trisymmetrons and pentasymmetrons
journal, April 2010


Cavin1 intrinsically disordered domains are essential for fuzzy electrostatic interactions and caveola formation
journal, February 2021


The structure and evolution of the major capsid protein of a large, lipid-containing DNA virus
journal, October 2002

  • Nandhagopal, N.; Simpson, A. A.; Gurnon, J. R.
  • Proceedings of the National Academy of Sciences, Vol. 99, Issue 23
  • DOI: 10.1073/pnas.232580699

Minor proteins, mobile arms and membrane–capsid interactions in the bacteriophage PRD1 capsid
journal, September 2002

  • San Martín, Carmen; Huiskonen, Juha T.; Bamford, Jaana K. H.
  • Nature Structural Biology, Vol. 9, Issue 10
  • DOI: 10.1038/nsb837

Structure of the Bacteriophage ϕ6 Nucleocapsid Suggests a Mechanism for Sequential RNA Packaging
journal, June 2006


Preclinical Development of a Fusion Peptide Conjugate as an HIV Vaccine Immunogen
journal, February 2020


PHENIX: a comprehensive Python-based system for macromolecular structure solution
journal, January 2010

  • Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor
  • Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221
  • DOI: 10.1107/S0907444909052925

Revised Mimivirus major capsid protein sequence reveals intron-containing gene structure and extra domain
journal, January 2009

  • Azza, Saïd; Cambillau, Christian; Raoult, Didier
  • BMC Molecular Biology, Vol. 10, Issue 1
  • DOI: 10.1186/1471-2199-10-39

Structure of Sputnik, a virophage, at 3.5-A resolution
journal, October 2012

  • Zhang, X.; Sun, S.; Xiang, Y.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 45
  • DOI: 10.1073/pnas.1211702109

Chlorovirus ATCV-1 is part of the human oropharyngeal virome and is associated with changes in cognitive functions in humans and mice
journal, October 2014

  • Yolken, Robert H.; Jones-Brando, Lorraine; Dunigan, David D.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 45
  • DOI: 10.1073/pnas.1418895111

Faustovirus, an Asfarvirus-Related New Lineage of Giant Viruses Infecting Amoebae
journal, April 2015

  • Reteno, Dorine Gaëlle; Benamar, Samia; Khalil, Jacques Bou
  • Journal of Virology, Vol. 89, Issue 13
  • DOI: 10.1128/JVI.00115-15

Infections with mimivirus in patients with chronic obstructive pulmonary disease
journal, December 2012


Near-atomic resolution using electron cryomicroscopy and single-particle reconstruction
journal, January 2008

  • Zhang, X.; Settembre, E.; Xu, C.
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue 6
  • DOI: 10.1073/pnas.0711623105

Insights into the Evolution of a Complex Virus from the Crystal Structure of Vaccinia Virus D13
journal, July 2011


Mimivirus in Pneumonia Patients
journal, March 2005

  • La Scola, Bernard; Marrie, Thomas J.; Auffray, Jean-Pierre
  • Emerging Infectious Diseases, Vol. 11, Issue 3
  • DOI: 10.3201/eid1103.040538

Atomic structure reveals the unique capsid organization of a dsRNA virus
journal, February 2009

  • Pan, J.; Dong, L.; Lin, L.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 11
  • DOI: 10.1073/pnas.0812071106

Phaser crystallographic software
journal, July 2007

  • McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D.
  • Journal of Applied Crystallography, Vol. 40, Issue 4
  • DOI: 10.1107/S0021889807021206

Works referencing / citing this record:

Boiling Acid Mimics Intracellular Giant Virus Genome Release
posted_content, September 2019

  • Schrad, Jason R.; Abrahão, Jônatas S.; Cortines, Juliana R.
  • bioRxiv
  • DOI: 10.1101/777854

Discovery and Further Studies on Giant Viruses at the IHU Mediterranee Infection That Modified the Perception of the Virosphere
journal, March 2019

  • Rolland, Clara; Andreani, Julien; Louazani, Amina
  • Viruses, Vol. 11, Issue 4
  • DOI: 10.3390/v11040312

Near-atomic structure of a giant virus
journal, January 2019


The cryo-EM structure of African swine fever virus unravels a unique architecture comprising two icosahedral protein capsids and two lipoprotein membranes
journal, October 2019

  • Andrés, German; Charro, Diego; Matamoros, Tania
  • Journal of Biological Chemistry, Vol. 295, Issue 1
  • DOI: 10.1074/jbc.ac119.011196

The so far farthest reaches of the double jelly roll capsid protein fold
journal, November 2018


All-atom normal mode dynamics of HIV-1 capsid
journal, September 2018


Diversification of giant and large eukaryotic dsDNA viruses predated the origin of modern eukaryotes
posted_content, October 2018

  • Guglielmini, Julien; Woo, Anthony; Krupovic, Mart
  • bioRxiv
  • DOI: 10.1101/455816

Structure of the African swine fever virus major capsid protein p72
journal, September 2019


Concurrence of Iridovirus, Polyomavirus, and a Unique Member of a New Group of Fish Papillomaviruses in Lymphocystis Disease-Affected Gilthead Sea Bream
journal, July 2016

  • López-Bueno, Alberto; Mavian, Carla; Labella, Alejandro M.
  • Journal of Virology, Vol. 90, Issue 19
  • DOI: 10.1128/jvi.01369-16

Putative Promoter Motif Analyses Reinforce the Evolutionary Relationships Among Faustoviruses, Kaumoebavirus, and Asfarvirus
journal, May 2018

  • Oliveira, Graziele P.; de Aquino, Isabella L. M.; Luiz, Ana P. M. F.
  • Frontiers in Microbiology, Vol. 9
  • DOI: 10.3389/fmicb.2018.01041

Medusavirus, a Novel Large DNA Virus Discovered from Hot Spring Water
journal, February 2019

  • Yoshikawa, Genki; Blanc-Mathieu, Romain; Song, Chihong
  • Journal of Virology, Vol. 93, Issue 8
  • DOI: 10.1128/jvi.02130-18

Faustovirus E12 Transcriptome Analysis Reveals Complex Splicing in Capsid Gene
journal, October 2018

  • Cherif Louazani, Amina; Baptiste, Emeline; Levasseur, Anthony
  • Frontiers in Microbiology, Vol. 9
  • DOI: 10.3389/fmicb.2018.02534

Kaumoebavirus, a New Virus That Clusters with Faustoviruses and Asfarviridae
journal, October 2016

  • Bajrai, Leena; Benamar, Samia; Azhar, Esam
  • Viruses, Vol. 8, Issue 11
  • DOI: 10.3390/v8110278

The Roles of Electrostatic Interactions in Capsid Assembly Mechanisms of Giant Viruses
journal, April 2019

  • Xian, Yuejiao; Karki, Chitra B.; Silva, Sebastian Miki
  • International Journal of Molecular Sciences, Vol. 20, Issue 8
  • DOI: 10.3390/ijms20081876

Mimivirus: leading the way in the discovery of giant viruses of amoebae
journal, February 2017

  • Colson, Philippe; La Scola, Bernard; Levasseur, Anthony
  • Nature Reviews Microbiology, Vol. 15, Issue 4
  • DOI: 10.1038/nrmicro.2016.197

Diversification of giant and large eukaryotic dsDNA viruses predated the origin of modern eukaryotes
journal, September 2019

  • Guglielmini, Julien; Woo, Anthony C.; Krupovic, Mart
  • Proceedings of the National Academy of Sciences, Vol. 116, Issue 39
  • DOI: 10.1073/pnas.1912006116

Protozoal giant viruses: agents potentially infectious to humans and animals
journal, July 2019

  • Tokarz-Deptuła, Beata; Niedźwiedzka-Rystwej, Paulina; Czupryńska, Paulina
  • Virus Genes, Vol. 55, Issue 5
  • DOI: 10.1007/s11262-019-01684-w

Architecture of African swine fever virus and implications for viral assembly
journal, October 2019


Protozoal giant viruses: agents potentially infectious to humans and animals
journal, July 2019

  • Tokarz-Deptuła, Beata; Niedźwiedzka-Rystwej, Paulina; Czupryńska, Paulina
  • Virus Genes, Vol. 55, Issue 5
  • DOI: 10.1007/s11262-019-01684-w

Cryo-EM structure of a Marseilleviridae virus particle reveals a large internal microassembly
journal, March 2018


Mimivirus: leading the way in the discovery of giant viruses of amoebae
journal, February 2017

  • Colson, Philippe; La Scola, Bernard; Levasseur, Anthony
  • Nature Reviews Microbiology, Vol. 15, Issue 4
  • DOI: 10.1038/nrmicro.2016.197

Structure of the African swine fever virus major capsid protein p72
journal, September 2019


Near-atomic structure of a giant virus
journal, January 2019


Cryo-EM reconstruction of the Cafeteria roenbergensis virus capsid suggests novel assembly pathway for giant viruses
journal, July 2017


A novel Asfarvirus-like virus identified as a potential cause of mass mortality of abalone
journal, March 2020


Medusavirus, a Novel Large DNA Virus Discovered from Hot Spring Water
journal, February 2019

  • Yoshikawa, Genki; Blanc-Mathieu, Romain; Song, Chihong
  • Journal of Virology, Vol. 93, Issue 8
  • DOI: 10.1128/jvi.02130-18

The so far farthest reaches of the double jelly roll capsid protein fold
journal, November 2018


All-atom normal mode dynamics of HIV-1 capsid
journal, September 2018


Putative Promoter Motif Analyses Reinforce the Evolutionary Relationships Among Faustoviruses, Kaumoebavirus, and Asfarvirus
journal, May 2018

  • Oliveira, Graziele P.; de Aquino, Isabella L. M.; Luiz, Ana P. M. F.
  • Frontiers in Microbiology, Vol. 9
  • DOI: 10.3389/fmicb.2018.01041

The Roles of Electrostatic Interactions in Capsid Assembly Mechanisms of Giant Viruses
journal, April 2019

  • Xian, Yuejiao; Karki, Chitra B.; Silva, Sebastian Miki
  • International Journal of Molecular Sciences, Vol. 20, Issue 8
  • DOI: 10.3390/ijms20081876

Discovery and Further Studies on Giant Viruses at the IHU Mediterranee Infection That Modified the Perception of the Virosphere
journal, March 2019

  • Rolland, Clara; Andreani, Julien; Louazani, Amina
  • Viruses, Vol. 11, Issue 4
  • DOI: 10.3390/v11040312

Comparative Genomics Unveils Regionalized Evolution of the Faustovirus Genomes
journal, May 2020

  • Geballa-Koukoulas, Khalil; Boudjemaa, Hadjer; Andreani, Julien
  • Viruses, Vol. 12, Issue 5
  • DOI: 10.3390/v12050577

Kaumoebavirus, a New Virus That Clusters with Faustoviruses and Asfarviridae
journal, October 2016

  • Bajrai, Leena; Benamar, Samia; Azhar, Esam
  • Viruses, Vol. 8, Issue 11
  • DOI: 10.3390/v8110278

Microscopic Characterization of the Brazilian Giant Samba Virus
journal, February 2017

  • Schrad, Jason; Young, Eric; Abrahão, Jônatas
  • Viruses, Vol. 9, Issue 2
  • DOI: 10.3390/v9020030