Structure of faustovirus, a large dsDNA virus

Klose, Thomas; Reteno, Dorine G.; Benamar, Samia; Hollerbach, Adam; Colson, Philippe; La Scola, Bernard; Rossmann, Michael G.

doi:10.1073/pnas.1523999113

Title: Structure of faustovirus, a large dsDNA virus

Journal Article · Mon May 16 00:00:00 EDT 2016 · Proceedings of the National Academy of Sciences of the United States of America

DOI:https://doi.org/10.1073/pnas.1523999113· OSTI ID:1258668

Klose, Thomas ^[1]; Reteno, Dorine G. ^[2]; Benamar, Samia ^[2]; Hollerbach, Adam ^[3]; Colson, Philippe ^[2]; La Scola, Bernard ^[2]; Rossmann, Michael G. ^[1]

Purdue Univ., West Lafayette, IN (United States). Dept. of Biological Sciences
Aix-Marseille Univ., Marseille (France). Research Inst. for Development. Dept. of Research on Emerging Infectious and Tropical Diseases (URMITE)
Purdue Univ., West Lafayette, IN (United States). Dept. of Chemistry

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.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Purdue Univ., West Lafayette, IN (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES); National Inst. of Health (NIH) (United States)

Contributing Organization:: Aix-Marseille Univ., Marseille (France)

Grant/Contract Number:: AC02-06CH11357; AI011219

OSTI ID:: 1258668

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Vol. 113, Issue 22; ISSN 0027-8424

Publisher:: National Academy of Sciences, Washington, DC (United States)Copyright Statement

Country of Publication:: United States

Language:: ENGLISH

Citation Metrics:

Cited by: 59 works

Citation information provided by
Web of Science

References (46)

LMSD: LIPID MAPS structure database Sud, M.; Fahy, E.; Cotter, D. Nucleic Acids Research, Vol. 35, Issue Database https://doi.org/10.1093/nar/gkl838	journal	January 2007
Electrostatics of nanosystems: Application to microtubules and the ribosome Baker, N. A.; Sept, D.; Joseph, S. Proceedings of the National Academy of Sciences, Vol. 98, Issue 18, p. 10037-10041 https://doi.org/10.1073/pnas.181342398	journal	August 2001
Physical Principles in the Construction of Regular Viruses Caspar, D. L. D.; Klug, A. Cold Spring Harbor Symposia on Quantitative Biology, Vol. 27, Issue 0 https://doi.org/10.1101/SQB.1962.027.001.005	journal	January 1962
PHENIX: a comprehensive Python-based system for macromolecular structure solution. Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.45787	text	January 2010
Viruses and viruslike particles of eukaryotic algae. Van Etten, J. L.; Lane, L. C.; Meints, R. H. Microbiological Reviews, Vol. 55, Issue 4 https://doi.org/10.1128/MMBR.55.4.586-620.1991	journal	January 1991
Dali server: conservation mapping in 3D Holm, Liisa; Rosenstrï¿½m, Pï¿½ivi Nucleic Acids Research, Vol. 38, Issue suppl_2 https://doi.org/10.1093/nar/gkq366	journal	May 2010
Herpesvirus assembly: An update Mettenleiter, Thomas C.; Klupp, Barbara G.; Granzow, Harald Virus Research, Vol. 143, Issue 2 https://doi.org/10.1016/j.virusres.2009.03.018	journal	August 2009
Electrospray ionization/tandem quadrupole mass spectrometric studies on phosphatidylcholines: The fragmentation processes Hsu, Fong-Fu; Turk, John Journal of the American Society for Mass Spectrometry, Vol. 14, Issue 4 https://doi.org/10.1016/S1044-0305(03)00064-3	journal	April 2003
Automated molecular microscopy: The new Leginon system Suloway, Christian; Pulokas, James; Fellmann, Denis Journal of Structural Biology, Vol. 151, Issue 1 https://doi.org/10.1016/j.jsb.2005.03.010	journal	July 2005
Towards automated crystallographic structure refinement with phenix.refine Afonine, Pavel V.; Grosse-Kunstleve, Ralf W.; Echols, Nathaniel Acta Crystallographica Section D Biological Crystallography, Vol. 68, Issue 4 https://doi.org/10.1107/S0907444912001308	journal	March 2012
On-Demand Ambient Ionization of Picoliter Samples Using Charge Pulses Li, Anyin; Hollerbach, Adam; Luo, Qingjie Angewandte Chemie International Edition, Vol. 54, Issue 23 https://doi.org/10.1002/anie.201501895	journal	April 2015
Insights into assembly from structural analysis of bacteriophage PRD1 Abrescia, Nicola G. A.; Cockburn, Joseph J. B.; Grimes, Jonathan M. Nature, Vol. 432, Issue 7013 https://doi.org/10.1038/nature03056	journal	November 2004
A Giant Virus in Amoebae Scola, B. L. Science, Vol. 299, Issue 5615 https://doi.org/10.1126/science.1081867	journal	March 2003
Analysis of the Complete Nucleotide Sequence of African Swine Fever Virus Yáñez, Rafael J.; Rodrı́guez, Javier M.; Nogal, Maria L. Virology, Vol. 208, Issue 1 https://doi.org/10.1006/viro.1995.1149	journal	April 1995
The Marine Algal Virus PpV01 Has an Icosahedral Capsid with T=219 Quasisymmetry Yan, X.; Chipman, P. R.; Castberg, T. Journal of Virology, Vol. 79, Issue 14 https://doi.org/10.1128/JVI.79.14.9236-9243.2005	journal	June 2005
The Capsid Proteins of a Large, Icosahedral dsDNA Virus Yan, Xiaodong; Yu, Zeyun; Zhang, Ping Journal of Molecular Biology, Vol. 385, Issue 4 https://doi.org/10.1016/j.jmb.2008.11.002	journal	January 2009
Three-dimensional structure and function of the Paramecium bursaria chlorella virus capsid Zhang, X.; Xiang, Y.; Dunigan, D. D. Proceedings of the National Academy of Sciences, Vol. 108, Issue 36 https://doi.org/10.1073/pnas.1107847108	journal	August 2011
XDS Kabsch, Wolfgang Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2 https://doi.org/10.1107/S0907444909047337	journal	January 2010
A PRD1 by Another Name? Fuller, Stephen Structure, Vol. 13, Issue 12 https://doi.org/10.1016/j.str.2005.11.004	journal	December 2005
UCSF Chimera?A visualization system for exploratory research and analysis Pettersen, Eric F.; Goddard, Thomas D.; Huang, Conrad C. Journal of Computational Chemistry, Vol. 25, Issue 13 https://doi.org/10.1002/jcc.20084	journal	January 2004
Computational studies of polyurethanases from Pseudomonas do Canto, Vanessa Petry; Thompson, Claudia Elizabeth; Netz, Paulo Augusto Journal of Molecular Modeling, Vol. 27, Issue 2 https://doi.org/10.1007/s00894-021-04671-x	journal	January 2021
African swine fever virus morphogenesis Salas, María L.; Andrés, Germán Virus Research, Vol. 173, Issue 1 https://doi.org/10.1016/j.virusres.2012.09.016	journal	April 2013
An Electron Microscope Study of the Structure of Sericesthis Iridescent Virus Wrigley, N. G. Journal of General Virology, Vol. 5, Issue 1 https://doi.org/10.1099/0022-1317-5-1-123	journal	July 1969
Maturation in Action: CryoEM Study of a Viral Capsid Caught during Expansion Veesler, David; Quispe, Joel; Grigorieff, Nikolaus Structure, Vol. 20, Issue 8 https://doi.org/10.1016/j.str.2012.05.011	journal	August 2012
Structures and organization of adenovirus cement proteins provide insights into the role of capsid maturation in virus entry and infection Reddy, V. S.; Nemerow, G. R. Proceedings of the National Academy of Sciences, Vol. 111, Issue 32 https://doi.org/10.1073/pnas.1408462111	journal	July 2014
Structural and Phylogenetic Analysis of Adenovirus Hexons by Use of High-Resolution X-Ray Crystallographic, Molecular Modeling, and Sequence-Based Methods Rux, J. J.; Kuser, P. R.; Burnett, R. M. Journal of Virology, Vol. 77, Issue 17 https://doi.org/10.1128/JVI.77.17.9553-9566.2003	journal	August 2003
Membrane Remodeling by the Double-Barrel Scaffolding Protein of Poxvirus Hyun, Jae-Kyung; Accurso, Cathy; Hijnen, Marcel PLoS Pathogens, Vol. 7, Issue 9 https://doi.org/10.1371/journal.ppat.1002239	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 Martı́n, Carmen San; Burnett, Roger M.; de Haas, Felix Structure, Vol. 9, Issue 10 https://doi.org/10.1016/S0969-2126(01)00642-6	journal	October 2001
EMAN2: An extensible image processing suite for electron microscopy Tang, Guang; Peng, Liwei; Baldwin, Philip R. Journal of Structural Biology, Vol. 157, Issue 1 https://doi.org/10.1016/j.jsb.2006.05.009	journal	January 2007
A tale of two symmetrons: Rules for construction of icosahedral capsids from trisymmetrons and pentasymmetrons Sinkovits, Robert S.; Baker, Timothy S. Journal of Structural Biology, Vol. 170, Issue 1 https://doi.org/10.1016/j.jsb.2009.12.003	journal	April 2010
Cavin1 intrinsically disordered domains are essential for fuzzy electrostatic interactions and caveola formation Tillu, Vikas A.; Rae, James; Gao, Ya Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-021-21035-4	journal	February 2021
The structure and evolution of the major capsid protein of a large, lipid-containing DNA virus Nandhagopal, N.; Simpson, A. A.; Gurnon, J. R. Proceedings of the National Academy of Sciences, Vol. 99, Issue 23 https://doi.org/10.1073/pnas.232580699	journal	October 2002
Minor proteins, mobile arms and membrane–capsid interactions in the bacteriophage PRD1 capsid San Martín, Carmen; Huiskonen, Juha T.; Bamford, Jaana K. H. Nature Structural Biology, Vol. 9, Issue 10 https://doi.org/10.1038/nsb837	journal	September 2002
Structure of the Bacteriophage ϕ6 Nucleocapsid Suggests a Mechanism for Sequential RNA Packaging Huiskonen, Juha T.; de Haas, Felix; Bubeck, Doryen Structure, Vol. 14, Issue 6 https://doi.org/10.1016/j.str.2006.03.018	journal	June 2006
Preclinical Development of a Fusion Peptide Conjugate as an HIV Vaccine Immunogen Ou, Li; Kong, Wing-Pui; Chuang, Gwo-Yu Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-59711-y	journal	February 2020
PHENIX: a comprehensive Python-based system for macromolecular structure solution Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221 https://doi.org/10.1107/S0907444909052925	journal	January 2010
Revised Mimivirus major capsid protein sequence reveals intron-containing gene structure and extra domain Azza, Saïd; Cambillau, Christian; Raoult, Didier BMC Molecular Biology, Vol. 10, Issue 1 https://doi.org/10.1186/1471-2199-10-39	journal	January 2009
Structure of Sputnik, a virophage, at 3.5-A resolution Zhang, X.; Sun, S.; Xiang, Y. Proceedings of the National Academy of Sciences, Vol. 109, Issue 45 https://doi.org/10.1073/pnas.1211702109	journal	October 2012
Chlorovirus ATCV-1 is part of the human oropharyngeal virome and is associated with changes in cognitive functions in humans and mice Yolken, Robert H.; Jones-Brando, Lorraine; Dunigan, David D. Proceedings of the National Academy of Sciences, Vol. 111, Issue 45 https://doi.org/10.1073/pnas.1418895111	journal	October 2014
Faustovirus, an Asfarvirus-Related New Lineage of Giant Viruses Infecting Amoebae Reteno, Dorine Gaëlle; Benamar, Samia; Khalil, Jacques Bou Journal of Virology, Vol. 89, Issue 13 https://doi.org/10.1128/JVI.00115-15	journal	April 2015
Infections with mimivirus in patients with chronic obstructive pulmonary disease Vanspauwen, M. J.; Franssen, F. M. E.; Raoult, D. Respiratory Medicine, Vol. 106, Issue 12 https://doi.org/10.1016/j.rmed.2012.08.019	journal	December 2012
Near-atomic resolution using electron cryomicroscopy and single-particle reconstruction Zhang, X.; Settembre, E.; Xu, C. Proceedings of the National Academy of Sciences, Vol. 105, Issue 6 https://doi.org/10.1073/pnas.0711623105	journal	January 2008
Insights into the Evolution of a Complex Virus from the Crystal Structure of Vaccinia Virus D13 Bahar, Mohammad W.; Graham, Stephen C.; Stuart, David I. Structure, Vol. 19, Issue 7 https://doi.org/10.1016/j.str.2011.03.023	journal	July 2011
Mimivirus in Pneumonia Patients La Scola, Bernard; Marrie, Thomas J.; Auffray, Jean-Pierre Emerging Infectious Diseases, Vol. 11, Issue 3 https://doi.org/10.3201/eid1103.040538	journal	March 2005
Atomic structure reveals the unique capsid organization of a dsRNA virus Pan, J.; Dong, L.; Lin, L. Proceedings of the National Academy of Sciences, Vol. 106, Issue 11 https://doi.org/10.1073/pnas.0812071106	journal	February 2009
Phaser crystallographic software McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Journal of Applied Crystallography, Vol. 40, Issue 4 https://doi.org/10.1107/S0021889807021206	journal	July 2007

Cited By (24)

Boiling Acid Mimics Intracellular Giant Virus Genome Release Schrad, Jason R.; Abrahão, Jônatas S.; Cortines, Juliana R. bioRxiv https://doi.org/10.1101/777854	posted_content	September 2019
Discovery and Further Studies on Giant Viruses at the IHU Mediterranee Infection That Modified the Perception of the Virosphere Rolland, Clara; Andreani, Julien; Louazani, Amina Viruses, Vol. 11, Issue 4 https://doi.org/10.3390/v11040312	journal	March 2019
Near-atomic structure of a giant virus Fang, Qianglin; Zhu, Dongjie; Agarkova, Irina Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-08319-6	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 Andrés, German; Charro, Diego; Matamoros, Tania Journal of Biological Chemistry, Vol. 295, Issue 1 https://doi.org/10.1074/jbc.ac119.011196	journal	October 2019
The so far farthest reaches of the double jelly roll capsid protein fold San Martín, Carmen; van Raaij, Mark J. Virology Journal, Vol. 15, Issue 1 https://doi.org/10.1186/s12985-018-1097-1	journal	November 2018
All-atom normal mode dynamics of HIV-1 capsid Na, Hyuntae; Song, Guang PLOS Computational Biology, Vol. 14, Issue 9 https://doi.org/10.1371/journal.pcbi.1006456	journal	September 2018
Diversification of giant and large eukaryotic dsDNA viruses predated the origin of modern eukaryotes Guglielmini, Julien; Woo, Anthony; Krupovic, Mart bioRxiv https://doi.org/10.1101/455816	posted_content	October 2018
Structure of the African swine fever virus major capsid protein p72 Liu, Qi; Ma, Bingting; Qian, Nianchao Cell Research, Vol. 29, Issue 11 https://doi.org/10.1038/s41422-019-0232-x	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 López-Bueno, Alberto; Mavian, Carla; Labella, Alejandro M. Journal of Virology, Vol. 90, Issue 19 https://doi.org/10.1128/jvi.01369-16	journal	July 2016
Putative Promoter Motif Analyses Reinforce the Evolutionary Relationships Among Faustoviruses, Kaumoebavirus, and Asfarvirus Oliveira, Graziele P.; de Aquino, Isabella L. M.; Luiz, Ana P. M. F. Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.01041	journal	May 2018
Medusavirus, a Novel Large DNA Virus Discovered from Hot Spring Water Yoshikawa, Genki; Blanc-Mathieu, Romain; Song, Chihong Journal of Virology, Vol. 93, Issue 8 https://doi.org/10.1128/jvi.02130-18	journal	February 2019
Faustovirus E12 Transcriptome Analysis Reveals Complex Splicing in Capsid Gene Cherif Louazani, Amina; Baptiste, Emeline; Levasseur, Anthony Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.02534	journal	October 2018
Kaumoebavirus, a New Virus That Clusters with Faustoviruses and Asfarviridae Bajrai, Leena; Benamar, Samia; Azhar, Esam Viruses, Vol. 8, Issue 11 https://doi.org/10.3390/v8110278	journal	October 2016
The Roles of Electrostatic Interactions in Capsid Assembly Mechanisms of Giant Viruses Xian, Yuejiao; Karki, Chitra B.; Silva, Sebastian Miki International Journal of Molecular Sciences, Vol. 20, Issue 8 https://doi.org/10.3390/ijms20081876	journal	April 2019
Mimivirus: leading the way in the discovery of giant viruses of amoebae Colson, Philippe; La Scola, Bernard; Levasseur, Anthony Nature Reviews Microbiology, Vol. 15, Issue 4 https://doi.org/10.1038/nrmicro.2016.197	journal	February 2017
Symmetry considerations elucidate the roles of global shape and local interactions in the equilibrium fluctuations and cooperativity of protein assemblies Song, Guang Physical Biology, Vol. 16, Issue 4 https://doi.org/10.1088/1478-3975/ab1051	journal	April 2019
Diversification of giant and large eukaryotic dsDNA viruses predated the origin of modern eukaryotes Guglielmini, Julien; Woo, Anthony C.; Krupovic, Mart Proceedings of the National Academy of Sciences, Vol. 116, Issue 39 https://doi.org/10.1073/pnas.1912006116	journal	September 2019
Protozoal giant viruses: agents potentially infectious to humans and animals Tokarz-Deptuła, Beata; Niedźwiedzka-Rystwej, Paulina; Czupryńska, Paulina Virus Genes, Vol. 55, Issue 5 https://doi.org/10.1007/s11262-019-01684-w	journal	July 2019
Architecture of African swine fever virus and implications for viral assembly Wang, Nan; Zhao, Dongming; Wang, Jialing Science, Vol. 366, Issue 6465 https://doi.org/10.1126/science.aaz1439	journal	October 2019
Cryo-EM structure of a Marseilleviridae virus particle reveals a large internal microassembly Okamoto, Kenta; Miyazaki, Naoyuki; Reddy, Hemanth K. N. Virology, Vol. 516 https://doi.org/10.1016/j.virol.2018.01.021	journal	March 2018
Cryo-EM reconstruction of the Cafeteria roenbergensis virus capsid suggests novel assembly pathway for giant viruses Xiao, Chuan; Fischer, Matthias G.; Bolotaulo, Duer M. Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-05824-w	journal	July 2017
A novel Asfarvirus-like virus identified as a potential cause of mass mortality of abalone Matsuyama, Tomomasa; Takano, Tomokazu; Nishiki, Issei Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-61492-3	journal	March 2020
Comparative Genomics Unveils Regionalized Evolution of the Faustovirus Genomes Geballa-Koukoulas, Khalil; Boudjemaa, Hadjer; Andreani, Julien Viruses, Vol. 12, Issue 5 https://doi.org/10.3390/v12050577	journal	May 2020
Microscopic Characterization of the Brazilian Giant Samba Virus Schrad, Jason; Young, Eric; Abrahão, Jônatas Viruses, Vol. 9, Issue 2 https://doi.org/10.3390/v9020030	journal	February 2017

Similar Records

Solid-to-fluid – like DNA transition in viruses facilitates infection

Journal Article · Tue Oct 14 00:00:00 EDT 2014 · Proceedings of the National Academy of Sciences of the United States of America · OSTI ID:1258668

Liu, Ting; Sae-Ueng, Udom; Li, Dong; +6 more

Segmentation and Comparative Modeling in an 8.6-Å Cryo-EM Map of the Singapore Grouper Iridovirus

Journal Article · Thu Aug 22 00:00:00 EDT 2019 · Structure · OSTI ID:1258668

Pintilie, Grigore; Chen, Dong -Hua; Tran, Bich Ngoc; +4 more

Initiation of RNA Polymerization and Polymerase Encapsidation by a Small dsRNA Virus

Journal Article · Thu Apr 14 00:00:00 EDT 2016 · PLoS Pathogens · OSTI ID:1258668

Collier, Aaron M.; Lyytinen, Outi L.; Guo, Yusong R.; +3 more

Related Subjects

60 APPLIED LIFE SCIENCES
59 BASIC BIOLOGICAL SCIENCES
faustovirus
structure
double-protein shell
major capsid protein

Title: Structure of faustovirus, a large dsDNA virus

Citation Formats

References (46)

Cited By (24)

Similar Records

Related Subjects