Cited by 34Bacteriophages and microbial interactionsPlant and Fungal Interactions ResearchAdvanced Electron Microscopy Techniques and Applications

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The giant mimivirus 1.2 Mb genome is elegantly organized into a 30-nm diameter helical protein shield

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Abstract

Mimivirus is the prototype of the Mimiviridae family of giant dsDNA viruses. Little is known about the organization of the 1.2 Mb genome inside the membrane-limited nucleoid filling the ~0.5 µm icosahedral capsids. Cryo-electron microscopy, cryo-electron tomography, and proteomics revealed that it is encased into a ~30-nm diameter helical protein shell surprisingly composed of two GMC-type oxidoreductases, which also form the glycosylated fibrils decorating the capsid. The genome is arranged in 5- or 6-start left-handed super-helices, with each DNA-strand lining the central channel. This luminal channel of the nucleoprotein fiber is wide enough to accommodate oxidative stress proteins and RNA polymerase subunits identified by proteomics. Such elegant supramolecular organization would represent a remarkable evolutionary strategy for packaging and protecting the genome, in a state ready for immediate transcription upon unwinding in the host cytoplasm. The parsimonious use of the same protein in two unrelated substructures of the virion is unexpected for a giant virus with thousand genes at its disposal.

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Research works printed but not linked: 77

  1. Abergel, 2007, Virus-encoded aminoacyl-tRNA synthetases: structural and functional characterization of mimivirus TyrRS and MetRS, Journal of Virology, 81, 12406, 10.1128/JVI.01107-07 · DOI
  2. Abergel, 2015, The rapidly expanding universe of giant viruses: Mimivirus, Pandoravirus, Pithovirus and Mollivirus, FEMS Microbiology Reviews, 39, 779, 10.1093/femsre/fuv037 · DOI
  3. Arslan, 2011, Distant Mimivirus relative with a larger genome highlights the fundamental features of Megaviridae, PNAS, 108, 17486, 10.1073/pnas.1110889108 · DOI
  4. Bai, 2015, Sampling the conformational space of the catalytic subunit of human γ-secretase, eLife, 4, 10.7554/eLife.11182 · DOI
  5. Bell, 2001, Viral eukaryogenesis: was the ancestor of the nucleus a complex DNA virus?, Journal of Molecular Evolution, 53, 251, 10.1007/s002390010215 · DOI
  6. Bell, 2020, Evidence supporting a viral origin of the eukaryotic nucleus, Virus Research, 289, 10.1016/j.virusres.2020.198168 · DOI
  7. Blanc-Mathieu, 2021, A persistent giant algal virus, with A unique morphology, encodes an unprecedented number of genes involved in energy metabolism, Journal of Virology, 95, e02446, 10.1128/JVI.02446-20 · DOI
  8. Bouyssié, 2020, Proline: an efficient and user-friendly software suite for large-scale proteomics, Bioinformatics, 36, 3148, 10.1093/bioinformatics/btaa118 · DOI · Paper page
  9. Boyer, 2011, Mimivirus shows dramatic genome reduction after intraamoebal culture, PNAS, 108, 10296, 10.1073/pnas.1101118108 · DOI
  10. Casabona, 2013, Proteomic characterization of Pseudomonas aeruginosa PAO1 inner membrane, Proteomics, 13, 2419, 10.1002/pmic.201200565 · DOI
  11. Chaikeeratisak, 2017, Assembly of a nucleus-like structure during viral replication in bacteria, Science, 355, 194, 10.1126/science.aal2130 · DOI
  12. Chelikani, 2014, Revisiting the genome packaging in viruses with lessons from the “Giants.”, Virology, 466–467, 15, 10.1016/j.virol.2014.06.022 · DOI
  13. Cheng, 2014, Exploiting radiation damage to map proteins in nucleoprotein complexes: the internal structure of bacteriophage T7, Journal of Structural Biology, 185, 250, 10.1016/j.jsb.2013.12.004 · DOI
  14. Claverie, 2006, Viruses take center stage in cellular evolution, Genome Biology, 7, 10.1186/gb-2006-7-6-110 · DOI
  15. Claverie, 2009, Mimivirus and Mimiviridae: giant viruses with an increasing number of potential hosts, including corals and sponges, Journal of Invertebrate Pathology, 101, 172, 10.1016/j.jip.2009.03.011 · DOI
  16. Claverie, 2010, Mimivirus: the emerging paradox of quasi-autonomous viruses, Trends in Genetics, 26, 431, 10.1016/j.tig.2010.07.003 · DOI
  17. Collier, 2016, Initiation of rna polymerization and polymerase encapsidation by a small dsrna virus, PLOS Pathogens, 12, 10.1371/journal.ppat.1005523 · DOI
  18. Colson, 2017, Mimivirus: leading the way in the discovery of giant viruses of amoebae, Nature Reviews. Microbiology, 15, 243, 10.1038/nrmicro.2016.197 · DOI
  19. Coudray, 2016, Deducing the symmetry of helical assemblies: Applications to membrane proteins, Journal of Structural Biology, 195, 167, 10.1016/j.jsb.2016.05.011 · DOI
  20. Diaz, 2010, Fourier-Bessel reconstruction of helical assemblies, Methods in Enzymology, 482, 131, 10.1016/S0076-6879(10)82005-1 · DOI
  21. DiMaio, 2015, Virology: A virus that infects A hyperthermophile encapsidates A-form DNA, Science, 348, 914, 10.1126/science.aaa4181 · DOI
  22. Ding, 2019, In situ structures of rotavirus polymerase in action and mechanism of mRNA transcription and release, Nature Communications, 10, 10.1038/s41467-019-10236-7 · DOI
  23. Ekeberg, 2015, Three-dimensional reconstruction of the giant mimivirus particle with an x-ray free-electron laser, Physical Review Letters, 114, 10.1103/PhysRevLett.114.098102 · DOI
  24. Estrozi, 2008, Fast projection matching for cryo-electron microscopy image reconstruction, Journal of Structural Biology, 162, 324, 10.1016/j.jsb.2008.01.014 · DOI
  25. Forterre, 2010, Giant viruses: conflicts in revisiting the virus concept, Intervirology, 53, 362, 10.1159/000312921 · DOI
  26. Goddard, 2018, Ucsf chimerax: Meeting modern challenges in visualization and analysis: Ucsf chimerax visualization system, Protein Science: A Publication of the Protein Society, 27, 14, 10.1002/pro.3235 · DOI · Paper page
  27. Gong, 2019, Dna-packing portal and capsid-associated tegument complexes in the tumor herpesvirus kshv, Cell, 178, 1329, 10.1016/j.cell.2019.07.035 · DOI
  28. Grimm, 2019, Structural basis of poxvirus transcription: vaccinia rna polymerase complexes, Cell, 179, 1537, 10.1016/j.cell.2019.11.024 · DOI
  29. Guizar-Sicairos, 2008, Efficient subpixel image registration algorithms, Optics Letters, 33, 156, 10.1364/ol.33.000156 · DOI
  30. Hagen, 2017, Implementation of a cryo-electron tomography tilt-scheme optimized for high resolution subtomogram averaging, Journal of Structural Biology, 197, 191, 10.1016/j.jsb.2016.06.007 · DOI
  31. Hahsler, 2019, Doran, dbscan: fast density-based clustering with R, Journal of Statistical Software, 91, 10.18637/jss.v091.i01 · DOI
  32. Harris, 2020, Array programming with NumPy, Nature, 585, 357, 10.1038/s41586-020-2649-2 · DOI · Paper page
  33. He, 2017, Helical reconstruction in RELION, Journal of Structural Biology, 198, 163, 10.1016/j.jsb.2017.02.003 · DOI
  34. Heymann, 2007, Bsoft: image processing and molecular modeling for electron microscopy, Journal of Structural Biology, 157, 3, 10.1016/j.jsb.2006.06.006 · DOI
  35. Kaneko, 2021, Eukaryotic virus composition can predict the efficiency of carbon export in the global ocean, IScience, 24, 10.1016/j.isci.2020.102002 · DOI
  36. Klose, 2010, The three-dimensional structure of mimivirus, Intervirology, 53, 268, 10.1159/000312911 · DOI
  37. Klose, 2015, A mimivirus enzyme that participates in viral entry, Structure, 23, 1058, 10.1016/j.str.2015.03.023 · DOI
  38. Kremer, 1996, Computer visualization of three-dimensional image data using IMOD, Journal of Structural Biology, 116, 71, 10.1006/jsbi.1996.0013 · DOI
  39. Kuznetsov, 2010, Atomic force microscopy investigation of the giant mimivirus, Virology, 404, 127, 10.1016/j.virol.2010.05.007 · DOI
  40. Kuznetsov, 2013, Morphogenesis of mimivirus and its viral factories: an atomic force microscopy study of infected cells, Journal of Virology, 87, 11200, 10.1128/JVI.01372-13 · DOI
  41. La Scola, 2003, A giant virus in amoebae, Science, 299, 10.1126/science.1081867 · DOI · Paper page
  42. Li, 2019, Web 3DNA 2.0 for the analysis, visualization, and modeling of 3D nucleic acid structures, Nucleic Acids Research, 47, W26, 10.1093/nar/gkz394 · DOI
  43. Liebschner, 2019, Macromolecular structure determination using X-rays, neutrons and electrons: recent developments in Phenix, Acta Crystallographica. Section D, Structural Biology, 75, 861, 10.1107/S2059798319011471 · DOI · Paper page
  44. Liu, 2019, Cryo-EM structures of herpes simplex virus type 1 portal vertex and packaged genome, Nature, 570, 257, 10.1038/s41586-019-1248-6 · DOI
  45. Liu, 2021, Virus-encoded histone doublets are essential and form nucleosome-like structures, Cell, 184, 4237, 10.1016/j.cell.2021.06.032 · DOI
  46. Malkin, 2003, Structure of intracellular mature vaccinia virus visualized by in situ atomic force microscopy, Journal of Virology, 77, 6332, 10.1128/jvi.77.11.6332-6340.2003 · DOI
  47. Mannor, 2011, K-Means Clustering, 563
  48. Mastronarde, 2005, Automated electron microscope tomography using robust prediction of specimen movements, Journal of Structural Biology, 152, 36, 10.1016/j.jsb.2005.07.007 · DOI
  49. Mishyna, 2017, Effects of radiation damage in studies of protein-DNA complexes by cryo-EM, Micron, 96, 57, 10.1016/j.micron.2017.02.004 · DOI
  50. Moniruzzaman, 2020, Widespread endogenization of giant viruses shapes genomes of green algae, Nature, 588, 141, 10.1038/s41586-020-2924-2 · DOI
  51. Mutsafi, 2014, Infection cycles of large DNA viruses: emerging themes and underlying questions, Virology, 466–467, 3, 10.1016/j.virol.2014.05.037 · DOI
  52. Notaro, 2021, Expanding the occurrence of polysaccharides to the viral world: the case of mimivirus, Angewandte Chemie, 60, 19897, 10.1002/anie.202106671 · DOI
  53. Pedregosa, 2011, Scikit-learn: machine learning in python, Journal of Machine Learning Research: JMLR, 12, 2825
  54. Pettersen, 2004, UCSF Chimera--A visualization system for exploratory research and analysis, Journal of Computational Chemistry, 25, 1605, 10.1002/jcc.20084 · DOI
  55. Piacente, 2017, The rare sugar N-acetylated viosamine is a major component of Mimivirus fibers, The Journal of Biological Chemistry, 292, 7385, 10.1074/jbc.M117.783217 · DOI
  56. Pintilie, 2010, Quantitative analysis of cryo-EM density map segmentation by watershed and scale-space filtering, and fitting of structures by alignment to regions, Journal of Structural Biology, 170, 427, 10.1016/j.jsb.2010.03.007 · DOI
  57. Ptchelkine, 2017, Unique architecture of thermophilic archaeal virus APBV1 and its genome packaging, Nature Communications, 8, 10.1038/s41467-017-01668-0 · DOI
  58. Rao, 2015, Mechanisms of dna packaging by large double-stranded dna viruses, Annual Review of Virology, 2, 351, 10.1146/annurev-virology-100114-055212 · DOI
  59. Raoult, 2004, The 1.2-megabase genome sequence of Mimivirus, Science, 306, 1344, 10.1126/science.1101485 · DOI
  60. Robinson, 2006, EM measurements define the dimensions of the “30-nm” chromatin fiber: evidence for a compact, interdigitated structure, PNAS, 103, 6506, 10.1073/pnas.0601212103 · DOI
  61. Rohou, 2015, CTFFIND4: Fast and accurate defocus estimation from electron micrographs, Journal of Structural Biology, 192, 216, 10.1016/j.jsb.2015.08.008 · DOI
  62. Sachse, 2015, EMBL—european molecular biology laboratory, structural and computational biology unit, meyerhofstr, AIMS Biophysics, 2, 219, 10.3934/biophy.2015.2.219 · DOI
  63. Scheres, 2012, RELION: implementation of a Bayesian approach to cryo-EM structure determination, Journal of Structural Biology, 180, 519, 10.1016/j.jsb.2012.09.006 · DOI · Paper page
  64. Schrad, 2020, Structural and proteomic characterization of the initiation of giant virus infection, Cell, 181, 1046, 10.1016/j.cell.2020.04.032 · DOI
  65. Schulz, 2020, Giant virus diversity and host interactions through global metagenomics, Nature, 578, 432, 10.1038/s41586-020-1957-x · DOI
  66. Suhre, 2005, Mimivirus gene promoters exhibit an unprecedented conservation among all eukaryotes, PNAS, 102, 14689, 10.1073/pnas.0506465102 · DOI
  67. Sun, 2015, Cryo-EM structure of the bacteriophage T4 portal protein assembly at near-atomic resolution, Nature Communications, 6, 10.1038/ncomms8548 · DOI
  68. Suzan-Monti, 2007, Ultrastructural characterization of the giant volcano-like virus factory of Acanthamoeba polyphaga Mimivirus, PLOS ONE, 2, 10.1371/journal.pone.0000328 · DOI
  69. Takemura, 2001, Poxviruses and the origin of the eukaryotic nucleus, Journal of Molecular Evolution, 52, 419, 10.1007/s002390010171 · DOI
  70. Toriyama, 1986, An rna-dependent rna polymerase associated with the filamentous nucleoproteins of rice stripe virus, Journal of General Virology, 67, 1247, 10.1099/0022-1317-67-7-1247 · DOI
  71. Valencia-Sánchez, 2021, The structure of a virus-encoded nucleosome, Nature Structural & Molecular Biology, 28, 413, 10.1038/s41594-021-00585-7 · DOI
  72. Wang, 2020, Structures of filamentous viruses infecting hyperthermophilic archaea explain DNA stabilization in extreme environments, PNAS, 117, 19643, 10.1073/pnas.2011125117 · DOI
  73. Waterhouse, 2018, SWISS-MODEL: homology modelling of protein structures and complexes, Nucleic Acids Research, 46, W296, 10.1093/nar/gky427 · DOI
  74. Wu, 2012, Bubblegrams reveal the inner body of bacteriophage φKZ, Science, 335, 10.1126/science.1214120 · DOI
  75. Xiao, 2009, Structural studies of the giant mimivirus, PLOS Biology, 7, 10.1371/journal.pbio.1000092 · DOI
  76. Zauberman, 2008, Distinct DNA exit and packaging portals in the virus Acanthamoeba polyphaga mimivirus, PLOS Biology, 6, 10.1371/journal.pbio.0060114 · DOI
  77. Zheng, 2017, MotionCor2: anisotropic correction of beam-induced motion for improved cryo-electron microscopy, Nature Methods, 14, 331, 10.1038/nmeth.4193 · DOI

Metadata

Authors
Villalta, A., Schmitt, A., Estrozi, L. F., Quemin, E. R., Alempic, J.-M., Lartigue, A., Pražák, V., Belmudes, L., Vasishtan, D., Colmant, A. M., Honoré, F. A., Couté, Y., Grünewald, K., & Abergel, C.
Affiliations
  • Centre National de la Recherche Scientifique (FR)
  • Leibniz Institute of Virology (LIV) (DE)
  • Centre for Human Genetics (GB)
  • Inserm (FR)
Corresponding author
Abergel, Chantal
Venue
eLife
Published
2022-07-28
Volume
11
ISSN
2050-084X (ISSN-L)
OpenAlex
W4288096192
Cited by
34
References
1
Citations by year
2026: 2 · 2025: 11 · 2024: 6 · 2023: 8 · 2022: 7
FWCI
4.26
Type
journal article
Language
en
Open access
Locations
  • eLife (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • HAL (submittedVersion, cc-by)
  • Desy publication database (The Deutsches Elektronen-Synchrotron) (submittedVersion, other-oa)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • European Research Council (832601)
  • Agence Nationale de la Recherche (ANR-16-CE11-0033-01, ANR-10-INBS-08-01, ANR-17-EURE-0003, ANR-10-INBS-04)
  • Wellcome Trust (107806/Z/15/Z)
  • Deutsche Forschungsgemeinschaft (INST 152/772-1|152/774-1|152/775-1|152/776-1)
  • Alexander von Humboldt-Stiftung (FRA 1200789 HFST-P)
Topics
  • Life Sciences › Immunology and Microbiology › Virology › Bacteriophages and microbial interactions
  • Life Sciences › Immunology and Microbiology › Virology › Plant and Fungal Interactions Research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Structural Biology › Advanced Electron Microscopy Techniques and Applications
Keywords
giant viruses, viral genome structure, nucleoid, supercoiled DNA, oxidative stress proteins, RNA polymerase, viral proteome, genome packaging
MeSH terms
Giant Viruses, Capsid, Nucleoproteins, Oxidoreductases, Genome, Viral, Cryoelectron Microscopy, Mimiviridae

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