Are kuravirus capsid diameters quantized? The first all-atom genome tracing method for double-stranded DNA viruses
Jazyk angličtina Země Anglie, Velká Británie Médium print
Typ dokumentu časopisecké články
Grantová podpora
VR-M 2016-06301
Vetenskapsrådet
Swedish University of Agricultural Sciences and Stockholm University
PubMed
38084886
PubMed Central
PMC10853797
DOI
10.1093/nar/gkad1153
PII: 7469970
Knihovny.cz E-zdroje
- MeSH
- DNA virů genetika metabolismus MeSH
- elektronová kryomikroskopie MeSH
- kapsida * metabolismus MeSH
- Podoviridae * MeSH
- sestavení viru genetika MeSH
- virové plášťové proteiny genetika metabolismus MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- DNA virů MeSH
- virové plášťové proteiny MeSH
The revolution in cryo-electron microscopy has resulted in unprecedented power to resolve large macromolecular complexes including viruses. Many methods exist to explain density corresponding to proteins and thus entire protein capsids have been solved at the all-atom level. However methods for nucleic acids lag behind, and no all-atom viral double-stranded DNA genomes have been published at all. We here present a method which exploits the spiral winding patterns of DNA in icosahedral capsids. The method quickly generates shells of DNA wound in user-specified, idealized spherical or cylindrical spirals. For transition regions, the method allows guided semiflexible fitting. For the kuravirus SU10, our method explains most of the density in a semiautomated fashion. The results suggest rules for DNA turns in the end caps under which two discrete parameters determine the capsid inner diameter. We suggest that other kuraviruses viruses may follow the same winding scheme, producing a discrete rather than continuous spectrum of capsid inner diameters. Our software may be used to explain the published density maps of other double-stranded DNA viruses and uncover their genome packaging principles.
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Zhou Z.H., Chen D.H., Jakana J., Rixon F.J., Chiu W.. Visualization of tegument-capsid interactions and DNA in intact herpes simplex virus type 1 virions. J. Virol. 1999; 73:3210–3218. PubMed PMC
Liu Y.T., Jih J., Dai X., Bi G.Q., Zhou Z.H.. Cryo-EM structures of herpes simplex virus type 1 portal vertex and packaged genome. Nature. 2019; 570:257–261. PubMed PMC
Cerritelli M.E., Cheng N., Rosenberg A.H., McPherson C.E., Booy F.P., Steven A.C.. Encapsidated conformation of bacteriophage T7 DNA. Cell. 1997; 91:271–280. PubMed
Purohit P.K., Inamdar M.M., Grayson P.D., Squires T.M., Kondev J., Phillips R.. Forces during bacteriophage DNA packaging and ejection. Biophys. J. 2005; 88:851–866. PubMed PMC
Widom J., Baldwin R.L.. Tests of spool models for DNA packaging in phage lambda. J. Mol. Biol. 1983; 171:419–437. PubMed
Harrison S.C. Packaging of DNA into bacteriophage heads: a model. J. Mol. Biol. 1983; 171:577–580. PubMed
Arsuaga J., Tan R.K., Vazquez M., Sumners D.W., Harvey S.C.. Investigation of viral DNA packaging using molecular mechanics models. Biophys. Chem. 2002; 101-102:475–484. PubMed
Lepault J., Dubochet J., Baschong W., Kellenberger E.. Organization of double-stranded DNA in bacteriophages: a study by cryo-electron microscopy of vitrified samples. EMBO J. 1987; 6:1507–1512. PubMed PMC
Petrov A.S., Harvey S.C.. Packaging double-helical DNA into viral capsids: structures, forces, and energetics. Biophys. J. 2008; 95:497–502. PubMed PMC
Leontis N.B., Stombaugh J., Westhof E.. The non-Watson-Crick base pairs and their associated isostericity matrices. Nucleic Acids Res. 2002; 30:3497–3531. PubMed PMC
Siborova M., Fuzik T., Prochazkova M., Novacek J., Benesik M., Nilsson A.S., Plevka P.. Tail proteins of phage SU10 reorganize into the nozzle for genome delivery. Nat. Commun. 2022; 13:5622. PubMed PMC
Hrebik D., Stverakova D., Skubnik K., Fuzik T., Pantucek R., Plevka P.. Structure and genome ejection mechanism of Staphylococcus aureus phage P68. Sci. Adv. 2019; 5:eaaw7414. PubMed PMC
Goddard T.D., Huang C.C., Ferrin T.E.. Visualizing density maps with UCSF Chimera. J. Struct. Biol. 2007; 157:281–287. PubMed
Goodsell D.S., Dickerson R.E.. Bending and curvature calculations in B-DNA. Nucleic Acids Res. 1994; 22:5497–5503. PubMed PMC
Cerny J., Bozikova P., Svoboda J., Schneider B.. A unified dinucleotide alphabet describing both RNA and DNA structures. Nucleic Acids Res. 2020; 48:6367–6381. PubMed PMC
Zgarbova M., Sponer J., Otyepka M., Cheatham T.E., Galindo-Murillo R., Jurecka P.. Refinement of the sugar-phosphate backbone torsion beta for AMBER force fields improves the description of Z- and B-DNA. J. Chem. Theory Comput. 2015; 11:5723–5736. PubMed
Tek A., Korostelev A.A., Flores S.C.. MMB-GUI: a fast morphing method demonstrates a possible ribosomal tRNA translocation trajectory. Nucleic Acids Res. 2016; 44:95–105. PubMed PMC
Cerny J., Bozikova P., Maly M., Tykac M., Biedermannova L., Schneider B.. Structural alphabets for conformational analysis of nucleic acids available at dnatco.Datmos.Org. Acta Crystallogr D Struct Biol. 2020; 76:805–813. PubMed PMC
Cerny J., Bozikova P., Schneider B.. DNATCO: assignment of DNA conformers at dnatco.Org. Nucleic Acids Res. 2016; 44:W284–W287. PubMed PMC
Schneider B., Bozikova P., Cech P., Svozil D., Cerny J.. A DNA structural alphabet distinguishes structural features of DNA bound to regulatory proteins and in the nucleosome core particle. Genes (Basel). 2017; 8:278. PubMed PMC
Flores S.C. Fast fitting to low resolution density maps: elucidating large-scale motions of the ribosome. Nucleic Acids Res. 2014; 42:e9. PubMed PMC
Prytkova T.R., Zhu X., Widom J., Schatz G.C.. Modeling DNA-bending in the nucleosome: role of AA periodicity. J. Phys. Chem. B. 2011; 115:8638–8644. PubMed PMC
Khan Mirzaei M., Eriksson H., Kasuga K., Haggard-Ljungquist E., Nilsson A.S.. Genomic, proteomic, morphological, and phylogenetic analyses of vB_EcoP_SU10, a podoviridae phage with C3 morphology. PLoS One. 2014; 9:e116294. PubMed PMC
Kwon J., Kim S.G., Giri S.S., Kim H.J., Kim S.W., Kang J.W., Lee S.B., Jung W.J., Chi C., Park S.C.. Genomic characterization of bacteriophage pSal-SNUABM-01, a novel elongated-head phage infecting Salmonella sp. Arch. Virol. 2022; 167:655–658. PubMed
Spakowitz A.J., Wang Z.G.. DNA packaging in bacteriophage: is twist important?. Biophys. J. 2005; 88:3912–3923. PubMed PMC
Renzo P., Talledo M., Arcondo M., Suárez K., Zumaeta K.. Isolation and characterization of ΦGF1, a morphotype C3 bacteriophage that infects Escherichia coli. 2019; bioRxiv doi:05 May 2019, preprint: not peer reviewed10.1101/627976. DOI
Batinovic S., Fujii Y., Nittami T.. Expansion of kuravirus-like phage sequences within the past decade, including Escherichia Phage YF01 from Japan, prompt the creation of three new genera. Viruses. 2023; 15:506. PubMed PMC
Kropinski A.M., Lingohr E.J., Ackermann H.W.. The genome sequence of enterobacterial phage 7-11, which possesses an unusually elongated head. Arch. Virol. 2011; 156:149–151. PubMed
Ren H., Li Z., Xu L., Li X., Wang L., Xu Y.. Genome sequence analysis of Vibrio parahaemolyticus lytic phage Vp_R1 with a C3 morphotype. Arch. Virol. 2019; 164:2865–2871. PubMed