Are kuravirus capsid diameters quantized? The first all-atom genome tracing method for double-stranded DNA viruses

. 2024 Feb 09 ; 52 (3) : e12.

Jazyk angličtina Země Anglie, Velká Británie Médium print

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid38084886

Grantová podpora
VR-M 2016-06301 Vetenskapsrådet
Swedish University of Agricultural Sciences and Stockholm University

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.

Zobrazit více v PubMed

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

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...