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Structural assembly of the tailed bacteriophage ϕ29.

Xu J, Wang D, Gui M, Xiang Y
Nat Commun 10 2366 (2019)
Related entries: 6qvk, 6qx7, 6qyd, 6qyj, 6qym, 6qyy, 6qyz, 6qz9, 6qzf

Cited: 27 times
EuropePMC logo PMID: 31147544

Abstract

The mature virion of the tailed bacteriophage ϕ29 is an ~33 MDa complex that contains more than 450 subunits of seven structural proteins assembling into a prolate head and a short non-contractile tail. Here, we report the near-atomic structures of the ϕ29 pre-genome packaging head (prohead), the mature virion and the genome-emptied virion. Structural comparisons suggest local rotation or oscillation of the head-tail connector upon DNA packaging and release. Termination of the DNA packaging occurs through pressure-dependent correlative positional and conformational changes in the connector. The funnel-shaped tail lower collar attaches the expanded narrow end of the connector and has a 180-Å long, 24-strand β barrel narrow stem tube that undergoes conformational changes upon genome release. The appendages form an interlocked assembly attaching the tail around the collar. The membrane active long loops at the distal end of the tail knob exit during the late stage of infection and form the cone-shaped tip of a largely hydrophobic helix barrel, prepared for membrane penetration.

Reviews citing this publication (7)

  1. NMR as a "Gold Standard" Method in Drug Design and Discovery. Emwas AH, Szczepski K, Poulson BG, Chandra K, McKay RT, Dhahri M, Alahmari F, Jaremko L, Lachowicz JI, Jaremko M. Molecules 25 E4597 (2020)
  2. Structural Insights into RNA Dimerization: Motifs, Interfaces and Functions. Bou-Nader C, Zhang J. Molecules 25 E2881 (2020)
  3. Keeping It Together: Structures, Functions, and Applications of Viral Decoration Proteins. Dedeo CL, Teschke CM, Alexandrescu AT. Viruses 12 E1163 (2020)
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  6. A Tour de Force on the Double Helix: Exploiting DNA Mechanics To Study DNA-Based Molecular Machines. Wasserman MR, Liu S. Biochemistry 58 4667-4676 (2019)
  7. Revolving hexameric ATPases as asymmetric motors to translocate double-stranded DNA genome along one strand. Bohmer M, Bhullar AS, Weitao T, Zhang L, Lee JH, Guo P. iScience 26 106922 (2023)

Articles citing this publication (20)

  1. A viral genome packaging motor transitions between cyclic and helical symmetry to translocate dsDNA. Woodson M, Pajak J, Mahler BP, Zhao W, Zhang W, Arya G, White MA, Jardine PJ, Morais MC. Sci Adv 7 eabc1955 (2021)
  2. A novel vibriophage exhibits inhibitory activity against host protein synthesis machinery. Thammatinna K, Egan ME, Htoo HH, Khanna K, Sugie J, Nideffer JF, Villa E, Tassanakajon A, Pogliano J, Nonejuie P, Chaikeeratisak V. Sci Rep 10 2347 (2020)
  3. Cryo-EM structure in situ reveals a molecular switch that safeguards virus against genome loss. Bayfield OW, Steven AC, Antson AA. Elife 9 e55517 (2020)
  4. Structural changes in bacteriophage T7 upon receptor-induced genome ejection. Chen W, Xiao H, Wang L, Wang X, Tan Z, Han Z, Li X, Yang F, Liu Z, Song J, Liu H, Cheng L. Proc Natl Acad Sci U S A 118 e2102003118 (2021)
  5. A Novel Genus of Actinobacterial Tectiviridae. Caruso SM, deCarvalho TN, Huynh A, Morcos G, Kuo N, Parsa S, Erill I. Viruses 11 E1134 (2019)
  6. Structures of a large prolate virus capsid in unexpanded and expanded states generate insights into the icosahedral virus assembly. Fang Q, Tang WC, Fokine A, Mahalingam M, Shao Q, Rossmann MG, Rao VB. Proc Natl Acad Sci U S A 119 e2203272119 (2022)
  7. CryoEM structure and assembly mechanism of a bacterial virus genome gatekeeper. Orlov I, Roche S, Brasilès S, Lukoyanova N, Vaney MC, Tavares P, Orlova EV. Nat Commun 13 7283 (2022)
  8. Isolation and Characterisation of the Bundooravirus Genus and Phylogenetic Investigation of the Salasmaviridae Bacteriophages. Stanton CR, Rice DTF, Beer M, Batinovic S, Petrovski S. Viruses 13 1557 (2021)
  9. Structure and host specificity of Staphylococcus epidermidis bacteriophage Andhra. Hawkins NC, Kizziah JL, Hatoum-Aslan A, Dokland T. Sci Adv 8 eade0459 (2022)
  10. Insights into a viral motor: the structure of the HK97 packaging termination assembly. Hawkins DEDP, Bayfield OW, Fung HKH, Grba DN, Huet A, Conway JF, Antson AA. Nucleic Acids Res 51 7025-7035 (2023)
  11. A structural dendrogram of the actinobacteriophage major capsid proteins provides important structural insights into the evolution of capsid stability. Podgorski JM, Freeman K, Gosselin S, Huet A, Conway JF, Bird M, Grecco J, Patel S, Jacobs-Sera D, Hatfull G, Gogarten JP, Ravantti J, White SJ. Structure 31 282-294.e5 (2023)
  12. NMR Mapping of Disordered Segments from a Viral Scaffolding Protein Enclosed in a 23 MDa Procapsid. Whitehead RD, Teschke CM, Alexandrescu AT. Biophys J 117 1387-1392 (2019)
  13. A symmetry mismatch unraveled: How phage HK97 scaffold flexibly accommodates a 12-fold pore at a 5-fold viral capsid vertex. Huet A, Oh B, Maurer J, Duda RL, Conway JF. Sci Adv 9 eadg8868 (2023)
  14. Tryptophan Residues Are Critical for Portal Protein Assembly and Incorporation in Bacteriophage P22. Woodbury BM, Motwani T, Leroux MN, Barnes LF, Lyktey NA, Banerjee S, Dedeo CL, Jarrold MF, Teschke CM. Viruses 14 1400 (2022)
  15. A Capsid Structure of Ralstonia solanacearum podoviridae GP4 with a Triangulation Number T = 9. Zheng J, Chen W, Xiao H, Yang F, Li X, Song J, Cheng L, Liu H. Viruses 14 2431 (2022)
  16. Cryo-EM Structures of Two Bacteriophage Portal Proteins Provide Insights for Antimicrobial Phage Engineering. Javed A, Villanueva H, Shataer S, Vasciaveo S, Savva R, Orlova EV. Viruses 13 2532 (2021)
  17. Neck and capsid architecture of the robust Agrobacterium phage Milano. Sonani RR, Esteves NC, Horton AA, Kelly RJ, Sebastian AL, Wang F, Kreutzberger MAB, Leiman PG, Scharf BE, Egelman EH. Commun Biol 6 921 (2023)
  18. Complete genome sequence of phi29-like Microbacterium foliorum podovirus phage PineapplePizza. LaBianca K, Butura J, McKnight A, Pan K, Whelan S, Punska E, Pause R, Igbinosa B, Ribbe A, Chien P, Russell D, Garlena R, Hatfull G, Jacobs-Sera D, Rocheleau J. Microbiol Resour Announc 12 e0047823 (2023)
  19. New Obolenskvirus Phages Brutus and Scipio: Biology, Evolution, and Phage-Host Interaction. Evseev PV, Shneider MM, Kolupaeva LV, Kasimova AA, Timoshina OY, Perepelov AV, Shpirt AM, Shelenkov AA, Mikhailova YV, Suzina NE, Knirel YA, Miroshnikov KA, Popova AV. Int J Mol Sci 25 2074 (2024)
  20. Structure of the siphophage neck-Tail complex suggests that conserved tail tip proteins facilitate receptor binding and tail assembly. Xiao H, Tan L, Tan Z, Zhang Y, Chen W, Li X, Song J, Cheng L, Liu H. PLoS Biol 21 e3002441 (2023)


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