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Double-stranded RNA virus outer shell assembly by bona fide domain-swapping.

<div class='caption-title'>Cryo-EM structure of bacteriophage 6 nucleocapsid.</div>
<div class='caption-title'>Domain swapped architecture of the outer 6 P8 shell.</div>
<div class='caption-title'>Hexameric packaging ATPase P4.</div>
Sun Z, El Omari K, Sun X, Ilca SL, Kotecha A, Stuart DI, Poranen MM, Huiskonen JT
OpenAccess logo Nat Commun 8 14814 (2017)
Related entries: 5muv, 5muw

Cited: 23 times
EuropePMC logo PMID: 28287099

Abstract

Correct outer protein shell assembly is a prerequisite for virion infectivity in many multi-shelled dsRNA viruses. In the prototypic dsRNA bacteriophage φ6, the assembly reaction is promoted by calcium ions but its biomechanics remain poorly understood. Here, we describe the near-atomic resolution structure of the φ6 double-shelled particle. The outer T=13 shell protein P8 consists of two alpha-helical domains joined by a linker, which allows the trimer to adopt either a closed or an open conformation. The trimers in an open conformation swap domains with each other. Our observations allow us to propose a mechanistic model for calcium concentration regulated outer shell assembly. Furthermore, the structure provides a prime exemplar of bona fide domain-swapping. This leads us to extend the theory of domain-swapping from the level of monomeric subunits and multimers to closed spherical shells, and to hypothesize a mechanism by which closed protein shells may arise in evolution.

Articles - 5muu mentioned but not cited (1)

  1. Double-stranded RNA virus outer shell assembly by bona fide domain-swapping. Sun Z, El Omari K, Sun X, Ilca SL, Kotecha A, Stuart DI, Poranen MM, Huiskonen JT. Nat Commun 8 14814 (2017)


Reviews citing this publication (4)

  1. Half a Century of Research on Membrane-Containing Bacteriophages: Bringing New Concepts to Modern Virology. Mäntynen S, Sundberg LR, Oksanen HM, Poranen MM. Viruses 11 E76 (2019)
  2. Chloroquine to fight COVID-19: A consideration of mechanisms and adverse effects? Zhan X, Dowell S, Shen Y, Lee DL. Heliyon 6 e04900 (2020)
  3. Diversity and Current Classification of dsRNA Bacteriophages. Mäntynen S, Salomaa MM, Poranen MM. Viruses 15 2154 (2023)
  4. Structural Studies of Bacteriophage Φ6 and Its Transformations during Its Life Cycle. Heymann JB. Viruses 15 2404 (2023)

Articles citing this publication (18)

  1. Shielding and activation of a viral membrane fusion protein. Halldorsson S, Li S, Li M, Harlos K, Bowden TA, Huiskonen JT. Nat Commun 9 349 (2018)
  2. Evolution of a virus-like architecture and packaging mechanism in a repurposed bacterial protein. Tetter S, Terasaka N, Steinauer A, Bingham RJ, Clark S, Scott AJP, Patel N, Leibundgut M, Wroblewski E, Ban N, Stockley PG, Twarock R, Hilvert D. Science 372 1220-1224 (2021)
  3. Recognition of six additional cystoviruses: Pseudomonas virus phi6 is no longer the sole species of the family Cystoviridae. Mäntynen S, Sundberg LR, Poranen MM. Arch Virol 163 1117-1124 (2018)
  4. ICTV Virus Taxonomy Profile: Cystoviridae. Poranen MM, Mäntynen S, Ictv Report Consortium. J Gen Virol 98 2423-2424 (2017)
  5. Structure Unveils Relationships between RNA Virus Polymerases. Mönttinen HAM, Ravantti JJ, Poranen MM. Viruses 13 313 (2021)
  6. Genome organization and interaction with capsid protein in a multipartite RNA virus. Beren C, Cui Y, Chakravarty A, Yang X, Rao ALN, Knobler CM, Zhou ZH, Gelbart WM. Proc Natl Acad Sci U S A 117 10673-10680 (2020)
  7. Mycobacterium tuberculosis CarD, an essential global transcriptional regulator forms amyloid-like fibrils. Kaur G, Kaundal S, Kapoor S, Grimes JM, Huiskonen JT, Thakur KG. Sci Rep 8 10124 (2018)
  8. Image processing for cryogenic transmission electron microscopy of symmetry-mismatched complexes. Huiskonen JT. Biosci Rep 38 BSR20170203 (2018)
  9. Acquisition of functions on the outer capsid surface during evolution of double-stranded RNA fungal viruses. Mata CP, Luque D, Gómez-Blanco J, Rodríguez JM, González JM, Suzuki N, Ghabrial SA, Carrascosa JL, Trus BL, Castón JR. PLoS Pathog 13 e1006755 (2017)
  10. Capsid Structure of Leishmania RNA Virus 1. Procházková M, Füzik T, Grybchuk D, Falginella FL, Podešvová L, Yurchenko V, Vácha R, Plevka P. J Virol 95 e01957-20 (2021)
  11. Microbial production of lipid-protein vesicles using enveloped bacteriophage phi6. Lyytinen OL, Starkova D, Poranen MM. Microb Cell Fact 18 29 (2019)
  12. Dual Role of a Viral Polymerase in Viral Genome Replication and Particle Self-Assembly. Sun X, Ilca SL, Huiskonen JT, Poranen MM. mBio 9 e01242-18 (2018)
  13. Structures of enveloped virions determined by cryogenic electron microscopy and tomography. Stass R, Ng WM, Kim YC, Huiskonen JT. Adv Virus Res 105 35-71 (2019)
  14. Component tree analysis of cystovirus φ6 nucleocapsid Cryo-EM single particle reconstructions. Oliveira LM, Ye Z, Katz A, Alimova A, Wei H, Herman GT, Gottlieb P. PLoS One 13 e0188858 (2018)
  15. The Molecular Mechanism of Domain Swapping of the C-Terminal Domain of the SARS-Coronavirus Main Protease. Terse VL, Gosavi S. Biophys J 120 504-516 (2021)
  16. Amino-acid composition after loop deletion drives domain swapping. Nandwani N, Surana P, Udgaonkar JB, Das R, Gosavi S. Protein Sci 26 1994-2002 (2017)
  17. Controlled Disassembly and Purification of Functional Viral Subassemblies Using Asymmetrical Flow Field-Flow Fractionation (AF4). Eskelin K, Poranen MM. Viruses 10 E579 (2018)
  18. Bacteriophages and their unique components provide limitless resources for exploitation. Szymanski CM. Front Microbiol 15 1342544 (2024)


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