PreprintCited by 53Bacteriophages and microbial interactionsAdvanced Electron Microscopy Techniques and ApplicationsEnzyme Structure and Function

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Cryo-electron microscopy of the f1 filamentous phage reveals a new paradigm in viral infection and assembly

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Conners, Rebecca, León-Quezada, Rayén Ignacia, McLaren, Mathew, Bennett, Nicholas J, Daum, Bertram, Rakonjac, Jasna, Gold, Vicki A M·2022·Nature Communications

Preprint — published as 10.1038/s41467-023-37915-w

Abstract

Phages are viruses that infect bacteria and dominate every ecosystem on our planet. As well as impacting microbial ecology, physiology and evolution, phages are exploited as tools in molecular biology and biotechnology. This is particularly true for the Ff (f1, fd or M13) phages, which represent a widely distributed group of filamentous viruses. Over nearly five decades, Ff has seen an extraordinary range of applications, including in phage display and nanotechnology. However, the complete structure of the phage capsid and consequently the mechanisms of infection and assembly remain largely mysterious. Using cryo-electron microscopy and a highly efficient system for production of short Ff-derived nanorods, we have determined the first structure of a filamentous virus, including the filament tips. Structure combined with mutagenesis was employed to identify domains of the phage that are important in bacterial attack and for release of new phage progeny. These data allow new models to be proposed for the phage lifecycle and will undoubtedly enable the development of novel biotechnological applications.

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Research works printed but not linked: 75

  1. 2019, Cryptic inoviruses revealed as pervasive in bacteria and archaea across Earth’s biomes, Nat Microbiol, 4, 1895, 10.1038/s41564-019-0510-x · DOI
  2. 10.1126/science.272.5270.1910 · DOI
  3. 10.1038/ismej.2008.109 · DOI
  4. 10.1073/pnas.56.1.126 · DOI
  5. 1972, Role of F pili in the penetration of bacteriophage f1, J Virol, 10, 835, 10.1128/jvi.10.4.835-843.1972 · DOI
  6. 10.1126/science.1171541 · DOI
  7. 10.1073/pnas.0800442106 · DOI
  8. Henry, K. A. , Arbabi-Ghahroudi, M. & Scott, J. K . Beyond phage display: non-traditional applications of the filamentous bacteriophage as a vaccine carrier, therapeutic biologic, and bioconjugation scaffold. Front. Microbiol. 6, (2015). · DOI
  9. 10.1002/anie.201908308 · DOI
  10. 1992, Terminating a macromolecular helix. Structural model for the minor proteins of bacteriophage M13, J. Mol. Biol, 228, 885
  11. 10.1016/0042-6822(83)90382-3 · DOI
  12. 2012, Next generation phage display by use of pVII and pIX as display scaffolds, Methods, 58, 40, 10.1016/j.ymeth.2012.07.005 · DOI
  13. 10.1016/S0022-2836(02)00260-7 · DOI
  14. 10.1006/jmbi.1999.2720 · DOI
  15. 10.1016/S0969-2126(99)80092-6 · DOI
  16. 10.1128/jb.179.20.6464-6471.1997 · DOI
  17. 10.1016/j.jmb.2005.11.069 · DOI
  18. Smilowitz, H . Bacteriophage f1 infection: fate of the parental major coat protein. J. Virol. 94–99 (1974). · DOI
  19. 2021, CryoEM structure of the outer membrane secretin channel pIV from the f1 filamentous bacteriophage, Nat Commun, 12, 6316, 10.1038/s41467-021-26610-3 · DOI · Paper page
  20. 10.1006/jmbi.1995.0393 · DOI
  21. 1989, Genetic analysis of the filamentous bacteriophage packaging signal and of the proteins that interact with it, J. Virol, 63, 3284, 10.1128/jvi.63.8.3284-3295.1989 · DOI
  22. 10.1006/jmbi.1998.2006 · DOI
  23. 10.1006/jmbi.1999.2851 · DOI
  24. 10.1016/0141-8130(90)90064-H · DOI
  25. 10.1016/S0022-2836(05)80032-4 · DOI
  26. 10.1016/j.jmb.2005.10.048 · DOI
  27. 10.1016/j.pbiomolbio.2014.02.003 · DOI
  28. 10.1016/j.jmb.2006.06.027 · DOI
  29. Mills, D. J . Setting up and operating a cryo-EM laboratory. Q. Rev. Biophys. 54, e2 (2021). · DOI
  30. 10.1073/pnas.1811929116 · DOI
  31. 10.1038/nsb0298-140 · DOI
  32. Sattar, S. , Bennett, N. J. , Wen, W. X. , Guthrie, J. M. , Blackwell, L. F. , Conway, J. F. & Rakonjac, J . Ff-nano, short functionalized nanorods derived from Ff (f1, fd, or M13) filamentous bacteriophage. Front. Microbiol. 6, 316 (2015). · DOI
  33. 2019, Real-time cryo-electron microscopy data preprocessing with Warp, Nat. Methods, 16, 1146, 10.1038/s41592-019-0580-y · DOI
  34. 10.1038/nmeth.4169 · DOI · Paper page
  35. 1982, Nucleotide sequence of bacteriophage f1 DNA, J. Virol, 44, 32, 10.1128/jvi.44.1.32-46.1982 · DOI
  36. Mäntynen, S. , Sundberg, L. R. , Oksanen, H. M. & Poranen, M. M . Half a century of research on membrane- containing bacteriophages: bringing new concepts to modern virology. Viruses 11, (2019). · DOI
  37. 10.1016/0022-2836(81)90050-4 · DOI
  38. 10.1016/0022-2836(85)90329-8 · DOI
  39. 2011, Characterization of a dual-function domain that mediates membrane insertion and excision of Ff filamentous bacteriophage, J. Mol. Biol, 411, 972, 10.1016/j.jmb.2011.07.002 · DOI
  40. Nugent, T. & Jones, D. T . Transmembrane protein topology prediction using support vector machines. BMC Bioinformatics 10, 159 (2009). · DOI
  41. 10.1016/S0092-8674(00)80342-6 · DOI
  42. 10.1038/nsmb946 · DOI
  43. 10.1016/j.jmb.2007.07.060 · DOI
  44. 2022, Cryo-EM structure of a type IV secretion system, Nature, 607, 191, 10.1038/s41586-022-04859-y · DOI
  45. 10.1073/pnas.1904428116 · DOI
  46. 10.1038/s41467-020-20241-w · DOI · Paper page
  47. 10.1128/jb.170.11.5312-5316.1988 · DOI
  48. 10.1006/jmbi.1997.0981 · DOI
  49. 1989, Pore-forming properties of the adsorption protein of filamentous phage fd, Biochim. Biophys. Acta - Biomembr, 985, 239, 10.1016/0005-2736(89)90408-2 · DOI
  50. 10.1016/j.neuron.2016.03.032 · DOI
  51. 10.1186/s12915-016-0335-5 · DOI
  52. 10.1073/pnas.94.8.4068 · DOI
  53. 1995, Electrostatic potential distribution of the gene V protein from Ff phage facilitates cooperative DNA binding: a model of the GVP-ssDNA complex, Protein Sci, 4, 187, 10.1002/pro.5560040206 · DOI
  54. Haase, M. , Tessmer, L. , Köhnlechner, L. & Kuhn, A . The M13 phage assembly machine has a membrane- spanning oligomeric ring structure. Viruses 14, (2022). · DOI
  55. 10.1016/0022-2836(88)90363-4 · DOI
  56. 10.1111/mmi.14187 · DOI
  57. 10.1016/S0022-2836(03)00950-1 · DOI
  58. 1994, The adsorption protein of filamentous phage fd: assignment of its disulfide bridges and identification of the domain incorporated in the coat, Biochemistry, 33, 13954, 10.1021/bi00250a051 · DOI
  59. 10.1038/nchembio.1453 · DOI
  60. 10.1016/S0014-5793(00)01946-3 · DOI
  61. 2011, Filamentous bacteriophage: biology, phage display and nanotechnology applications, Curr. Issues Mol. Biol, 13, 51
  62. Sambrook, J .& Russell, D. W . Molecular Cloning: A Laboratory Manual, 4th edition. (2012).
  63. 10.1038/nmeth.2089 · DOI · Paper page
  64. 10.1002/jcc.20084 · DOI
  65. 10.1107/S0907444910007493 · DOI · Paper page
  66. 2011, REFMAC5 for the refinement of macromolecular crystal structures, Acta Crystallogr. D. Struct. Biol, 67, 355, 10.1107/S0907444911001314 · DOI
  67. 10.1107/S1399004714018070 · DOI
  68. 10.1002/pro.3330 · DOI · Paper page
  69. Berman, H. , Henrick, K. & Nakamura, H . Announcing the worldwide Protein Data Bank. Nat. Struct. Biol. 10, 980 (2003). · DOI · Paper page
  70. 10.1038/s42003-021-01907-7 · DOI
  71. 10.1016/0022-2836(92)90858-H · DOI
  72. Cha, T-G. , Tsedev, U. , Ransil, A. , Embree, A. , Gordon, D. B. , Belcher, A. M. , Voigt, C. A. , Cha, T.-G. , Gordon, D. B. , Voigt, A. , Tsedev, U. , Belcher, A. M. , Ransil, A. & Embree, A . Genetic control of aerogel and nanofoam properties, applied to Ni–MnOx cathode design. Adv. Funct. Mater. 31, 2010867 (2021). · DOI
  73. 10.1006/jmbi.2000.4042 · DOI
  74. 10.1016/S0378-1119(97)00298-9 · DOI
  75. 10.1016/j.cell.2016.08.025 · DOI

Metadata

Authors
Conners, R., León-Quezada, R. I., McLaren, M., Bennett, N. J., Daum, B., Rakonjac, J., & Gold, V. A. M.
Affiliations
  • University of Exeter (GB)
  • Massey University (NZ)
Corresponding author
  • Rakonjac, Jasna
  • Gold, Vicki A M
Venue
Nature Communications
Publisher
openRxiv
Published
2022-11-04
Volume
14
Issue
1
Pages
2724-2724
ISSN
2041-1723 (ISSN-L)
OpenAlex
W4376225524
Cited by
53
References
1
Citations by year
2026: 9 · 2025: 17 · 2024: 20 · 2023: 7
FWCI
8.57
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • Nature Communications (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nd)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • RePEc: Research Papers in Economics (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • University of Missouri
  • Callaghan Innovation
  • Wellcome Trust (206181/Z/17/Z, 206181, Z/17/Z, 210363/Z/18/Z, 202904, 210363, 202904/Z/16/Z)
  • Diamond Light Source
  • University of Exeter
  • European Commission (HORIZON2020, 803894)
  • Massey University
  • Medical Research Council
  • Biotechnology and Biological Sciences Research Council (BB/R000484/1, BB/R008639/1)
Topics
  • Life Sciences › Immunology and Microbiology › Virology › Bacteriophages and microbial interactions
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Structural Biology › Advanced Electron Microscopy Techniques and Applications
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Structural Biology › Enzyme Structure and Function
Keywords
phage assembly, phage infection mechanism, nanorods, bacteriophages
MeSH terms
Bacteria, Bacteriophages, Humans, Virus Diseases, Ecosystem, Inovirus, Cryoelectron Microscopy

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