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Annual Review of Microbiology

Volume 78, 2024

Viral Genome Delivery Across Bacterial Cell Surfaces

Abstract

In 1952, Hershey and Chase used bacteriophage T2 genome delivery inside to demonstrate that DNA, not protein, is the genetic material. Over 70 years later, our understanding of bacteriophage structure has grown dramatically, mainly thanks to the cryogenic electron microscopy revolution. In stark contrast, phage genome delivery in prokaryotes remains poorly understood, mainly due to the inherent challenge of studying such a transient and complex process. Here, we review the current literature on viral genome delivery across bacterial cell surfaces. We focus on icosahedral bacterial viruses that we arbitrarily sort into three groups based on the presence and size of a tail apparatus. We inventory the building blocks implicated in genome delivery and critically analyze putative mechanisms of genome ejection. Bacteriophage genome delivery into bacteria is a topic of growing interest, given the renaissance of phage therapy in Western medicine as a therapeutic alternative to face the antibiotic resistance crisis.

Keyword(s): bacteriophage, DNA ejectosome, ejection proteins, genome ejection, phage therapy, tail apparatus
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/content/journals/10.1146/annurev-micro-041222-124727
2024-11-20
2025-04-28
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Literature Cited

  1. 1.
    Ackermann HW. 2006.. Classification of bacteriophages. . In The Bacteriophages, ed. R Calendar , pp. 8–16. New York:: Oxford Univ. Press. , 2nd ed..
     [Google Scholar]
  2. 2.
    Al-Shayeb B, Sachdeva R, Chen LX, Ward F, Munk P, et al. 2020.. Clades of huge phages from across Earth's ecosystems. . Nature 578::425–31
     [Crossref] [Google Scholar]
  3. 3.
    Andres D, Hanke C, Baxa U, Seul A, Barbirz S, Seckler R. 2010.. Tailspike interactions with lipopolysaccharide effect DNA ejection from phage P22 particles in vitro. . J. Biol. Chem. 285::36768–75
     [Crossref] [Google Scholar]
  4. 4.
    Benn G, Mikheyeva IV, Inns PG, Forster JC, Ojkic N, et al. 2021.. Phase separation in the outer membrane of Escherichia coli. . PNAS 118:(44):e2112237118
     [Crossref] [Google Scholar]
  5. 5.
    Bernal RA, Hafenstein S, Olson NH, Bowman VD, Chipman PR, et al. 2003.. Structural studies of bacteriophage α3 assembly. . J. Mol. Biol. 325::11–24
     [Crossref] [Google Scholar]
  6. 6.
    Bertozzi Silva J, Storms Z, Sauvageau D. 2016.. Host receptors for bacteriophage adsorption. . FEMS Microbiol. Lett. 363::fnw002
     [Crossref] [Google Scholar]
  7. 7.
    Bhardwaj A, Molineux IJ, Casjens SR, Cingolani G. 2011.. Atomic structure of bacteriophage Sf6 tail needle knob. . J. Biol. Chem. 286::30867–77
     [Crossref] [Google Scholar]
  8. 8.
    Bohm J, Lambert O, Frangakis AS, Letellier L, Baumeister W, Rigaud JL. 2001.. FhuA-mediated phage genome transfer into liposomes: a cryo-electron tomography study. . Curr. Biol. 11::1168–75
     [Crossref] [Google Scholar]
  9. 9.
    Carter RH, Demidenko AA, Hattingh-Willis S, Rothman-Denes LB. 2003.. Phage N4 RNA polymerase II recruitment to DNA by a single-stranded DNA-binding protein. . Genes Dev. 17::2334–45
     [Crossref] [Google Scholar]
  10. 10.
    Cater K, Dandu VS, Bari SM, Lackey K, Everett GF, Hatoum-Aslan A. 2017.. A novel Staphylococcus podophage encodes a unique lysin with unusual modular design. . mSphere 2::e00040-17
     [Crossref] [Google Scholar]
  11. 11.
    Cerritelli ME, Wall JS, Simon MN, Conway JF, Steven AC. 1996.. Stoichiometry and domainal organization of the long tail-fiber of bacteriophage T4: a hinged viral adhesin. . J. Mol. Biol. 260::767–80
     [Crossref] [Google Scholar]
  12. 12.
    Ceyssens PJ, Minakhin L, Van den Bossche A, Yakunina M, Klimuk E, et al. 2014.. Development of giant bacteriophage ΦKZ is independent of the host transcription apparatus. . J. Virol. 88::10501–10
     [Crossref] [Google Scholar]
  13. 13.
    Chaikeeratisak V, Nguyen K, Egan ME, Erb ML, Vavilina A, Pogliano J. 2017.. The phage nucleus and tubulin spindle are conserved among large Pseudomonas phages. . Cell Rep. 20::1563–71
     [Crossref] [Google Scholar]
  14. 14.
    Chang CY, Kemp P, Molineux IJ. 2010.. Gp15 and gp16 cooperate in translocating bacteriophage T7 DNA into the infected cell. . Virology 398::176–86
     [Crossref] [Google Scholar]
  15. 15.
    Chang JT, Schmid MF, Haase-Pettingell C, Weigele PR, King JA, Chiu W. 2010.. Visualizing the structural changes of bacteriophage epsilon15 and its Salmonella host during infection. . J. Mol. Biol. 402::731–40
     [Crossref] [Google Scholar]
  16. 16.
    Chang JY, Gorzelnik KV, Thongchol J, Zhang J. 2022.. Structural assembly of Qβ virion and its diverse forms of virus-like particles. . Viruses 14::225
     [Crossref] [Google Scholar]
  17. 17.
    Chen W, Xiao H, Wang L, Wang X, Tan Z, et al. 2021.. Structural changes in bacteriophage T7 upon receptor-induced genome ejection. . PNAS 118::e2102003118
     [Crossref] [Google Scholar]
  18. 18.
    Choi KH, McPartland J, Kaganman I, Bowman VD, Rothman-Denes LB, Rossmann MG. 2008.. Insight into DNA and protein transport in double-stranded DNA viruses: the structure of bacteriophage N4. . J. Mol. Biol. 378::726–36
     [Crossref] [Google Scholar]
  19. 19.
    Cuervo A, Fabrega-Ferrer M, Machon C, Conesa JJ, Fernandez FJ, et al. 2019.. Structures of T7 bacteriophage portal and tail suggest a viral DNA retention and ejection mechanism. . Nat. Commun. 10::3746
     [Crossref] [Google Scholar]
  20. 20.
    Cui Z, Gorzelnik KV, Chang JY, Langlais C, Jakana J, et al. 2017.. Structures of Qβ virions, virus-like particles, and the Qβ–MurA complex reveal internal coat proteins and the mechanism of host lysis. . PNAS 114::11697–702
     [Crossref] [Google Scholar]
  21. 21.
    Cumby N, Reimer K, Mengin-Lecreulx D, Davidson AR, Maxwell KL. 2015.. The phage tail tape measure protein, an inner membrane protein and a periplasmic chaperone play connected roles in the genome injection process of E. coli phage HK97. . Mol. Microbiol. 96::437–47
     [Crossref] [Google Scholar]
  22. 22.
    Dai W, Fu C, Raytcheva D, Flanagan J, Khant HA, et al. 2013.. Visualizing virus assembly intermediates inside marine cyanobacteria. . Nature 502::707–10
     [Crossref] [Google Scholar]
  23. 23.
    Dai X, Li Z, Lai M, Shu S, Du Y, et al. 2017.. In situ structures of the genome and genome-delivery apparatus in a single-stranded RNA virus. . Nature 541::112–16
     [Crossref] [Google Scholar]
  24. 24.
    Dawes J. 1975.. Characterisation of the bacteriophage T4 receptor site. . Nature 256::127–28
     [Crossref] [Google Scholar]
  25. 25.
    Doore SM, Fane BA. 2016.. The Microviridae: diversity, assembly, and experimental evolution. . Virology 491::45–55
     [Crossref] [Google Scholar]
  26. 26.
    Evilevitch A. 2018.. The mobility of packaged phage genome controls ejection dynamics. . eLife 7::e37345
     [Crossref] [Google Scholar]
  27. 27.
    Evilevitch A, Lavelle L, Knobler CM, Raspaud E, Gelbart WM. 2003.. Osmotic pressure inhibition of DNA ejection from phage. . PNAS 100::9292–95
     [Crossref] [Google Scholar]
  28. 28.
    Evseev P, Shneider M, Miroshnikov K. 2022.. Evolution of phage tail sheath protein. . Viruses 14::1148
     [Crossref] [Google Scholar]
  29. 29.
    Falco SC, Laan KV, Rothman-Denes LB. 1977.. Virion-associated RNA polymerase required for bacteriophage N4 development. . PNAS 74::520–23
     [Crossref] [Google Scholar]
  30. 30.
    Falco SC, Rothman-Denes LB. 1979.. Bacteriophage N4-induced transcribing activities in Escherichia coli. II. Association of the N4 transcriptional apparatus with the cytoplasmic membrane. . Virology 95::466–75
     [Crossref] [Google Scholar]
  31. 31.
    Fokine A, Battisti AJ, Bowman VD, Efimov AV, Kurochkina LP, et al. 2007.. Cryo-EM study of the Pseudomonas bacteriophage ΦKZ. . Structure 15::1099–104
     [Crossref] [Google Scholar]
  32. 32.
    Fraser A, Prokhorov NS, Jiao F, Pettitt BM, Scheuring S, Leiman PG. 2021.. Quantitative description of a contractile macromolecular machine. . Sci. Adv. 7:(24):eabf9601
     [Crossref] [Google Scholar]
  33. 33.
    Ge P, Scholl D, Prokhorov NS, Avaylon J, Shneider MM, et al. 2020.. Action of a minimal contractile bactericidal nanomachine. . Nature 580::658–62
     [Crossref] [Google Scholar]
  34. 34.
    Gehring K, Charbit A, Brissaud E, Hofnung M. 1987.. Bacteriophage λ receptor site on the Escherichia coli K-12 LamB protein. . J. Bacteriol. 169::2103–6
     [Crossref] [Google Scholar]
  35. 35.
    Gidden J, Denson J, Liyanage R, Ivey DM, Lay JO. 2009.. Lipid compositions in Escherichia coli and Bacillus subtilis during growth as determined by MALDI-TOF and TOF/TOF mass spectrometry. . Int. J. Mass Spectrom. 283::178–84
     [Crossref] [Google Scholar]
  36. 36.
    Golmohammadi R, Fridborg K, Bundule M, Valegard K, Liljas L. 1996.. The crystal structure of bacteriophage Qβ at 3.5 Å resolution. . Structure 4::543–54
     [Crossref] [Google Scholar]
  37. 37.
    Gonzalez-Garcia VA, Pulido-Cid M, Garcia-Doval C, Bocanegra R, van Raaij MJ, et al. 2015.. Conformational changes leading to T7 DNA delivery upon interaction with the bacterial receptor. . J. Biol. Chem. 290::10038–44
     [Crossref] [Google Scholar]
  38. 38.
    González-Huici V, Salas M, Hermoso JM. 2004.. The push-pull mechanism of bacteriophage O29 DNA injection. . Mol. Microbiol. 52::529–40
     [Crossref] [Google Scholar]
  39. 39.
    Goulet A, Spinelli S, Mahony J, Cambillau C. 2020.. Conserved and diverse traits of adhesion devices from Siphoviridae recognizing proteinaceous or saccharidic receptors. . Viruses 12::512
     [Crossref] [Google Scholar]
  40. 40.
    Grayson P, Han L, Winther T, Phillips R. 2007.. Real-time observations of single bacteriophage λ DNA ejections in vitro. . PNAS 104::14652–57
     [Crossref] [Google Scholar]
  41. 41.
    Guerrero-Ferreira RC, Hupfeld M, Nazarov S, Taylor NM, Shneider MM, et al. 2019.. Structure and transformation of bacteriophage A511 baseplate and tail upon infection of Listeria cells. . EMBO J. 38::e99455
     [Crossref] [Google Scholar]
  42. 42.
    Guerrero-Ferreira RC, Wright ER. 2013.. Cryo-electron tomography of bacterial viruses. . Virology 435::179–86
     [Crossref] [Google Scholar]
  43. 43.
    Hardy JM, Dunstan RA, Lithgow T, Coulibaly F. 2022.. Tall tails: cryo-electron microscopy of phage tail DNA ejection conduits. . Biochem. Soc. Trans. 50::459–71
     [Crossref] [Google Scholar]
  44. 44.
    Hawkins NC, Kizziah JL, Hatoum-Aslan A, Dokland T. 2022.. Structure and host specificity of Staphylococcus epidermidis bacteriophage Andhra. . Sci. Adv. 8::eade0459
     [Crossref] [Google Scholar]
  45. 45.
    Hershey AD, Chase M. 1952.. Independent functions of viral protein and nucleic acid in growth of bacteriophage. . J. Gen. Physiol. 36::39–56
     [Crossref] [Google Scholar]
  46. 46.
    Hrebik D, Stverakova D, Skubnik K, Fuzik T, Pantucek R, Plevka P. 2019.. Structure and genome ejection mechanism of Staphylococcus aureus phage P68. . Sci. Adv. 5::eaaw7414
     [Crossref] [Google Scholar]
  47. 47.
    Hu B, Margolin W, Molineux IJ, Liu J. 2013.. The bacteriophage T7 virion undergoes extensive structural remodeling during infection. . Science 339::576–79
     [Crossref] [Google Scholar]
  48. 48.
    Hu B, Margolin W, Molineux IJ, Liu J. 2015.. Structural remodeling of bacteriophage T4 and host membranes during infection initiation. . PNAS 112::E4919–28
     [Google Scholar]
  49. 49.
    Huang Y, Sun H, Wei S, Cai L, Liu L, et al. 2023.. Structure and proposed DNA delivery mechanism of a marine roseophage. . Nat. Commun. 14::3609
     [Crossref] [Google Scholar]
  50. 50.
    Iglesias SM, Lokareddy RK, Yang R, Li F, Yeggoni DP, et al. 2023.. Molecular architecture of Salmonella typhimurium virus P22 genome ejection machinery. . J. Mol. Biol. 435::168365
     [Crossref] [Google Scholar]
  51. 51.
    Inagaki M, Kawaura T, Wakashima H, Kato M, Nishikawa S, Kashimura N. 2003.. Different contributions of the outer and inner R-core residues of lipopolysaccharide to the recognition by spike H and G proteins of bacteriophage ΦX174. . FEMS Microbiol. Lett. 226::221–27
     [Crossref] [Google Scholar]
  52. 52.
    Inagaki M, Wakashima H, Kato M, Kaitani K, Nishikawa S. 2005.. Crucial role of the lipid part of lipopolysaccharide for conformational change of minor spike H protein of bacteriophage ΦiX174. . FEMS Microbiol. Lett. 251::305–11
     [Crossref] [Google Scholar]
  53. 53.
    Israel V. 1977.. E proteins of bacteriophage P22. I. Identification and ejection from wild-type and defective particles. . J. Virol. 23::91–97
     [Crossref] [Google Scholar]
  54. 54.
    Jeembaeva M, Castelnovo M, Larsson F, Evilevitch A. 2008.. Osmotic pressure: resisting or promoting DNA ejection from phage?. J. Mol. Biol. 381::310–23
     [Crossref] [Google Scholar]
  55. 55.
    Jeembaeva M, Jonsson B, Castelnovo M, Evilevitch A. 2010.. DNA heats up: energetics of genome ejection from phage revealed by isothermal titration calorimetry. . J. Mol. Biol. 395::1079–87
     [Crossref] [Google Scholar]
  56. 56.
    Jin Y, Sdao SM, Dover JA, Porcek NB, Knobler CM, et al. 2015.. Bacteriophage P22 ejects all of its internal proteins before its genome. . Virology 485::128–34
     [Crossref] [Google Scholar]
  57. 57.
    Juhala RJ, Ford ME, Duda RL, Youlton A, Hatfull GF, Hendrix RW. 2000.. Genomic sequences of bacteriophages HK97 and HK022: pervasive genetic mosaicism in the lambdoid bacteriophages. . J. Mol. Biol. 299::27–51
     [Crossref] [Google Scholar]
  58. 58.
    Junkermeier EH, Hengge R. 2021.. A novel locally c-di-GMP-controlled exopolysaccharide synthase required for bacteriophage N4 infection of Escherichia coli. . mBio 12::e0324921
     [Crossref] [Google Scholar]
  59. 59.
    Kazmierczak KM, Davydova EK, Mustaev AA, Rothman-Denes LB. 2002.. The phage N4 virion RNA polymerase catalytic domain is related to single-subunit RNA polymerases. . EMBO J. 21::5815–23
     [Crossref] [Google Scholar]
  60. 60.
    Kemp P, Gupta M, Molineux IJ. 2004.. Bacteriophage T7 DNA ejection into cells is initiated by an enzyme-like mechanism. . Mol. Microbiol. 53::1251–65
     [Crossref] [Google Scholar]
  61. 61.
    Kiino DR, Rothman-Denes LB. 1989.. Genetic analysis of bacteriophage N4 adsorption. . J. Bacteriol. 171::4595–602
     [Crossref] [Google Scholar]
  62. 62.
    Kindt J, Tzlil S, Ben-Shaul A, Gelbart WM. 2001.. DNA packaging and ejection forces in bacteriophage. . PNAS 98::13671–74
     [Crossref] [Google Scholar]
  63. 63.
    Koning RI, Gomez-Blanco J, Akopjana I, Vargas J, Kazaks A, et al. 2016.. Asymmetric cryo-EM reconstruction of phage MS2 reveals genome structure in situ. . Nat. Commun. 7::12524
     [Crossref] [Google Scholar]
  64. 64.
    Krahn PM, O'Callaghan RJ, Paranchych W. 1972.. Stages in phage R17 infection. VI. Injection of A protein and RNA into the host cell. . Virology 47::628–37
     [Crossref] [Google Scholar]
  65. 65.
    Krylov VN, Smirnova TA, Minenkova IB, Plotnikova TG, Zhazikov IZ, Khrenova EA. 1984.. Pseudomonas bacteriophage ΦKZ contains an inner body in its capsid. . Can. J. Microbiol. 30::758–62
     [Crossref] [Google Scholar]
  66. 66.
    Laughlin TG, Deep A, Prichard AM, Seitz C, Gu Y, et al. 2022.. Architecture and self-assembly of the jumbo bacteriophage nuclear shell. . Nature 608::429–35
     [Crossref] [Google Scholar]
  67. 67.
    Leavitt JC, Gilcrease EB, Woodbury BM, Teschke CM, Casjens SR. 2021.. Intravirion DNA can access the space occupied by the bacteriophage P22 ejection proteins. . Viruses 13::1504
     [Crossref] [Google Scholar]
  68. 68.
    Leavitt JC, Gogokhia L, Gilcrease EB, Bhardwaj A, Cingolani G, Casjens SR. 2013.. The tip of the tail needle affects the rate of DNA delivery by bacteriophage p22. . PLOS ONE 8::e70936
     [Crossref] [Google Scholar]
  69. 69.
    Lee H, Baxter AJ, Bator CM, Fane BA, Hafenstein SL. 2022.. Cryo-EM structure of gokushovirus ΦEC6098 reveals a novel capsid architecture for a single-scaffolding protein, microvirus assembly system. . J. Virol. 96::e0099022
     [Crossref] [Google Scholar]
  70. 70.
    Leforestier A, Brasiles S, de Frutos M, Raspaud E, Letellier L, et al. 2008.. Bacteriophage T5 DNA ejection under pressure. . J. Mol. Biol. 384::730–39
     [Crossref] [Google Scholar]
  71. 71.
    Lenneman BR, Rothman-Denes LB. 2015.. Structural and biochemical investigation of bacteriophage N4-encoded RNA polymerases. . Biomolecules 5::647–67
     [Crossref] [Google Scholar]
  72. 72.
    Li D, Liu T, Zuo X, Li T, Qiu X, Evilevitch A. 2015.. Ionic switch controls the DNA state in phage λ. . Nucleic Acids Res. 43::6348–58
     [Crossref] [Google Scholar]
  73. 73.
    Li F, Hou CD, Lokareddy RK, Yang R, Forti F, et al. 2023.. High-resolution cryo-EM structure of the Pseudomonas bacteriophage E217. . Nat. Commun. 14::4052
     [Crossref] [Google Scholar]
  74. 74.
    Li F, Hou CD, Yang R, Whitehead R 3rd, Teschke CM, Cingolani G. 2022.. High-resolution cryo-EM structure of the Shigella virus Sf6 genome delivery tail machine. . Sci. Adv. 8::eadc9641
     [Crossref] [Google Scholar]
  75. 75.
    Lithgow T, Stubenrauch CJ, Stumpf MPH. 2023.. Surveying membrane landscapes: a new look at the bacterial cell surface. . Nat. Rev. Microbiol. 21::502–18
     [Crossref] [Google Scholar]
  76. 76.
    Liu X, Zhang Q, Murata K, Baker ML, Sullivan MB, et al. 2010.. Structural changes in a marine podovirus associated with release of its genome into Prochlorococcus. . Nat. Struct. Mol. Biol. 17::830–36
     [Crossref] [Google Scholar]
  77. 77.
    Lof D, Schillen K, Jonsson B, Evilevitch A. 2007.. Forces controlling the rate of DNA ejection from phage λ. . J. Mol. Biol. 368::55–65
     [Crossref] [Google Scholar]
  78. 78.
    Lupo D, Leptihn S, Nagler G, Haase M, Molineux IJ, Kuhn A. 2016.. The T7 ejection nanomachine components gp15–gp16 form a spiral ring complex that binds DNA and a lipid membrane. . Virology 486::263–71
     [Crossref] [Google Scholar]
  79. 79.
    McKenna R, Xia D, Willingmann P, Ilag LL, Krishnaswamy S, et al. 1992.. Atomic structure of single-stranded DNA bacteriophage ΦX174 and its functional implications. . Nature 355::137–43
     [Crossref] [Google Scholar]
  80. 80.
    McPartland J, Rothman-Denes LB. 2009.. The tail sheath of bacteriophage N4 interacts with the Escherichia coli receptor. . J. Bacteriol. 191::525–32
     [Crossref] [Google Scholar]
  81. 81.
    Megrian D, Taib N, Witwinowski J, Beloin C, Gribaldo S. 2020.. One or two membranes? Diderm Firmicutes challenge the Gram-positive/Gram-negative divide. . Mol. Microbiol. 113::659–71
     [Crossref] [Google Scholar]
  82. 82.
    Mendoza SD, Nieweglowska ES, Govindarajan S, Leon LM, Berry JD, et al. 2020.. A bacteriophage nucleus-like compartment shields DNA from CRISPR nucleases. . Nature 577::244–48
     [Crossref] [Google Scholar]
  83. 83.
    Meng R, Jiang M, Cui Z, Chang JY, Yang K, et al. 2019.. Structural basis for the adsorption of a single-stranded RNA bacteriophage. . Nat. Commun. 10::3130
     [Crossref] [Google Scholar]
  84. 84.
    Menon ND, Kumar MS, Satheesh Babu TG, Bose S, Vijayakumar G, et al. 2021.. A novel N4-like bacteriophage isolated from a wastewater source in South India with activity against several multidrug-resistant clinical Pseudomonas aeruginosa isolates. . mSphere 6::e01215-20
     [Crossref] [Google Scholar]
  85. 85.
    Molineux IJ. 2001.. No syringes please, ejection of phage T7 DNA from the virion is enzyme driven. . Mol. Microbiol. 40::1–8
     [Crossref] [Google Scholar]
  86. 86.
    Molineux IJ, Panja D. 2013.. Popping the cork: mechanisms of phage genome ejection. . Nat. Rev. Microbiol. 11::194–204
     [Crossref] [Google Scholar]
  87. 87.
    Murakami KS, Davydova EK, Rothman-Denes LB. 2008.. X-ray crystal structure of the polymerase domain of the bacteriophage N4 virion RNA polymerase. . PNAS 105::5046–51
     [Crossref] [Google Scholar]
  88. 88.
    Nchinda GW, Al-Atoom N, Coats MT, Cameron JM, Waffo AB. 2021.. Uniqueness of RNA coliphage Qβ display system in directed evolutionary biotechnology. . Viruses 13::568
     [Crossref] [Google Scholar]
  89. 89.
    Nieweglowska ES, Brilot AF, Mendez-Moran M, Kokontis C, Baek M, et al. 2023.. The ΦPA3 phage nucleus is enclosed by a self-assembling 2D crystalline lattice. . Nat. Commun. 14::927
     [Crossref] [Google Scholar]
  90. 90.
    Nobrega FL, Vlot M, de Jonge PA, Dreesens LL, Beaumont HJE, et al. 2018.. Targeting mechanisms of tailed bacteriophages. . Nat. Rev. Microbiol. 16::760–73
     [Crossref] [Google Scholar]
  91. 91.
    North OI, Sakai K, Yamashita E, Nakagawa A, Iwazaki T, et al. 2019.. Phage tail fibre assembly proteins employ a modular structure to drive the correct folding of diverse fibres. . Nat. Microbiol. 4::1645–53
     [Crossref] [Google Scholar]
  92. 92.
    Novacek J, Siborova M, Benesik M, Pantucek R, Doskar J, Plevka P. 2016.. Structure and genome release of Twort-like Myoviridae phage with a double-layered baseplate. . PNAS 113::9351–56
     [Crossref] [Google Scholar]
  93. 93.
    Panja D, Molineux IJ. 2010.. Dynamics of bacteriophage genome ejection in vitro and in vivo. . Phys. Biol. 7::045006
     [Crossref] [Google Scholar]
  94. 94.
    Paranchych W, Ainsworth SK, Dick AJ, Krahn PM. 1971.. Stages in phage R17 infection. V. Phage eclipse and the role of F pili. . Virology 45::615–28
     [Crossref] [Google Scholar]
  95. 95.
    Parent KN, Erb ML, Cardone G, Nguyen K, Gilcrease EB, et al. 2014.. OmpA and OmpC are critical host factors for bacteriophage Sf6 entry in Shigella. . Mol. Microbiol. 92::47–60
     [Crossref] [Google Scholar]
  96. 96.
    Parent KN, Schrad JR, Cingolani G. 2018.. Breaking symmetry in viral icosahedral capsids as seen through the lenses of X-ray crystallography and cryo-electron microscopy. . Viruses 10::67
     [Crossref] [Google Scholar]
  97. 97.
    Perez GL, Huynh B, Slater M, Maloy S. 2009.. Transport of phage P22 DNA across the cytoplasmic membrane. . J. Bacteriol. 191::135–40
     [Crossref] [Google Scholar]
  98. 98.
    Perez-Ruiz M, Pulido-Cid M, Luque-Ortega JR, Valpuesta JM, Cuervo A, Carrascosa JL. 2021.. Assisted assembly of bacteriophage T7 core components for genome translocation across the bacterial envelope. . PNAS 118::e2026719118
     [Crossref] [Google Scholar]
  99. 99.
    Petrov AS, Douglas SS, Harvey SC. 2013.. Effects of pulling forces, osmotic pressure, condensing agents and viscosity on the thermodynamics and kinetics of DNA ejection from bacteriophages to bacterial cells: a computational study. . J. Phys. Condens. Matter 25::115101
     [Crossref] [Google Scholar]
  100. 100.
    Piuri M, Hatfull GF. 2006.. A peptidoglycan hydrolase motif within the mycobacteriophage TM4 tape measure protein promotes efficient infection of stationary phase cells. . Mol. Microbiol. 62::1569–85
     [Crossref] [Google Scholar]
  101. 101.
    Plisson C, White HE, Auzat I, Zafarani A, Sao-Jose C, et al. 2007.. Structure of bacteriophage SPP1 tail reveals trigger for DNA ejection. . EMBO J. 26::3720–28
     [Crossref] [Google Scholar]
  102. 102.
    Prokhorov NS, Riccio C, Zdorovenko EL, Shneider MM, Browning C, et al. 2017.. Function of bacteriophage G7C esterase tailspike in host cell adsorption. . Mol. Microbiol. 105::385–98
     [Crossref] [Google Scholar]
  103. 103.
    Raetz CR, Reynolds CM, Trent MS, Bishop RE. 2007.. Lipid A modification systems in gram-negative bacteria. . Annu. Rev. Biochem. 76::295–329
     [Crossref] [Google Scholar]
  104. 104.
    Rakhuba DV, Kolomiets EI, Dey ES, Novik GI. 2010.. Bacteriophage receptors, mechanisms of phage adsorption and penetration into host cell. . Pol. J. Microbiol. 59::145–55
     [Crossref] [Google Scholar]
  105. 105.
    Rodriguez-Rubio L, Martinez B, Donovan DM, Rodriguez A, Garcia P. 2013.. Bacteriophage virion-associated peptidoglycan hydrolases: potential new enzybiotics. . Crit. Rev. Microbiol. 39::427–34
     [Crossref] [Google Scholar]
  106. 106.
    Roessner CA, Ihler GM. 1984.. Proteinase sensitivity of bacteriophage lambda tail proteins gpJ and pH in complexes with the lambda receptor. . J. Bacteriol. 157::165–70
     [Crossref] [Google Scholar]
  107. 107.
    Roessner CA, Ihler GM. 1986.. Formation of transmembrane channels in liposomes during injection of λ DNA. . J. Biol. Chem. 261::386–90
     [Crossref] [Google Scholar]
  108. 108.
    Sao-Jose C, de Frutos M, Raspaud E, Santos MA, Tavares P. 2007.. Pressure built by DNA packing inside virions: enough to drive DNA ejection in vitro, largely insufficient for delivery into the bacterial cytoplasm. . J. Mol. Biol. 374::346–55
     [Crossref] [Google Scholar]
  109. 109.
    Sciara G, Bebeacua C, Bron P, Tremblay D, Ortiz-Lombardia M, et al. 2010.. Structure of lactococcal phage p2 baseplate and its mechanism of activation. . PNAS 107::6852–57
     [Crossref] [Google Scholar]
  110. 110.
    Serwer P, Wright ET, Hakala KW, Weintraub ST. 2008.. Evidence for bacteriophage T7 tail extension during DNA injection. . BMC Res. Notes 1::36
     [Crossref] [Google Scholar]
  111. 111.
    Silhavy TJ, Kahne D, Walker S. 2010.. The bacterial cell envelope. . Cold Spring Harb. Perspect. Biol. 2::a000414
     [Crossref] [Google Scholar]
  112. 112.
    Smith DE, Tans SJ, Smith SB, Grimes S, Anderson DL, Bustamante C. 2001.. The bacteriophage straight Φ29 portal motor can package DNA against a large internal force. . Nature 413::748–52
     [Crossref] [Google Scholar]
  113. 113.
    Sokolova OS, Shaburova OV, Pechnikova EV, Shaytan AK, Krylov SV, et al. 2014.. Genome packaging in EL and Lin68, two giant phiKZ-like bacteriophages of P. aeruginosa. . Virology 468–470::472–78
     [Crossref] [Google Scholar]
  114. 114.
    Sonani RR, Esteves NC, Horton AA, Kelly RJ, Sebastian AL, et al. 2023.. Neck and capsid architecture of the robust Agrobacterium phage Milano. . Commun. Biol. 6::921
     [Crossref] [Google Scholar]
  115. 115.
    Spinelli S, Bebeacua C, Orlov I, Tremblay D, Klaholz BP, et al. 2014.. Cryo-electron microscopy structure of lactococcal siphophage 1358 virion. . J. Virol. 88::8900–10
     [Crossref] [Google Scholar]
  116. 116.
    Spinelli S, Veesler D, Bebeacua C, Cambillau C. 2014.. Structures and host-adhesion mechanisms of lactococcal siphophages. . Front. Microbiol. 5::3
     [Crossref] [Google Scholar]
  117. 117.
    Struthers-Schlinke JS, Robins WP, Kemp P, Molineux IJ. 2000.. The internal head protein Gp16 controls DNA ejection from the bacteriophage T7 virion. . J. Mol. Biol. 301::35–45
     [Crossref] [Google Scholar]
  118. 118.
    Sun L, Young LN, Zhang X, Boudko SP, Fokine A, et al. 2014.. Icosahedral bacteriophage ΦX174 forms a tail for DNA transport during infection. . Nature 505::432–35
     [Crossref] [Google Scholar]
  119. 119.
    Sun Y, Roznowski AP, Tokuda JM, Klose T, Mauney A, et al. 2017.. Structural changes of tailless bacteriophage ΦX174 during penetration of bacterial cell walls. . PNAS 114:(52):13708–13
     [Crossref] [Google Scholar]
  120. 120.
    Swanson NA, Hou CD, Cingolani G. 2022.. Viral ejection proteins: mosaically conserved, conformational gymnasts. . Microorganisms 10::504
     [Crossref] [Google Scholar]
  121. 121.
    Swanson NA, Lokareddy RK, Li F, Hou CF, Leptihn S, et al. 2021.. Cryo-EM structure of the periplasmic tunnel of T7 DNA-ejectosome at 2.7 Å resolution. . Mol. Cell 81::3145–59.e7
     [Crossref] [Google Scholar]
  122. 122.
    Swanson NA, Lokareddy RK, Li F, Hou CF, Pavlenok M, et al. 2021.. Expression and purification of phage T7 ejection proteins for cryo-EM analysis. . STAR Protoc. 2::100960
     [Crossref] [Google Scholar]
  123. 123.
    Taylor NM, Prokhorov NS, Guerrero-Ferreira RC, Shneider MM, Browning C, et al. 2016.. Structure of the T4 baseplate and its function in triggering sheath contraction. . Nature 533::346–52
     [Crossref] [Google Scholar]
  124. 124.
    Taylor NMI, van Raaij MJ, Leiman PG. 2018.. Contractile injection systems of bacteriophages and related systems. . Mol. Microbiol. 108::6–15
     [Crossref] [Google Scholar]
  125. 125.
    Thomas D, Prevelige P Jr. 1991.. A pilot protein participates in the initiation of P22 procapsid assembly. . Virology 182::673–81
     [Crossref] [Google Scholar]
  126. 126.
    Thomas JA, Rolando MR, Carroll CA, Shen PS, Belnap DM, et al. 2008.. Characterization of Pseudomonas chlororaphis myovirus 201Φ2-1 via genomic sequencing, mass spectrometry, and electron microscopy. . Virology 376::330–38
     [Crossref] [Google Scholar]
  127. 127.
    Tremblay DM, Tegoni M, Spinelli S, Campanacci V, Blangy S, et al. 2006.. Receptor-binding protein of Lactococcus lactis phages: identification and characterization of the saccharide receptor-binding site. . J. Bacteriol. 188::2400–10
     [Crossref] [Google Scholar]
  128. 128.
    Turner RD, Mesnage S, Hobbs JK, Foster SJ. 2018.. Molecular imaging of glycan chains couples cell-wall polysaccharide architecture to bacterial cell morphology. . Nat. Commun. 9::1263
     [Crossref] [Google Scholar]
  129. 129.
    Twort F. 1915.. An investigation on the nature of ultra-microscopic viruses. . Lancet 186::4814
     [Crossref] [Google Scholar]
  130. 130.
    Tzlil S, Kindt JT, Gelbart WM, Ben-Shaul A. 2003.. Forces and pressures in DNA packaging and release from viral capsids. . Biophys. J. 84::1616–27
     [Crossref] [Google Scholar]
  131. 131.
    Villanueva Valencia JR, Li D, Casjens SR, Evilevitch A. 2023.. ‘SAXS-osmometer’ method provides measurement of DNA pressure in viral capsids and delivers an empirical equation of state. . Nucleic Acids Res. 51::11415–27
     [Crossref] [Google Scholar]
  132. 132.
    Vollmer W, Blanot D, de Pedro MA. 2008.. Peptidoglycan structure and architecture. . FEMS Microbiol. Rev. 32::149–67
     [Crossref] [Google Scholar]
  133. 133.
    Vybiral D, Takac M, Loessner M, Witte A, von Ahsen U, Blasi U. 2003.. Complete nucleotide sequence and molecular characterization of two lytic Staphylococcus aureus phages: 44AHJD and P68. . FEMS Microbiol. Lett. 219::275–83
     [Crossref] [Google Scholar]
  134. 134.
    Wang C, Tu J, Liu J, Molineux IJ. 2019.. Structural dynamics of bacteriophage P22 infection initiation revealed by cryo-electron tomography. . Nat. Microbiol. 4::1049–56
     [Crossref] [Google Scholar]
  135. 135.
    Whitfield C, Szymanski CM, Lewis AL, Aebi M. 2022.. Eubacteria. . In Essentials of Glycobiology, ed. A Varki, RD Cummings, JD Esko, P Stanley, GW Hart , et al., pp. 279–96. New York:: Cold Spring Harb.
     [Google Scholar]
  136. 136.
    Wittmann J, Turner D, Millard AD, Mahadevan P, Kropinski AM, Adriaenssens EM. 2020.. From orphan phage to a proposed new family—the diversity of N4-like viruses. . Antibiotics 9::663
     [Crossref] [Google Scholar]
  137. 137.
    Wu W, Leavitt JC, Cheng N, Gilcrease EB, Motwani T, et al. 2016.. Localization of the Houdinisome (ejection proteins) inside the bacteriophage P22 virion by bubblegram imaging. . mBio 7:(4):e01152-16
     [Crossref] [Google Scholar]
  138. 138.
    Wu W, Thomas JA, Cheng N, Black LW, Steven AC. 2012.. Bubblegrams reveal the inner body of bacteriophage phiKZ. . Science 335::182
     [Crossref] [Google Scholar]
  139. 139.
    Xiang Y, Leiman PG, Li L, Grimes S, Anderson DL, Rossmann MG. 2009.. Crystallographic insights into the autocatalytic assembly mechanism of a bacteriophage tail spike. . Mol. Cell 34::375–86
     [Crossref] [Google Scholar]
  140. 140.
    Xu J, Gui M, Wang D, Xiang Y. 2016.. The bacteriophage Φ29 tail possesses a pore-forming loop for cell membrane penetration. . Nature 534::544–47
     [Crossref] [Google Scholar]
  141. 141.
    Yang F, Jiang YL, Zhang JT, Zhu J, Du K, et al. 2023.. Fine structure and assembly pattern of a minimal myophage Pam3. . PNAS 120::e2213727120
     [Crossref] [Google Scholar]
  142. 142.
    Yap ML, Klose T, Arisaka F, Speir JA, Veesler D, et al. 2016.. Role of bacteriophage T4 baseplate in regulating assembly and infection. . PNAS 113::2654–59
     [Crossref] [Google Scholar]
  143. 143.
    Young R. 2014.. Phage lysis: three steps, three choices, one outcome. . J. Microbiol. 52::243–58
     [Crossref] [Google Scholar]
  144. 144.
    Zehring WA, Rothman-Denes LB. 1983.. Purification and characterization of coliphage N4 RNA polymerase II activity from infected cell extracts. . J. Biol. Chem. 258::8074–80
     [Crossref] [Google Scholar]
  145. 145.
    Zhong Q, Carratala A, Nazarov S, Guerrero-Ferreira RC, Piccinini L, et al. 2016.. Genetic, structural, and phenotypic properties of MS2 coliphage with resistance to ClO2 disinfection. . Environ. Sci. Technol. 50::13520–28
     [Crossref] [Google Scholar]
  146. 146.
    Zinke M, Sachowsky KAA, Oster C, Zinn-Justin S, Ravelli R, et al. 2020.. Architecture of the flexible tail tube of bacteriophage SPP1. . Nat. Commun. 11::5759
     [Crossref] [Google Scholar]
  147. 147.
    Zivin R, Zehring W, Rothman-Denes LB. 1981.. Transcriptional map of bacteriophage N4: location and polarity of N4 RNAs. . J. Mol. Biol. 152::335–56
     [Crossref] [Google Scholar]
/content/journals/10.1146/annurev-micro-041222-124727
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Viral Genome Delivery Across Bacterial Cell Surfaces
Annual Review of Microbiology 78, 125 (2024); https://doi.org/10.1146/annurev-micro-041222-124727
/content/journals/10.1146/annurev-micro-041222-124727
/content/journals/10.1146/annurev-micro-041222-124727
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