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Structure and Function of Bacteriophages

  • Marta Sanz-Gaitero
  • Mateo Seoane-Blanco
  • Mark J. van RaaijEmail author
Living reference work entry

Abstract

Bacteriophages, or phages, are viruses with an exquisitely evolved structure to accomplish their goals. These goals are recognizing a suitable host bacterium, profiting from the host metabolism, and producing multiple progeny phages that are stable enough to survive until they find a new host bacterium to infect. Their genomes consist of single-stranded RNA, double-stranded RNA, single-stranded DNA, or double-stranded DNA, depending on phage type. They store their genome in highly symmetric protein capsids to protect it from degradation. Often these capsids are icosahedral, but helical and other shapes are also used. Tectiviridae and Corticoviridae have an internal lipid membrane, while Cystoviridae sport an outer membrane layer. Phages with tails, belonging to the Caudovirales order, are the most commonly encountered bacteriophages and have icosahedral or prolate capsids. In addition to the capsid, phages need a host cell recognition apparatus. The small icosahedral Leviviridae have a single minor capsid protein for this purpose. More complex phages dedicate multiple proteins to host cell recognition, and examples of this are the helical Inoviridae and the icosahedral Tectiviridae, Corticoviridae, and Cystoviridae. The Caudovirales have highly efficient tail protein complexes for DNA transfer. These tails are flexible (Siphoviridae), extensible (Podoviridae), or contractile (Myoviridae). Apart from elements designed for genome protection, host recognition, and genome transfer, more complicated phage particles may contain proteins for environmental sensing, binding to suitable matrices where host bacteria are likely to be encountered, and other functions.

Notes

Acknowledgments

Structure figures were generated using the PYMOL Molecular Graphics System (Schrödinger LLC) and UCSF CHIMERA (Pettersen et al. 2004). The research in our lab is funded by grants BFU2017-82207-P from the Spanish Ministry of Science, Innovation and Universities, State Agency of Research, co-financed by the European Regional Development Fund of the European Union. We thank Antonio Pichel for help with the sections on the Microviridae and Cystoviridae and for preparing Figs. 5 and 9. We are also grateful to Carmen San Martín (CNB-CSIC) and Carmela García-Doval (University of Zurich) for proofreading, to Don Marvin for advice on inovirus structure, and to Petr Leiman (University of Texas Medical Branch) for advice on figures; any remaining mistakes are the responsibility of the authors.

References

  1. Abrescia NG, Cockburn JJ, Grimes JM, Sutton GC, Diprose JM, Butcher SJ, Fuller SD, San Martín C, Burnett RM, Stuart DI, Bamford DH, Bamford JKH (2004) Insights into assembly from structural analysis of bacteriophage PRD1. Nature 432:68–74PubMedCrossRefGoogle Scholar
  2. Abrescia NG, Grimes JM, Kivelä HM, Assenberg R, Sutton GC, Butcher SJ, Bamford JK, Bamford DH, Stuart DI (2008) Insights into virus evolution and membrane biogenesis from the structure of the marine lipid-containing bacteriophage PM2. Mol Cell 31:749–761PubMedCrossRefGoogle Scholar
  3. Abrescia NG, Bamford DH, Grimes JM, Stuart DI (2012) Structure unifies the viral universe. Annu Rev Biochem 81:795–822PubMedCrossRefGoogle Scholar
  4. Ackermann HW, Prangishvili D (2012) Prokaryote viruses studied by electron microscopy. Arch Virol 157:1843–1849PubMedCrossRefGoogle Scholar
  5. Ageno M, Donelli G, Guglielmi F (1973) Structure and physico-chemical properties of bacteriophage G. II, the shape and symmetry of the capsid. Micron 4:376–403Google Scholar
  6. Aksyuk AA, Leiman PG, Kurochkina LP, Shneider MM, Kostyuchenko VA, Mesyanzhinov VV, Rossmann MG (2009a) The tail sheath structure of bacteriophage T4: a molecular machine for infecting bacteria. EMBO J 28:821–829PubMedPubMedCentralCrossRefGoogle Scholar
  7. Aksyuk AA, Leiman PG, Shneider MM, Mesyanzhinov VV, Rossmann MG (2009b) The structure of gene product 6 of bacteriophage T4, the hinge-pin of the baseplate. Structure 17:800–808PubMedCrossRefGoogle Scholar
  8. Arisaka F, Yap ML, Janamaru S, Rossmann MG (2016) Molecular assembly and structure of the bacteriophage T4 tail. Biophys Rev 8:385–396PubMedPubMedCentralCrossRefGoogle Scholar
  9. Arnaud CA, Effantin G, Vivès C, Engilberge S, Bacia M, Boulanger P, Girard E, Schoehn G, Breyton C (2017) Bacteriophage T5 tail tube structure suggests a trigger mechanism for Siphoviridae DNA ejection. Nat Commun 8:1953PubMedPubMedCentralCrossRefGoogle Scholar
  10. Bamford DH, Palva ET, Lounatmaa K (1976) Ultrastructure and life cycle of the lipid-containing bacteriophage ϕ6. J Gen Virol 32:249–259PubMedCrossRefGoogle Scholar
  11. Baptista C, Santos MA, São-José C (2008) Phage SPP1 reversible adsorption to Bacillus subtilis cell wall teichoic acids accelerates virus recognition of membrane receptor YueB. J Bacteriol 190:4989–4996PubMedPubMedCentralCrossRefGoogle Scholar
  12. Bartual SG, Garcia-Doval C, Alonso J, Schoehn G, van Raaij MJ (2010a) Two-chaperone assisted soluble expression and purification of the bacteriophage T4 long tail fibre protein gp37. Protein Expr Purif 70:116–121PubMedCrossRefGoogle Scholar
  13. Bartual SG, Otero JM, Garcia-Doval C, Llamas-Saiz AL, Kahn R, Fox GC, van Raaij MJ (2010b) Structure of the bacteriophage T4 long tail fiber receptor-binding tip. Proc Natl Acad Sci U S A 107:20287–20292PubMedPubMedCentralCrossRefGoogle Scholar
  14. Bebeacua C, Bron P, Lai L, Vegge CS, Brøndsted L, Spinelli S, Campanacci V, Veesler D, van Heel M, Cambillau C (2010) Structure and molecular assignment of lactococcal phage TP901-1 baseplate. J Biol Chem 285:39079–39086PubMedPubMedCentralCrossRefGoogle Scholar
  15. Bernal RA, Hafenstein S, Olson NH, Bowman VD, Chipman PR, Baker TS, Fane BA, Rossmann MG (2003) Structural studies of bacteriophage α3 assembly. J Mol Biol 325:11–24PubMedPubMedCentralCrossRefGoogle Scholar
  16. Bernhardt TG, Wang IN, Struck DK, Young R (2001) A protein antibiotic in the phage Qβ virion: diversity in lysis targets. Science 292:2326–2327PubMedCrossRefGoogle Scholar
  17. Bhardwaj A, Molineux IJ, Casjens SR, Cingolani G (2011) Atomic structure of bacteriophage Sf6 tail needle knob. J Biol Chem 286:30867–30877PubMedPubMedCentralCrossRefGoogle Scholar
  18. Bhardwaj A, Olia AS, Cingolani G (2014) Architecture of viral genome-delivery molecular machines. Curr Opin Struct Biol 25:1–8PubMedCrossRefGoogle Scholar
  19. Black LW, Thomas JA (2012) Condensed genome structure. Adv Exp Med Biol 726:469–487PubMedPubMedCentralCrossRefGoogle Scholar
  20. Bollback JP, Huelsenbeck JP (2001) Phylogeny, genome evolution, and host specificity of single-stranded RNA bacteriophage (family Leviviridae). J Mol Evol 52:117–128PubMedCrossRefGoogle Scholar
  21. Boudko SP, Londer YY, Letarov AV, Sernova NV, Engel J, Mesyanzhinov VV (2002) Domain organization, folding and stability of bacteriophage T4 fibritin, a segmented coiled-coil protein. Eur J Biochem 269:833–841PubMedCrossRefGoogle Scholar
  22. Boudko SP, Strelkov SV, Engel J, Stetefeld J (2004) Design and crystal structure of bacteriophage T4 mini-fibritin NCCF. J Mol Biol 339:927–935PubMedCrossRefGoogle Scholar
  23. Brewer GJ (1978) Membrane-localized replication of bacteriophage PM2. Virology 84:242–245PubMedCrossRefGoogle Scholar
  24. Browning C, Shneider MM, Bowman VD, Schwarzer D, Leiman PG (2012) Phage pierces the host cell membrane with the iron-loaded spike. Structure 20:326–339PubMedCrossRefGoogle Scholar
  25. Butcher SJ, Manole V, Karhu NJ (2012) Lipid-containing viruses: bacteriophage PRD1 assembly. Adv Exp Med Biol 726:365–377PubMedCrossRefGoogle Scholar
  26. Büttner CR, Wu Y, Maxwell KL, Davidson AR (2016) Baseplate assembly of phage mu: defining the conserved core components of contractile-tailed phages and related bacterial systems. Proc Natl Acad Sci U S A 113:10174–10179PubMedPubMedCentralCrossRefGoogle Scholar
  27. Caldentey J, Bamford DH (1992) The lytic enzyme of the Pseudomonas phage ϕ6. Purification and biochemical characterization. Biochim Biophys Acta 1159:44–50PubMedCrossRefGoogle Scholar
  28. Canelo E, Phillips OM, del Roure RN (1985) Relating cistrons and functions in bacteriophage PM2. Virology 140:364–367PubMedCrossRefGoogle Scholar
  29. Casjens S, King J (1975) Virus assembly. Annu Rev Biochem 44:555–611PubMedCrossRefGoogle Scholar
  30. Casjens SR, Molineux IJ (2012) Short noncontractile tail machines: adsorption and DNA delivery by podoviruses. Adv Exp Med Biol 726:143–179PubMedCrossRefGoogle Scholar
  31. Caspar DL, Klug A (1962) Physical principles in the construction of regular viruses. Cold Spring Harb Symp Quant Biol 27:1–24PubMedCrossRefGoogle Scholar
  32. Chaban Y, Lurz R, Brasiles S, Cornilleau C, Karreman M, Zinn-Justin S, Tavares P, Orlova EV (2015) Structural rearrangements in the phage head-to-tail interface during assembly and infection. Proc Natl Acad Sci U S A 112:7009–7014PubMedPubMedCentralCrossRefGoogle Scholar
  33. Chipman PR, Agbandje-McKenna M, Renaudin J, Baker TS, McKenna R (1998) Structural analysis of the Spiroplasma virus, SpV4: implications for evolutionary variation to obtain host diversity among the Microviridae. Structure 6:135–145PubMedPubMedCentralCrossRefGoogle Scholar
  34. 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 378:726–736PubMedPubMedCentralCrossRefGoogle Scholar
  35. Cockburn JJ, Abrescia NG, Grimes JM, Sutton GC, Diprose JM, Benevides JM, Thomas GJ, Bamford DH, Bamford JK, Stuart DI (2004) Membrane structure and interactions with protein and DNA in bacteriophage PRD1. Nature 432:122–125PubMedCrossRefGoogle Scholar
  36. Cuervo A, Pulido-Cid M, Chagoyen M, Arranz R, González-García V, Garcia-Doval C, Castón JR, Valpuesta JM, van Raaij MJ, Martín-Benito K, Carrascosa JL (2013) Structural characterization of the bacteriophage T7 tail. J Biol Chem 288:26290–26299PubMedPubMedCentralCrossRefGoogle Scholar
  37. Dai X, Li Z, Lai M, Shu S, Du Y, Zhou ZH, Sun R (2017) In situ structures of the genome and genome-delivery apparatus in a single-stranded RNA virus. Nature 541:112–116PubMedCrossRefGoogle Scholar
  38. Davidson AR, Cardarelli L, Pell LG, Radford DR, Maxwell KL (2012) Long noncontractile tail machines of bacteriophages. Adv Exp Med Biol 726:115–142PubMedCrossRefGoogle Scholar
  39. Doore SM, Fane BA (2016) The Microviridae: diversity, assembly, and experimental evolution. Virology 461:45–55CrossRefGoogle Scholar
  40. Dunne M, Denyes JM, Arndt H, Loessner MJ, Leiman PG, Klumpp J (2018) Salmonella phage S16 tail fiber adhesin features a rare polyglycine rich domain for host recognition. Structure 26:1573–1582PubMedCrossRefGoogle Scholar
  41. El Omari K, Meier C, Kainov D, Sutton G, Grimes JM, Poranen MM, Bamford DH, Tuma R, Stuart DI, Mancini EJ (2013a) Tracking in atomic detail the functional specializations in viral RecA helicases that occur during evolution. Nucleic Acids Res 41:9396–9410PubMedPubMedCentralCrossRefGoogle Scholar
  42. El Omari K, Sutton G, Ravantti JJ, Zhang HW, Walter TS, Grimes JM, Bamford DH, Stuart DI, Mancini EJ (2013b) Plate tectonics of virus shell assembly. Structure 21:1384–1395PubMedPubMedCentralCrossRefGoogle Scholar
  43. Espejo RT, Canelo ES, Sinsheimer RL (1969) DNA of bacteriophage PM2: a closed circular double-stranded molecule. Proc Natl Acad Sci U S A 63:1164–1168PubMedPubMedCentralCrossRefGoogle Scholar
  44. Farley MM, Tu J, Kearns DB, Molineaux IJ, Liu J (2017) Ultrastructural analysis of bacteriophage ϕ29 during infection of Bacillus subtilis. J Struct Biol 197:163–171PubMedCrossRefGoogle Scholar
  45. Feng JN, Model P, Russel M (1999) A trans-envelope protein complex needed for filamentous phage assembly and export. Mol Microbiol 34:745–755PubMedCrossRefGoogle Scholar
  46. Fiers W, Contreras R, Duerinck F, Haegeman G, Iserentant D, Merregaert J, Min Jou W, Molemans F, Raeymaekers A, Van den Berghe A, Volckaert G, Ysebaert M (1976) Complete nucleotide sequence of bacteriophage MS2 RNA: primary and secondary structure of the replicase gene. Nature 260:500–507PubMedCrossRefGoogle Scholar
  47. Flayhan A, Vellieux FM, Lurz R, Maury O, Contreras-Martel C, Girard E, Boulanger P, Breyton C (2014) Crystal structure of pb9, the distal tail protein of bacteriophage T5: a conserved structural motif among all siphophages. J Virol 88:820–828PubMedPubMedCentralCrossRefGoogle Scholar
  48. Fokine A, Rossmann MG (2014) Molecular architecture of tailed double-stranded DNA phages. Bacteriophage 4:e28281PubMedPubMedCentralCrossRefGoogle Scholar
  49. Fokine A, Chipman PR, Leiman PG, Mesyanzhinov VV, Rao VB, Rossmann MG (2004) Molecular architecture of the prolate head of bacteriophage T4. Proc Natl Acad Sci 101:6003–6008PubMedCrossRefGoogle Scholar
  50. Fokine A, Islam MZ, Zhang Z, Bowman VD, Rao VB, Rossmann MG (2011) Structure of the three N-terminal immunoglobulin domains of the highly immunogenic outer capsid protein from a T4-like bacteriophage. J Virol 85:8141–8148PubMedPubMedCentralCrossRefGoogle Scholar
  51. Fokine A, Zhang Z, Kanamaru S, Bowman VD, Aksyuk AA, Arisaka F, Rao VB, Rossmann MG (2013) The molecular architecture of the bacteriophage T4 neck. J Mol Biol 425:1731–1744PubMedPubMedCentralCrossRefGoogle Scholar
  52. Frilander M, Bamford DH (1995) In vitro packaging of the single-stranded RNA genomic precursors of the segmented double-stranded RNA bacteriophage ϕ6: the three segments modulate each other’s packaging efficiency. J Mol Biol 246:418–428PubMedCrossRefGoogle Scholar
  53. Garcia-Doval C, van Raaij MJ (2012) Structure of the receptor-binding carboxy-terminal domain of bacteriophage T7 tail fibers. Proc Natl Acad Sci U S A 109:9390–9395PubMedPubMedCentralCrossRefGoogle Scholar
  54. Garcia-Doval C, van Raaij MJ (2013) Bacteriophage receptor recognition and nucleic acid transfer. Subcell Biochem 68:489–518PubMedCrossRefGoogle Scholar
  55. Garcia-Doval C, Castón JR, Luque D, Granell M, Otero JM, Llamas-Saiz AL, Renouard M, Boulanger P, van Raaij MJ (2015) Structure of the receptor-binding carboxy-terminal domain of the bacteriophage T5 L-shaped tail fibre with and without its intra-molecular chaperone. Viruses 7:6424–6440PubMedPubMedCentralCrossRefGoogle Scholar
  56. Golmohammadi R, Valegard K, Fridborg K, Liljas L (1993) The refined structure of bacteriophage MS2 at 2.8 Å resolution. J Mol Biol 234:620–639PubMedCrossRefGoogle Scholar
  57. Golmohammadi R, Fridborg K, Bundule M, Valegard K, Liljas L (1996) The crystal structure of bacteriophage Qβ at 3.5 Å resolution. Structure 4:543–554PubMedCrossRefGoogle Scholar
  58. González-García VA, Pulido-Cid M, Garcia-Doval C, Bocanegra R, van Raaij MJ, Martin-Benito J, Cuervo A, Carrascosa JL (2015) Conformational changes leading to T7 DNA delivery upon interaction with the bacterial receptor. J Biol Chem 290:10038–10044PubMedPubMedCentralCrossRefGoogle Scholar
  59. Gorzelnik KV, Cui Z, Reed CA, Jakana J, Young R, Zhang J (2016) Asymmetric cryo-EM structure of the canonical Allolevivirus Qβ reveals a single maturation protein and the genomic ssRNA in situ. Proc Natl Acad Sci U S A 113:11519–11524PubMedPubMedCentralCrossRefGoogle Scholar
  60. Granell M, Namura M, Alvira S, Kanamaru S, van Raaij MJ (2017) Crystal structure of the carboxy-terminal region of the bacteriophage T4 proximal long tail fiber protein gp34. Viruses 9:E168PubMedCrossRefGoogle Scholar
  61. Guerrero-Ferreira RC, Hupfeld M, Nazarov S, Taylor NM, Shneider MM, Obbineni JM, Loessner MJ, Ishikawa T, Klumpp J, Leiman PG (2019) Structure and transformation of bacteriophage A511 baseplate and tail upon infection of Listeria cells. EMBO J 38:e99455PubMedCrossRefGoogle Scholar
  62. Haggård-Ljungquist E, Halling C, Calendar R (1992) DNA sequences of the tail fiber genes of bacteriophage P2: evidence for horizontal transfer of tail fiber genes among unrelated bacteriophages. J Bacteriol 174:1462–1477PubMedPubMedCentralCrossRefGoogle Scholar
  63. Henderson R (2015) Overview and future of single particle electron cryomicroscopy. Arch Biochem Biophys 581:19–24PubMedCrossRefGoogle Scholar
  64. Higashitani A, Higashitani N, Horiuchi K (1997) Minus-strand origin of filamentous phage versus transcriptional promoters in recognition of RNA polymerase. Proc Natl Acad Sci U S A 94:2909–2914PubMedPubMedCentralCrossRefGoogle Scholar
  65. Higman VA (2013) Nuclear magnetic resonance methods for studying soluble, fibrous, and membrane-embedded proteins. In: Rusa JM, Piñeiro A (eds) Proteins in solution and at interfaces: methods and applications in biotechnology and materials science. Wiley, New York, pp 23–48CrossRefGoogle Scholar
  66. Holliger P, Riechmann L, Williams RL (1999) Crystal structure of the two N-terminal domains of g3p from filamentous phage fd at 1.9 Å: evidence for conformational lability. J Mol Biol 288:649–657PubMedCrossRefGoogle Scholar
  67. Hong C, Oksanen HM, Liu X, Jakana J, Bamford DH, Chiu W (2014) A structural model of the genome packaging process in a membrane-containing double stranded DNA virus. PLoS Biol 12:e1002024PubMedPubMedCentralCrossRefGoogle Scholar
  68. Hu GB, Wei H, Rice WJ, Stokes DL, Paul Gottlieb P (2008) Electron cryo-tomographic structure of cystovirus ϕ12. Virology 372:1–9PubMedCrossRefGoogle Scholar
  69. Hu B, Margolin W, Molineaux IJ, Liu J (2013) The bacteriophage T7 virion undergoes extensive structural remodeling during infection. Science 339:577–579CrossRefGoogle Scholar
  70. Hu B, Margolin W, Molineux IJ, Liu J (2015) Structural remodelling of bacteriophage T4 and host membranes during infection initiation. Proc Natl Acad Sci U S A 112:E4919–E4928PubMedPubMedCentralCrossRefGoogle Scholar
  71. Hua J, Huet A, Lopez CA, Toropova K, Pope WH, Duda RL, Hendrix RW, Conway JF (2017) Capsids and genomes of jumbo-sized bacteriophages reveal the evolutionary reach of the HK97 fold. MBio 8:e01579-01517CrossRefGoogle Scholar
  72. Huiskonen JT, Kivelä HM, Bamford DH, Butcher SJ (2004) The PM2 virion has a novel organization with an internal membrane and pentameric receptor binding spikes. Nat Struct Mol Biol 11:850–856PubMedCrossRefGoogle Scholar
  73. Huiskonen JT, Manole V, Butcher SJ (2007) Tale of two spikes in bacteriophage PRD1. Proc Natl Acad Sci U S A 104:6666–6671PubMedPubMedCentralCrossRefGoogle Scholar
  74. Hyman P, van Raaij MJ (2018) Bacteriophage T4 long tail fiber domains. Biophys Rev 10:463–471PubMedCrossRefGoogle Scholar
  75. 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 226:221–227PubMedCrossRefGoogle Scholar
  76. Jäälinoja HT, Huiskonen JT, Butcher SJ (2007) Electron cryomicroscopy comparison of the architectures of the enveloped bacteriophages ϕ6 and ϕ8. Structure 15:157–167PubMedCrossRefGoogle Scholar
  77. Johnson JE, Speir JA (1997) Quasi-equivalent viruses: a paradigm for protein assemblies. J Mol Biol 269:665–675PubMedCrossRefGoogle Scholar
  78. Kanamaru S, Leiman PG, Kostyuchenko VA, Chipman PR, Mesyanzhinov VV, Arisaka F, Rossmann MG (2002) Structure of the cell-puncturing device of bacteriophage T4. Nature 415:553–557PubMedCrossRefGoogle Scholar
  79. Karlsson F, Borrebaeck CA, Nilsson N, Malmborg-Hager AC (2003) The mechanism of bacterial infection by filamentous phages involves molecular interactions between TolA and phage protein 3 domains. J Bacteriol 185:2628–2634PubMedPubMedCentralCrossRefGoogle Scholar
  80. Katsura I (1990) Mechanism of length determination in bacteriophage lambda tails. Adv Biophys 26:1–18PubMedCrossRefGoogle Scholar
  81. Kikuchi Y, King J (1975) Assembly of the tail of bacteriophage T4. J Supramol Struct 3:24–38PubMedCrossRefGoogle Scholar
  82. Kivelä HM, Männistö RH, Kalkkinen N, Bamford DH (1999) Purification and protein composition of PM2, the first lipid-containing bacterial virus to be isolated. Virology 262:364–374PubMedCrossRefGoogle Scholar
  83. Kivelä HM, Kalkkinen N, Bamford DH (2002) Bacteriophage PM2 has a protein capsid surrounding a spherical proteinaceous lipid core. J Virol 76:8169–8178PubMedPubMedCentralCrossRefGoogle Scholar
  84. Kivelä HM, Daugelavičius R, Hankkio RH, Bamford JKH, Bamford DH (2004) Penetration of membrane-containing double-stranded-DNA bacteriophage PM2 into Pseudoalteromonas hosts. J Bacteriol 186:5342–5354PubMedPubMedCentralCrossRefGoogle Scholar
  85. Kivelä HM, Abrescia NGA, Bamford JKH, Grimes JM, Stuart DI, Bamford DH (2008) Selenomethionine labeling of large biological macromolecular complexes: probing the structure of marine bacterial virus PM2. J Struct Biol 161:204–210PubMedCrossRefGoogle Scholar
  86. Koç C, Xia G, Kühner P, Spinelli S, Roussel A, Cambillau C, Stehle T (2016) Structure of the host-recognition device of Staphylococcus aureus phage ϕ11. Sci Rep 6:27581PubMedPubMedCentralCrossRefGoogle Scholar
  87. Korasick DA, Tanner JJ (2018) Determination of protein oligomeric structure from small-angle X-ray scattering. Protein Sci 27:814–824PubMedPubMedCentralCrossRefGoogle Scholar
  88. Kostyuchenko VA, Navruzbekov GA, Kurochkina LP, Strelkov SV, Mesyanzhinov VV, Rossmann MG (1999) The structure of bacteriophage T4 gene product 9: the trigger for tail contraction. Structure 7:1213–1222PubMedCrossRefGoogle Scholar
  89. Kostyuchenko VA, Chipman PR, Leiman PG, Arisaka F, Mesyanzhinov VV, Rossmann MG (2005) The tail structure of bacteriophage T4 and its mechanism of contraction. Nat Struct Mol Biol 12:810–813PubMedCrossRefGoogle Scholar
  90. Krupovic M, Daugelavicius R, Bamford DH (2007) A novel lysis system in PM2, a lipid-containing marine double-stranded DNA bacteriophage. Mol Microbiol 64:1635–1648PubMedCrossRefGoogle Scholar
  91. Kudryashev M, Wang RY, Brackmann M, Scherer S, Maier T, Baker D, DiMaio F, Stahlberg H, Egelman EH, Basler M (2015) Structure of the type VI secretion system contractile sheath. Cell 160:952–962PubMedPubMedCentralCrossRefGoogle Scholar
  92. Kühlbrandt W (2014) Cryo-EM enters a new era. elife 3:e03678PubMedPubMedCentralCrossRefGoogle Scholar
  93. Lavigne R, Darius P, Summer EJ, Seto D, Mahdevan P, Nilson AS, Ackermann KAM (2009) Classification of Myoviridae bacteriophages using protein sequence similarity. BMC Microbiol 9:224PubMedPubMedCentralCrossRefGoogle Scholar
  94. Leiman PG (2018) Stretching the arms of the type VI secretion sheath protein. EMBO Rep 19:191–193PubMedPubMedCentralCrossRefGoogle Scholar
  95. Leiman PG, Shneider MM (2012) Contractile tail machines of bacteriophages. Adv Exp Med Biol 726:93–114PubMedCrossRefGoogle Scholar
  96. Leiman PG, Kostyuchenko VA, Shneider MM, Kurochkina LP, Mesyanzhinov VV, Rossmann MG (2000) Structure of bacteriophage T4 gene product 11, the interface between the baseplate and short tail fibers. J Mol Biol 301:975–985PubMedCrossRefGoogle Scholar
  97. Leiman PG, Chipman PR, Kostyuchenko VA, Mesyanzhinov VV, Rossmann MG (2004) Three-dimensional rearrangement of proteins in the tail of bacteriophage T4 on infection of its host. Cell 118:419–429PubMedCrossRefGoogle Scholar
  98. Leiman PG, Shneider MM, Mesyanzhinov VV, Rossmann MG (2006) Evolution of bacteriophage tails: structure of T4 gene product 10. J Mol Biol 358:912–921PubMedCrossRefGoogle Scholar
  99. Leiman PG, Battisti AJ, Bowman VD, Stumeyer K, Mühlenhoff M, Gerardy-Schahn R, Scholl D, Molineaux IJ (2007) The structures of bacteriophages K1E and K1-5 explain processive degradation of polysaccharide capsules and evolution of new host specificities. J Mol Biol 371:836–849PubMedCrossRefGoogle Scholar
  100. Leiman PG, Arisaka F, van Raaij MJ, Kostyuchenko VA, Aksyuk AA, Kanamaru S, Rossmann MG (2010) Morphogenesis of the T4 tail and tail fibers. Virol J 7:355PubMedPubMedCentralCrossRefGoogle Scholar
  101. Lhuillier S, Gallopin M, Gilquin B, Brasilès S, Lancelot N, Letellier G, Gilles M, Dethan G, Orlova EV, Couprie J, Tavares P, Zinn-Justin S (2009) Structure of bacteriophage SPP1 head-to-tail connection reveals mechanism for viral DNA gating. Proc Natl Acad Sci U S A 106:8507–8512PubMedPubMedCentralCrossRefGoogle Scholar
  102. Li X, Koç C, Kühner P, Stierhof YD, Krismer B, Enright MC, Penadés JR, Wolz C, Stehle T, Cambillau C, Peschel A, Xia G (2016) An essential role for the baseplate protein gp45 in phage adsorption to Staphylococcus aureus. Sci Rep 6:26455PubMedPubMedCentralCrossRefGoogle Scholar
  103. Liu Y, Eisenberg D (2002) 3D domain swapping: as domains continue to swap. Protein Sci 11:1285–1299PubMedPubMedCentralCrossRefGoogle Scholar
  104. Liu X, Zhang Q, Murata K, Baker ML, Sullivan MB, Fu C, Dougherty MT, Schmid MF, Osburne MS, Chisholm SW, Chiu W (2010) Structural changes in a marine podovirus associated with release of its genome into Prochlorococcus. Nat Struct Mol Biol 17:830–836PubMedPubMedCentralCrossRefGoogle Scholar
  105. Llamas-Saiz AL, van Raaij MJ (2013) X-ray crystallography of biological macromolecules: fundamentals and applications. In: Rusa JM, Piñeiro A (eds) Proteins in solution and at interfaces: methods and applications in biotechnology and materials science. Wiley, New York, pp 3–22Google Scholar
  106. Lortat-Jacob H, Chouin E, Cusack S, van Raaij MJ (2001) Kinetic analysis of adenovirus fiber binding to its receptor reveals an avidity mechanism for trimeric receptor-ligand interactions. J Biol Chem 276:9009–9015PubMedCrossRefGoogle Scholar
  107. Lubkowski J, Hennecke F, Plückthun A, Wlodawer A (1999) Filamentous phage infection: crystal structure of g3p in complex with its coreceptor, the C-terminal domain of TolA. Structure 7:711–722PubMedCrossRefGoogle Scholar
  108. Mahony J, Stockdale SR, Collins B, Spinelli S, Douillard FP, Cambillau C, van Sinderen D (2016) Lactococcus lactis phage TP901-1 as a model for Siphoviridae virion assembly. Bacteriophage 6:e1123795PubMedPubMedCentralCrossRefGoogle Scholar
  109. Männistö RH, Kivelä HM, Paulin L, Bamford DH, Bamford JK (1999) The complete genome sequence of PM2, the first lipid-containing bacterial virus to be isolated. Virology 262:355–336PubMedCrossRefGoogle Scholar
  110. Mäntynen S, Sundberg LR, Poranen MM (2018) Recognition of six additional cystoviruses: Pseudomonas virus phi6 is no longer the sole species of the family Cystoviridae. Arch Virol 163:1117–1124PubMedCrossRefGoogle Scholar
  111. Marvin DA (1998) Filamentous phage structure, infection and assembly. Curr Opin Struct Biol 8:150–158PubMedCrossRefGoogle Scholar
  112. Marvin DA (2017) Fibre diffraction studies of biological macromolecules. Prog Biophys Mol Biol 127:43–87PubMedCrossRefGoogle Scholar
  113. Marvin DA, Welsh LC, Symmons MF, Scott WR, Straus SK (2006) Molecular structure of fd (f1, M13) filamentous bacteriophage refined with respect to X-ray fibre diffraction and solid-state NMR data supports specific models of phage assembly at the bacterial membrane. J Mol Biol 355:294–309PubMedCrossRefGoogle Scholar
  114. Marvin DA, Symmons MF, Straus SK (2014) Structure and assembly of filamentous bacteriophages. Prog Biophys Mol Biol 114:80–122PubMedCrossRefGoogle Scholar
  115. Maxwell KL, Yee AA, Booth V, Arrowsmith CH, Gold M, Davidson AR (2001) The solution structure of bacteriophage λ protein W, a small morphogenetic protein possessing a novel fold. J Mol Biol 308:9–14PubMedCrossRefGoogle Scholar
  116. Maxwell KL, Yee AA, Arrowsmith CH, Gold M, Davidson AR (2002) The solution structure of the bacteriophage λ head-tail joining protein, gpFII. J Mol Biol 318:1395–1404PubMedCrossRefGoogle Scholar
  117. Merckel MC, Huiskonen JT, Bamford DH, Goldman A, Tuma R (2005) The structure of the bacteriophage PRD1 spike sheds light on the evolution of viral capsid architecture. Mol Cell 18:161–170PubMedCrossRefGoogle Scholar
  118. Mitraki A, Papanikolopoulou K, van Raaij MJ (2006) Natural triple β-stranded fibrous folds. Adv Protein Chem 73:97–124PubMedCrossRefGoogle Scholar
  119. Moak M, Molineux IJ (2004) Peptidoglycan hydrolytic activities associated with bacteriophage virions. Mol Microbiol 51:1169–1183PubMedCrossRefGoogle Scholar
  120. Morais MC, Choi KH, Koti JS, Chipman PR, Anderson DL, Rossmann MG (2005) Conservation of the capsid structure in tailed dsDNA bacteriophages: the pseudoatomic structure of ϕ29. Mol Cell 18:149–159PubMedCrossRefGoogle Scholar
  121. Moreno-Madrid F, Martín-González N, Llauró A, Ortega-Esteban A, Hernando-Pérez M, Douglas T, Schaap IA, de Pablo PJ (2017) Atomic force microscopy of virus shells. Biochem Soc Trans 45:499–511PubMedCrossRefGoogle Scholar
  122. Nemecek D, Gilcrease EB, Kang S, Prevelige PE, Casjens S, Thomas GJ (2007) Subunit conformations and assembly states of a DNA-translocating motor: the terminase of bacteriophage P22. J Mol Biol 374:817–836PubMedPubMedCentralCrossRefGoogle Scholar
  123. Nemecek D, Boura E, Wu W, Cheng N, Plevka P, Qiao J, Mindich L, Heymann JB, Hurley JH, Steven AC (2013) Subunit folds and maturation pathway of a dsRNA virus capsid. Structure 21:1374–1383PubMedPubMedCentralCrossRefGoogle Scholar
  124. Ni CZ, Syed R, Kodandapani R, Wickersham J, Peabody DS, Ely KR (1995) Crystal structure of the MS2 coat protein dimer: implications for RNA binding and virus assembly. Structure 3:255–263PubMedCrossRefGoogle Scholar
  125. Nováček J, Šiborová S, Benešík M, Pantůček R, Doškař J, Plevka P (2016) Structure and genome release of Twort-like Myoviridae phage with a double-layered baseplate. Proc Natl Acad Sci U S A 113:9351–9356PubMedPubMedCentralCrossRefGoogle Scholar
  126. Olia AS, Casjens S, Cingolani G (2007) Structure of phage P22 cell envelope–penetrating needle. Nat Struct Mol Biol 14:1221–1226PubMedCrossRefGoogle Scholar
  127. Olia AS, Prevelige PE, Johnson JE, Cingolani G (2011) Three-dimensional structure of a viral genome-delivery portal vertex. Nat Struct Mol Biol 18:597–603PubMedPubMedCentralCrossRefGoogle Scholar
  128. Oliveira LM, Ye Z, Katz A, Alimova A, Wei H, Herman GT, Gottlieb P (2018) Component tree analysis of cystovirus ϕ6 nucleocapsid cryo-EM single particle reconstructions. PLoS One 13:e0188858PubMedPubMedCentralCrossRefGoogle Scholar
  129. 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 10:67PubMedCentralCrossRefPubMedGoogle Scholar
  130. Pell LG, Liu A, Edmonds L, Donaldson LW, Howell PL, Davidson AR (2009a) The X-ray crystal structure of the phage λ tail terminator protein reveals the biologically relevant hexameric ring structure and demonstrates a conserved mechanism of tail termination among diverse long-tailed phages. J Mol Biol 389:938–951PubMedCrossRefGoogle Scholar
  131. Pell LG, Kanelis V, Donaldson LW, Howell PL, Davidson AR (2009b) The phage λ major tail protein structure reveals a common evolution for long-tailed phages and the type VI bacterial secretion system. Proc Natl Acad Sci U S A 106:4160–4165PubMedPubMedCentralCrossRefGoogle Scholar
  132. Pell LG, Gasmi-Seabrook GM, Morais M, Neudecker P, Kanelis V, Bona D, Donaldson LW, Edwards AM, Howell PL, Davidson AR, Maxwell KL (2010 Oct 29) The solution structure of the C-terminal Ig-like domain of the bacteriophage λ tail tube protein. J Mol Biol 403(3):468–479PubMedCrossRefGoogle Scholar
  133. Perucchetti R, Parris W, Becker A, Gold M (1988) Late stages in bacteriophage λ head morphogenesis: in vitro studies on the action of the bacteriophage λ D-gene and W-gene products. Virology 165:103–114PubMedCrossRefGoogle Scholar
  134. Petrovski S, Dyson ZA, Seviour RJ, Tillet D (2012) Small but sufficient: the Rhodococcus phage RRH1 has the smallest known Siphoviridae genome at 14.2 kilobases. J Virol 86:358–363PubMedPubMedCentralCrossRefGoogle Scholar
  135. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE (2004) UCSF Chimera, a visualization system for exploratory research and analysis. J Comput Chem 25:1605–1612CrossRefGoogle Scholar
  136. Philippe C, Krupovic M, Jaomanjaka F, Claisse O, Petrel M, le Marrec M (2018) Bacteriophage GC1, a novel Tectivirus infecting Gluconobacter cerinus, an acetic acid bacterium associated with wine-making. Viruses 10:39PubMedCentralCrossRefPubMedGoogle Scholar
  137. Plevka P, Tars K, Liljas L (2008) Crystal packing of a bacteriophage MS2 coat protein mutant corresponds to octahedral particles. Protein Sci 17:1731–1739PubMedPubMedCentralCrossRefGoogle Scholar
  138. Poranen MM, Tuma R (2004) Self-assembly of double-stranded RNA bacteriophages. Virus Res 101:93–100PubMedCrossRefGoogle Scholar
  139. Prasad BV, Schmid MF (2012) Principles of virus structural organization. Adv Exp Med Biol 726:17–47PubMedPubMedCentralCrossRefGoogle Scholar
  140. Prevelige PE, Cortines JR (2018) Phage assembly and the special role of the portal protein. Curr Opin Virol 31:66–73PubMedCrossRefGoogle Scholar
  141. Prevelige PE, Fane BA (2012) Building the machines: scaffolding proteins functions during bacteriophage morphogenesis. Adv Exp Med Biol 726:325–350PubMedCrossRefGoogle Scholar
  142. Rakonjac J, Bennett NJ, Spagnuolo J, Gagic D, Russel M (2011) Filamentous bacteriophage: biology, phage display and nanotechnology applications. Curr Issues Mol Biol 13:51–57PubMedGoogle Scholar
  143. Rakonjac J, Russel M, Khanum S, Brooke SJ, Rajič M (2017) Filamentous phage: structure and biology. Adv Exp Med Biol 1053:1–20PubMedCrossRefGoogle Scholar
  144. Rao VB, Feiss M (2015) Mechanisms of DNA packaging by large double-stranded DNA viruses. Annu Rev Virol 9:351–378CrossRefGoogle Scholar
  145. Ross PD, Cheng N, Conway JF, Firek BA, Hendrix RW, Duda RL, Steven AC (2005) Crosslinking renders bacteriophage HK97 capsid maturation irreversible and effects an essential stabilization. EMBO J 24:1352–1363PubMedPubMedCentralCrossRefGoogle Scholar
  146. Rumnieks J, Tars K (2014) Crystal structure of the bacteriophage Qβ coat protein in complex with the RNA operator of the replicase gene. J Mol Biol 426:1039–1049PubMedCrossRefGoogle Scholar
  147. Russel M, Linderoth NA, Sali A (1997) Filamentous phage assembly: variation on a protein export theme. Gene 192:23–32PubMedCrossRefGoogle Scholar
  148. Santos-Pérez I, Oksanen HM, Bamford DH, Goñi FM, Reguera D, Abrescia NGA (2017) Membrane-assisted viral DNA ejection. Biochim Biophys Acta 1861:664–672CrossRefGoogle Scholar
  149. Schulz EC, Dickmanns A, Urlaub H, Schmitt A, Mühlenhoff M, Stummeyer K, Schwarzer D, Gerardy-Schahn R, Ficner R (2010a) Crystal structure of an intramolecular chaperone mediating triple-β-helix folding. Nat Struct Mol Biol 17:210–215PubMedCrossRefGoogle Scholar
  150. Schulz EC, Schwarzer D, Frank M, Stummeyer K, Mühlenhoff M, Dickmanns A, Gerardy-Schahn R, Ficner R (2010b) Structural basis for the recognition and cleavage of polysialic acid by the bacteriophage K1F tailspike protein EndoNF. J Mol Biol 397:341–351PubMedCrossRefGoogle Scholar
  151. Sciara G, Bebeacua C, Bron P, Tremblay D, Ortiz-Lombardia M, Lichière J, van Heel M, Campanacci V, Moineau S, Cambillau C (2010) Structure of lactococcal phage p2 baseplate and its mechanism of activation. Proc Natl Acad Sci U S A 107:6852–6857PubMedPubMedCentralCrossRefGoogle Scholar
  152. Seul A, Müller JJ, Andres D, Stettner E, Heinemann U, Seckler R (2014) Bacteriophage P22 tailspike: structure of the complete protein and function of the interdomain linker. Acta Cryst D70:1336–1345Google Scholar
  153. Spinelli S, Desmyter A, Verrips CT, de Haard HJ, Moineau S (2006) Cambillau C (2006) Lactococcal bacteriophage p2 receptor-binding protein structure suggests a common ancestor gene with bacterial and mammalian viruses. Nat Struct Mol Biol 13:85–89PubMedCrossRefGoogle Scholar
  154. Stockley PG, White SJ, Dykeman E, Manfield I, Rolfsson O, Patel N, Bingham R, Barker A, Wroblewski E, Chandler-Bostock R, Weiss EU, Ranson NA, Tuma R, Twarock R (2016) Bacteriophage MS2 genomic RNA encodes an assembly instruction manual for its capsid. Bacteriophage 6:e1157666PubMedPubMedCentralCrossRefGoogle Scholar
  155. Su S, Gao YG, Zhang H, Terwilliger TC, Wang AH (1997) Analyses of the stability and function of three surface mutants (R82C, K69H, and L32R) of the gene V protein from Ff phage by X-ray crystallography. Protein Sci 6:771–780PubMedPubMedCentralCrossRefGoogle Scholar
  156. Suhanovsky MM, Teschke CM (2015) Nature’s favorite building block: deciphering folding and capsid assembly of proteins with the HK97-fold. Virology 479-480:487–497PubMedCrossRefGoogle Scholar
  157. Sun L, Young LN, Zhang X, Boudko SP, Fokine A, Zbornik E, Roznowski AP, Molineux IJ, Rossmann MG, Bentley A, Fane BA (2014) Icosahedral bacteriophage ϕX174 forms a tail for DNA transport during infection. Nature 505:432–435PubMedCrossRefGoogle Scholar
  158. Sun Z, El Omari K, Sun X, Ilca SL, Kotecha A, Stuart DI, Poranen MM, Huiskonen JT (2017) Double-stranded RNA virus outer shell assembly by bona fide domain-swapping. Nat Commun 8:14814PubMedPubMedCentralCrossRefGoogle Scholar
  159. Takata T, Haase-Pettingell C, King J (2012) The C-terminal cysteine annulus participates in auto-chaperone function for Salmonella phage P22 tailspike folding and assembly. Bacteriophage 2:36–49PubMedPubMedCentralCrossRefGoogle Scholar
  160. Tang J, Olson N, Jardine PJ, Grimes S, Anderson DL, Baker TS (2008) DNA poised for release in bacteriophage ϕ29. Structure 16:935–943PubMedPubMedCentralCrossRefGoogle Scholar
  161. Tang J, Lander GC, Olia A, Li R, Casjens S, Prevelige P, Cingolani G, Baker TS, Johnson JE (2011) Peering down the barrel of a bacteriophage portal: the genome packaging and release valve in P22. Structure 19:496–502PubMedPubMedCentralCrossRefGoogle Scholar
  162. Tao P, Mahalingam M, Zhu J, Moayeri M, Sha J, Lawrence WS, Leppla SH, Chopra AK, Rao VB (2018) A bacteriophage T4 nanoparticle-based dual vaccine against anthrax and plague. MBio 9:e01926-18PubMedPubMedCentralCrossRefGoogle Scholar
  163. Tavares P, Zinn-Justin S, Orlova EV (2012) Genome gating in tailed bacteriophage capsids. Adv Exp Med Biol 726:585–600PubMedCrossRefGoogle Scholar
  164. Taylor GL (2010) Introduction to phasing. Acta Cryst D66:325–338Google Scholar
  165. Taylor NM, Prokhorov NS, Guerrero-Ferreira RC, Shneider MM, Browning C, Goldie KN, Stahlberg H, Leiman PG (2016) Structure of the T4 baseplate and its function in triggering sheath contraction. Nature 533:346–352PubMedCrossRefGoogle Scholar
  166. Taylor NMI, van Raaij MJ, Leiman PG (2018) Contractile injection systems of bacteriophages and related systems. Mol Microbiol 108:6–15PubMedCrossRefGoogle Scholar
  167. Thiriot DS, Nevzorov AA, Zagyanskiy L, Wu CH, Opella SJ (2004) Structure of the coat protein in Pf1 bacteriophage determined by solid-state NMR spectroscopy. J Mol Biol 341:869–879PubMedCrossRefGoogle Scholar
  168. Thomassen E, Gielen G, Schütz M, Schoehn G, Abrahams JP, Miller S, van Raaij MJ (2003) The structure of the receptor-binding domain of the bacteriophage T4 short tail fibre reveals a knitted trimeric metal-binding fold. J Mol Biol 331:361–373PubMedCrossRefGoogle Scholar
  169. Tremblay DM, Tegoni M, Spinelli S, Campanacci V, Blangy S, Huyghe C, Desmyter A, Labrie S, Moineau S, Cambillau C (2006) Receptor-binding protein of Lactococcus lactis phages: identification and characterization of the saccharide receptor-binding site. J Bacteriol 188:2400–2410PubMedPubMedCentralCrossRefGoogle Scholar
  170. van Raaij MJ, Schoehn G, Burda MR, Miller S (2001) Crystal structure of a heat and protease-stable part of the bacteriophage T4 short tail fibre. J Mol Biol 314:1137–1146PubMedCrossRefGoogle Scholar
  171. Veesler D, Robin G, Lichière J, Auzat I, Tavares P, Bron P, Campanacci V, Cambillau C (2010) Crystal structure of bacteriophage SPP1 distal tail protein (gp19.1): a baseplate hub paradigm in gram-positive infecting phages. J Biol Chem 285:36666–36673PubMedPubMedCentralCrossRefGoogle Scholar
  172. Veesler D, Quispe J, Grigorieff N, Potter CS, Carragher B, Johnson JE (2012a) Maturation in action: CryoEM study of a viral capsid caught during expansion. Structure 20:1384–1390PubMedPubMedCentralCrossRefGoogle Scholar
  173. Veesler D, Spinelli S, Mahony J, Lichiere J, Blangy S, Bricogne G, Legrand P, Ortiz- Lombardia M, Campanacci V, van Sinderen D, Cambillau C (2012b) Structure of the phage TP901-1 1.8 MDa baseplate suggests an alternative host adhesion mechanism. Proc Natl Acad Sci U S A 109:8954–8958PubMedPubMedCentralCrossRefGoogle Scholar
  174. Vinga I, Baptista C, Auzat I, Petipas I, Lurz R, Tavares P, Santos MA, São-José C (2012) Role of bacteriophage SPP1 tail spike protein gp21 on host cell receptor binding and trigger of phage DNA ejection. Mol Microbiol 83:289–303PubMedCrossRefGoogle Scholar
  175. Walter M, Fiedler C, Grassl R, Biebl M, Rachel R, Hermo-Parrado XL, Llamas-Saiz AL, Seckler R, Miller S, van Raaij MJ (2008) Structure of the receptor-binding protein of bacteriophage Det7: a podoviral tail spike in a myovirus. J Virol 82:2265–2273PubMedCrossRefGoogle Scholar
  176. Wang YA, Yu X, Overman S, Tsuboi M, Thomas GJ, Egelman EH (2006) The structure of a filamentous bacteriophage. J Mol Biol 361:209–215PubMedCrossRefGoogle Scholar
  177. Xiang Y, Rossmann MG (2011) Structure of bacteriophage ϕ29 head fibers has a supercoiled triple repeating helix-turn-helix motif. Proc Natl Acad Sci U S A 108:4806–4810PubMedPubMedCentralCrossRefGoogle Scholar
  178. Xiang Y, Morais MC, Cohen DN, Bowman VD, Anderson DL, Rossmann MG (2008) Crystal and cryoEM structural studies of a cell wall degrading enzyme in the bacteriophage ϕ29 tail. Proc Natl Acad Sci U S A 105:9552–9557PubMedPubMedCentralCrossRefGoogle Scholar
  179. 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 34:375–386PubMedPubMedCentralCrossRefGoogle Scholar
  180. Xu L, Benson SD, Butcher SJ, Bamford DH, Burnett RM (2003) The receptor binding protein P2 of PRD1, a virus targeting antibiotic-resistant bacteria, has a novel fold suggesting multiple functions. Structure 11:309–322PubMedCrossRefGoogle Scholar
  181. Xu J, Hendrix RW, Duda RL (2014) Chaperone-protein interactions that mediate assembly of the bacteriophage λ tail to the correct length. J Mol Biol 426:1004–1018PubMedCrossRefGoogle Scholar
  182. Xu J, Gui M, Wang D, Xiang Y (2016) The bacteriophage ϕ29 tail possesses a pore-forming loop for cell membrane penetration. Nature 534:544–547PubMedCrossRefGoogle Scholar
  183. Yap ML, Rossmann MG (2014) Structure and function of bacteriophage T4. Future Microbiol 9:1319–1327PubMedPubMedCentralCrossRefGoogle Scholar
  184. Yutin N, Backstrom D, Ettema TJG, Krupovic M, Koonin EV (2018) Vast diversity of prokaryotic virus genomes encoding double jelly-roll major capsid proteins uncovered by genomic and metagenomic sequence analysis. Virol J 15:67PubMedPubMedCentralCrossRefGoogle Scholar
  185. Zheng W, Wang F, Taylor NMI, Guerrero-Ferreira RC, Leiman PG, Egelman EH (2017) Refined cryo-EM structure of the T4 tail tube: exploring the lowest dose limit. Structure 25:1436–1441PubMedPubMedCentralCrossRefGoogle Scholar
  186. Zimmer SG, Millette RL (1975) DNA-dependent RNA polymerase from Pseudomonas BAL-31. II. Transcription of the allomorphic forms of bacteriophage PM2 DNA. Biochemistry 14:300–307PubMedCrossRefGoogle Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Marta Sanz-Gaitero
    • 1
  • Mateo Seoane-Blanco
    • 1
  • Mark J. van Raaij
    • 1
    Email author
  1. 1.Department of Macromolecular StructureCentro Nacional de Biotecnologia (CNB-CSIC)MadridSpain

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