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Structure and Function of Bacteriophages

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Bacteriophages

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.

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References

  • 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 432:68–74

    Article  CAS  PubMed  Google Scholar 

  • 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 31:749–761

    Article  CAS  PubMed  Google Scholar 

  • Abrescia NG, Bamford DH, Grimes JM, Stuart DI (2012) Structure unifies the viral universe. Annu Rev Biochem 81:795–822

    Article  CAS  PubMed  Google Scholar 

  • Ackermann HW, Prangishvili D (2012) Prokaryote viruses studied by electron microscopy. Arch Virol 157:1843–1849

    Article  CAS  PubMed  Google Scholar 

  • Ageno M, Donelli G, Guglielmi F (1973) Structure and physico-chemical properties of bacteriophage G. II, the shape and symmetry of the capsid. Micron 4:376–403

    Google Scholar 

  • 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 28:821–829

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 17:800–808

    Article  CAS  PubMed  Google Scholar 

  • Arisaka F, Yap ML, Janamaru S, Rossmann MG (2016) Molecular assembly and structure of the bacteriophage T4 tail. Biophys Rev 8:385–396

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 8:1953

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bamford DH, Palva ET, Lounatmaa K (1976) Ultrastructure and life cycle of the lipid-containing bacteriophage ϕ6. J Gen Virol 32:249–259

    Article  CAS  PubMed  Google Scholar 

  • 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 190:4989–4996

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 70:116–121

    Article  PubMed  CAS  Google Scholar 

  • 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 107:20287–20292

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 285:39079–39086

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 325:11–24

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bernhardt TG, Wang IN, Struck DK, Young R (2001) A protein antibiotic in the phage Qβ virion: diversity in lysis targets. Science 292:2326–2327

    Article  CAS  PubMed  Google Scholar 

  • Bhardwaj A, Molineux IJ, Casjens SR, Cingolani G (2011) Atomic structure of bacteriophage Sf6 tail needle knob. J Biol Chem 286:30867–30877

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bhardwaj A, Olia AS, Cingolani G (2014) Architecture of viral genome-delivery molecular machines. Curr Opin Struct Biol 25:1–8

    Article  CAS  PubMed  Google Scholar 

  • Black LW, Thomas JA (2012) Condensed genome structure. Adv Exp Med Biol 726:469–487

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bollback JP, Huelsenbeck JP (2001) Phylogeny, genome evolution, and host specificity of single-stranded RNA bacteriophage (family Leviviridae). J Mol Evol 52:117–128

    Article  CAS  PubMed  Google Scholar 

  • 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 269:833–841

    Article  CAS  PubMed  Google Scholar 

  • Boudko SP, Strelkov SV, Engel J, Stetefeld J (2004) Design and crystal structure of bacteriophage T4 mini-fibritin NCCF. J Mol Biol 339:927–935

    Article  CAS  PubMed  Google Scholar 

  • Brewer GJ (1978) Membrane-localized replication of bacteriophage PM2. Virology 84:242–245

    Article  CAS  PubMed  Google Scholar 

  • Browning C, Shneider MM, Bowman VD, Schwarzer D, Leiman PG (2012) Phage pierces the host cell membrane with the iron-loaded spike. Structure 20:326–339

    Article  CAS  PubMed  Google Scholar 

  • Butcher SJ, Manole V, Karhu NJ (2012) Lipid-containing viruses: bacteriophage PRD1 assembly. Adv Exp Med Biol 726:365–377

    Article  CAS  PubMed  Google Scholar 

  • 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 113:10174–10179

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Caldentey J, Bamford DH (1992) The lytic enzyme of the Pseudomonas phage ϕ6. Purification and biochemical characterization. Biochim Biophys Acta 1159:44–50

    Article  CAS  PubMed  Google Scholar 

  • Canelo E, Phillips OM, del Roure RN (1985) Relating cistrons and functions in bacteriophage PM2. Virology 140:364–367

    Article  CAS  PubMed  Google Scholar 

  • Casjens S, King J (1975) Virus assembly. Annu Rev Biochem 44:555–611

    Article  CAS  PubMed  Google Scholar 

  • Casjens SR, Molineux IJ (2012) Short noncontractile tail machines: adsorption and DNA delivery by podoviruses. Adv Exp Med Biol 726:143–179

    Article  CAS  PubMed  Google Scholar 

  • Caspar DL, Klug A (1962) Physical principles in the construction of regular viruses. Cold Spring Harb Symp Quant Biol 27:1–24

    Article  CAS  PubMed  Google Scholar 

  • 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 112:7009–7014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 6:135–145

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 378:726–736

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 432:122–125

    Article  CAS  PubMed  Google Scholar 

  • 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 288:26290–26299

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 541:112–116

    Article  CAS  PubMed  Google Scholar 

  • Davidson AR, Cardarelli L, Pell LG, Radford DR, Maxwell KL (2012) Long noncontractile tail machines of bacteriophages. Adv Exp Med Biol 726:115–142

    Article  CAS  PubMed  Google Scholar 

  • Doore SM, Fane BA (2016) The Microviridae: diversity, assembly, and experimental evolution. Virology 461:45–55

    Article  CAS  Google Scholar 

  • 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 26:1573–1582

    Article  CAS  PubMed  Google Scholar 

  • 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 41:9396–9410

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 21:1384–1395

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Espejo RT, Canelo ES, Sinsheimer RL (1969) DNA of bacteriophage PM2: a closed circular double-stranded molecule. Proc Natl Acad Sci U S A 63:1164–1168

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Farley MM, Tu J, Kearns DB, Molineaux IJ, Liu J (2017) Ultrastructural analysis of bacteriophage ϕ29 during infection of Bacillus subtilis. J Struct Biol 197:163–171

    Article  CAS  PubMed  Google Scholar 

  • Feng JN, Model P, Russel M (1999) A trans-envelope protein complex needed for filamentous phage assembly and export. Mol Microbiol 34:745–755

    Article  CAS  PubMed  Google Scholar 

  • 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 260:500–507

    Article  CAS  PubMed  Google Scholar 

  • 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 88:820–828

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fokine A, Rossmann MG (2014) Molecular architecture of tailed double-stranded DNA phages. Bacteriophage 4:e28281

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 101:6003–6008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 85:8141–8148

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 425:1731–1744

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 246:418–428

    Article  CAS  PubMed  Google Scholar 

  • 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 109:9390–9395

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Garcia-Doval C, van Raaij MJ (2013) Bacteriophage receptor recognition and nucleic acid transfer. Subcell Biochem 68:489–518

    Article  CAS  PubMed  Google Scholar 

  • 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 7:6424–6440

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Golmohammadi R, Valegard K, Fridborg K, Liljas L (1993) The refined structure of bacteriophage MS2 at 2.8 Å resolution. J Mol Biol 234:620–639

    Article  CAS  PubMed  Google Scholar 

  • Golmohammadi R, Fridborg K, Bundule M, Valegard K, Liljas L (1996) The crystal structure of bacteriophage Qβ at 3.5 Å resolution. Structure 4:543–554

    Article  CAS  PubMed  Google Scholar 

  • 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 290:10038–10044

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 113:11519–11524

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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:E168

    Article  PubMed  CAS  Google Scholar 

  • 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:e99455

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • 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 174:1462–1477

    Article  PubMed  PubMed Central  Google Scholar 

  • Henderson R (2015) Overview and future of single particle electron cryomicroscopy. Arch Biochem Biophys 581:19–24

    Article  CAS  PubMed  Google Scholar 

  • 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 94:2909–2914

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 23–48

    Chapter  Google Scholar 

  • 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 288:649–657

    Article  CAS  PubMed  Google Scholar 

  • 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:e1002024

    Article  PubMed  PubMed Central  Google Scholar 

  • Hu GB, Wei H, Rice WJ, Stokes DL, Paul Gottlieb P (2008) Electron cryo-tomographic structure of cystovirus ϕ12. Virology 372:1–9

    Article  CAS  PubMed  Google Scholar 

  • Hu B, Margolin W, Molineaux IJ, Liu J (2013) The bacteriophage T7 virion undergoes extensive structural remodeling during infection. Science 339:577–579

    Article  CAS  Google Scholar 

  • 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–E4928

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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:e01579-01517

    Article  Google Scholar 

  • 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 11:850–856

    Article  CAS  PubMed  Google Scholar 

  • Huiskonen JT, Manole V, Butcher SJ (2007) Tale of two spikes in bacteriophage PRD1. Proc Natl Acad Sci U S A 104:6666–6671

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hyman P, van Raaij MJ (2018) Bacteriophage T4 long tail fiber domains. Biophys Rev 10:463–471

    Article  CAS  PubMed  Google Scholar 

  • 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 226:221–227

    Article  CAS  PubMed  Google Scholar 

  • Jäälinoja HT, Huiskonen JT, Butcher SJ (2007) Electron cryomicroscopy comparison of the architectures of the enveloped bacteriophages ϕ6 and ϕ8. Structure 15:157–167

    Article  PubMed  CAS  Google Scholar 

  • Johnson JE, Speir JA (1997) Quasi-equivalent viruses: a paradigm for protein assemblies. J Mol Biol 269:665–675

    Article  CAS  PubMed  Google Scholar 

  • 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 415:553–557

    Article  CAS  PubMed  Google Scholar 

  • 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 185:2628–2634

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Katsura I (1990) Mechanism of length determination in bacteriophage lambda tails. Adv Biophys 26:1–18

    Article  CAS  PubMed  Google Scholar 

  • Kikuchi Y, King J (1975) Assembly of the tail of bacteriophage T4. J Supramol Struct 3:24–38

    Article  CAS  PubMed  Google Scholar 

  • 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 262:364–374

    Article  PubMed  Google Scholar 

  • Kivelä HM, Kalkkinen N, Bamford DH (2002) Bacteriophage PM2 has a protein capsid surrounding a spherical proteinaceous lipid core. J Virol 76:8169–8178

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 186:5342–5354

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 161:204–210

    Article  PubMed  CAS  Google Scholar 

  • 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 6:27581

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Korasick DA, Tanner JJ (2018) Determination of protein oligomeric structure from small-angle X-ray scattering. Protein Sci 27:814–824

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 7:1213–1222

    Article  CAS  PubMed  Google Scholar 

  • 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 12:810–813

    Article  CAS  PubMed  Google Scholar 

  • Krupovic M, Daugelavicius R, Bamford DH (2007) A novel lysis system in PM2, a lipid-containing marine double-stranded DNA bacteriophage. Mol Microbiol 64:1635–1648

    Article  CAS  PubMed  Google Scholar 

  • 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 160:952–962

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kühlbrandt W (2014) Cryo-EM enters a new era. elife 3:e03678

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 9:224

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Leiman PG (2018) Stretching the arms of the type VI secretion sheath protein. EMBO Rep 19:191–193

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leiman PG, Shneider MM (2012) Contractile tail machines of bacteriophages. Adv Exp Med Biol 726:93–114

    Article  CAS  PubMed  Google Scholar 

  • 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 301:975–985

    Article  CAS  PubMed  Google Scholar 

  • 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 118:419–429

    Article  CAS  PubMed  Google Scholar 

  • Leiman PG, Shneider MM, Mesyanzhinov VV, Rossmann MG (2006) Evolution of bacteriophage tails: structure of T4 gene product 10. J Mol Biol 358:912–921

    Article  CAS  PubMed  Google Scholar 

  • 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 371:836–849

    Article  CAS  PubMed  Google Scholar 

  • 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 7:355

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 106:8507–8512

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 6:26455

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu Y, Eisenberg D (2002) 3D domain swapping: as domains continue to swap. Protein Sci 11:1285–1299

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 17:830–836

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 3–22

    Google Scholar 

  • 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 276:9009–9015

    Article  CAS  PubMed  Google Scholar 

  • 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 7:711–722

    Article  CAS  PubMed  Google Scholar 

  • 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:e1123795

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 262:355–336

    Article  PubMed  Google Scholar 

  • 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 163:1117–1124

    Article  PubMed  CAS  Google Scholar 

  • Marvin DA (1998) Filamentous phage structure, infection and assembly. Curr Opin Struct Biol 8:150–158

    Article  CAS  PubMed  Google Scholar 

  • Marvin DA (2017) Fibre diffraction studies of biological macromolecules. Prog Biophys Mol Biol 127:43–87

    Article  CAS  PubMed  Google Scholar 

  • 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 355:294–309

    Article  CAS  PubMed  Google Scholar 

  • Marvin DA, Symmons MF, Straus SK (2014) Structure and assembly of filamentous bacteriophages. Prog Biophys Mol Biol 114:80–122

    Article  CAS  PubMed  Google Scholar 

  • 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 308:9–14

    Article  CAS  PubMed  Google Scholar 

  • 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 318:1395–1404

    Article  CAS  PubMed  Google Scholar 

  • 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 18:161–170

    Article  CAS  PubMed  Google Scholar 

  • Mitraki A, Papanikolopoulou K, van Raaij MJ (2006) Natural triple β-stranded fibrous folds. Adv Protein Chem 73:97–124

    Article  CAS  PubMed  Google Scholar 

  • Moak M, Molineux IJ (2004) Peptidoglycan hydrolytic activities associated with bacteriophage virions. Mol Microbiol 51:1169–1183

    Article  CAS  PubMed  Google Scholar 

  • 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 18:149–159

    Article  CAS  PubMed  Google Scholar 

  • 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 45:499–511

    Article  CAS  PubMed  Google Scholar 

  • 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 374:817–836

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 21:1374–1383

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 3:255–263

    Article  CAS  PubMed  Google Scholar 

  • 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 113:9351–9356

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Olia AS, Casjens S, Cingolani G (2007) Structure of phage P22 cell envelope–penetrating needle. Nat Struct Mol Biol 14:1221–1226

    Article  CAS  PubMed  Google Scholar 

  • Olia AS, Prevelige PE, Johnson JE, Cingolani G (2011) Three-dimensional structure of a viral genome-delivery portal vertex. Nat Struct Mol Biol 18:597–603

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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:e0188858

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    Article  PubMed Central  CAS  Google Scholar 

  • 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 389:938–951

    Article  CAS  PubMed  Google Scholar 

  • 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 106:4160–4165

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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):468–479

    Article  CAS  PubMed  Google Scholar 

  • 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 165:103–114

    Article  CAS  PubMed  Google Scholar 

  • 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 86:358–363

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 25:1605–1612

    Article  CAS  PubMed  Google Scholar 

  • 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 10:39

    Article  PubMed Central  CAS  Google Scholar 

  • Plevka P, Tars K, Liljas L (2008) Crystal packing of a bacteriophage MS2 coat protein mutant corresponds to octahedral particles. Protein Sci 17:1731–1739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Poranen MM, Tuma R (2004) Self-assembly of double-stranded RNA bacteriophages. Virus Res 101:93–100

    Article  CAS  PubMed  Google Scholar 

  • Prasad BV, Schmid MF (2012) Principles of virus structural organization. Adv Exp Med Biol 726:17–47

    Article  CAS  PubMed  Google Scholar 

  • Prevelige PE, Cortines JR (2018) Phage assembly and the special role of the portal protein. Curr Opin Virol 31:66–73

    Article  CAS  PubMed  Google Scholar 

  • Prevelige PE, Fane BA (2012) Building the machines: scaffolding proteins functions during bacteriophage morphogenesis. Adv Exp Med Biol 726:325–350

    Article  CAS  PubMed  Google Scholar 

  • Rakonjac J, Bennett NJ, Spagnuolo J, Gagic D, Russel M (2011) Filamentous bacteriophage: biology, phage display and nanotechnology applications. Curr Issues Mol Biol 13:51–57

    CAS  PubMed  Google Scholar 

  • Rakonjac J, Russel M, Khanum S, Brooke SJ, Rajič M (2017) Filamentous phage: structure and biology. Adv Exp Med Biol 1053:1–20

    Article  CAS  PubMed  Google Scholar 

  • Rao VB, Feiss M (2015) Mechanisms of DNA packaging by large double-stranded DNA viruses. Annu Rev Virol 9:351–378

    Article  CAS  Google Scholar 

  • 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 24:1352–1363

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 426:1039–1049

    Article  CAS  PubMed  Google Scholar 

  • Russel M, Linderoth NA, Sali A (1997) Filamentous phage assembly: variation on a protein export theme. Gene 192:23–32

    Article  CAS  PubMed  Google Scholar 

  • Santos-Pérez I, Oksanen HM, Bamford DH, Goñi FM, Reguera D, Abrescia NGA (2017) Membrane-assisted viral DNA ejection. Biochim Biophys Acta 1861:664–672

    Article  CAS  Google Scholar 

  • 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 17:210–215

    Article  CAS  PubMed  Google Scholar 

  • 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 397:341–351

    Article  CAS  PubMed  Google Scholar 

  • 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 107:6852–6857

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 D70:1336–1345

    Google Scholar 

  • 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 13:85–89

    Article  CAS  PubMed  Google Scholar 

  • 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:e1157666

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 6:771–780

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suhanovsky MM, Teschke CM (2015) Nature’s favorite building block: deciphering folding and capsid assembly of proteins with the HK97-fold. Virology 479-480:487–497

    Article  CAS  PubMed  Google Scholar 

  • 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 505:432–435

    Article  CAS  PubMed  Google Scholar 

  • 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 8:14814

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 2:36–49

    Article  PubMed  PubMed Central  Google Scholar 

  • Tang J, Olson N, Jardine PJ, Grimes S, Anderson DL, Baker TS (2008) DNA poised for release in bacteriophage ϕ29. Structure 16:935–943

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 19:496–502

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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:e01926-18

    Article  PubMed  PubMed Central  Google Scholar 

  • Tavares P, Zinn-Justin S, Orlova EV (2012) Genome gating in tailed bacteriophage capsids. Adv Exp Med Biol 726:585–600

    Article  CAS  PubMed  Google Scholar 

  • Taylor GL (2010) Introduction to phasing. Acta Cryst D66:325–338

    Google Scholar 

  • 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 533:346–352

    Article  CAS  PubMed  Google Scholar 

  • Taylor NMI, van Raaij MJ, Leiman PG (2018) Contractile injection systems of bacteriophages and related systems. Mol Microbiol 108:6–15

    Article  CAS  PubMed  Google Scholar 

  • 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 341:869–879

    Article  CAS  PubMed  Google Scholar 

  • 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 331:361–373

    Article  CAS  PubMed  Google Scholar 

  • 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 188:2400–2410

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 314:1137–1146

    Article  PubMed  CAS  Google Scholar 

  • 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 285:36666–36673

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 20:1384–1390

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 109:8954–8958

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 83:289–303

    Article  CAS  PubMed  Google Scholar 

  • 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 82:2265–2273

    Article  CAS  PubMed  Google Scholar 

  • Wang YA, Yu X, Overman S, Tsuboi M, Thomas GJ, Egelman EH (2006) The structure of a filamentous bacteriophage. J Mol Biol 361:209–215

    Article  CAS  PubMed  Google Scholar 

  • 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 108:4806–4810

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 105:9552–9557

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 34:375–386

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 11:309–322

    Article  CAS  PubMed  Google Scholar 

  • 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 426:1004–1018

    Article  CAS  PubMed  Google Scholar 

  • Xu J, Gui M, Wang D, Xiang Y (2016) The bacteriophage ϕ29 tail possesses a pore-forming loop for cell membrane penetration. Nature 534:544–547

    Article  CAS  PubMed  Google Scholar 

  • Yap ML, Rossmann MG (2014) Structure and function of bacteriophage T4. Future Microbiol 9:1319–1327

    Article  CAS  PubMed  Google Scholar 

  • 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 15:67

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 25:1436–1441

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zimmer SG, Millette RL (1975) DNA-dependent RNA polymerase from Pseudomonas BAL-31. II. Transcription of the allomorphic forms of bacteriophage PM2 DNA. Biochemistry 14:300–307

    Article  CAS  PubMed  Google Scholar 

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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.

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Sanz-Gaitero, M., Seoane-Blanco, M., van Raaij, M.J. (2019). Structure and Function of Bacteriophages. In: Harper, D., Abedon, S., Burrowes, B., McConville, M. (eds) Bacteriophages. Springer, Cham. https://doi.org/10.1007/978-3-319-40598-8_1-1

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