Abstract
Tailed dsDNA bacteriophage virions bind to susceptible cells with the tips of their tails and then deliver their DNA through the tail into the cells to initiate infection. This chapter discusses what is known about this process in the short-tailed phages (Podoviridae). Their short tails require that many of these virions adsorb to the outer layers of the cell and work their way down to the outer membrane surface before releasing their DNA. Interestingly, the receptor-binding protein of many short-tailed phages (and some with long tails) has an enzymatic activity that cleaves their polysaccharide receptors. Reversible adsorption and irreversible adsorption to primary and secondary receptors are discussed, including how sequence divergence in tail fiber and tailspike proteins leads to different host specificities. Upon reaching the outer membrane of Gram-negative cells, some podoviral tail machines release virion proteins into the cell that help the DNA efficiently traverse the outer layers of the cell and/or prepare the cell cytoplasm for phage genome arrival. Podoviruses utilize several rather different variations on this theme. The virion DNA is then released into the cell; the energetics of this process is discussed. Phages like T7 and N4 deliver their DNA relatively slowly, using enzymes to pull the genome into the cell. At least in part this mechanism ensures that genes in late-entering DNA are not expressed at early times. On the other hand, phages like P22 probably deliver their DNA more rapidly so that it can be circularized before the cascade of gene expression begins.
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Adam G, Delbrück M (1968) Reduction in dimensionality in biological diffusion processes. In: Rich A, Davidson N (eds) Structural chemisty and molecular biology. W. H. Freeman and Company, San Francisco, pp 198–215
Agirrezabala X, Martin-Benito J, Caston JR, Miranda R, Valpuesta JM, Carrascosa JL (2005) Maturation of phage T7 involves structural modification of both shell and inner core components. EMBO J 24:3820–3829
Agirrezabala X, Velazquez-Muriel JA, Gomez-Puertas P, Scheres SH, Carazo JM, Carrascosa JL (2007) Quasi-atomic model of bacteriophage T7 procapsid shell: insights into the structure and evolution of a basic fold. Structure 15:461–472
Alcorlo M, Gonzalez-Huici V, Hermoso JM, Meijer WJ, Salas M (2007) The phage φ29 membrane protein p16.7, involved in DNA replication, is required for efficient ejection of the viral genome. J Bacteriol 189:5542–5549
Allison GE, Verma NK (2000) Serotype-converting bacteriophages and O-antigen modification in Shigella flexneri. Trends Microbiol 8:17–23
Anand VS, Patel SS (2006) Transient state kinetics of transcription elongation by T7 RNA polymerase. J Biol Chem 281:35677–35685
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 285:36768–36775
Astumian RD (1997) Thermodynamics and kinetics of a Brownian motor. Science 276:917–922
Bandyopadhyay PN, Das Gupta B, Joshi A, Chakravorty M (1979) Is the injection of DNA enough to cause bacteriophage P22-induced changes in the cellular transport process of Salmonella typhimurium? J Virol 32:98–101
Baptista C, Santos MA, Sao-Jose 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
Barbirz S, Muller JJ, Uetrecht C, Clark AJ, Heinemann U, Seckler R (2008) Crystal structure of Escherichia coli phage HK620 tailspike: podoviral tailspike endoglycosidase modules are evolutionarily related. Mol Microbiol 69:303–316
Baumann RG, Mullaney J, Black LW (2006) Portal fusion protein constraints on function in DNA packaging of bacteriophage T4. Mol Microbiol 61:16–32
Baxa U, Steinbacher S, Miller S, Weintraub A, Huber R, Seckler R (1996) Interactions of phage P22 tails with their cellular receptor, Salmonella O-antigen polysaccharide. Biophys J 71:2040–2048
Bayer M, Iberer R, Bischof K, Rassi E, Stabentheiner E, Zellnig G, Koraimann G (2001) Functional and mutational analysis of p19, a DNA transfer protein with muramidase activity. J Bacteriol 183:3176–3183
Bayer ME, Thurow H, Bayer MH (1979) Penetration of the polysaccharide capsule of Escherichia coli (Bi161/42) by bacteriophage K29. Virology 94:95–118
Bayer ME, Takeda K, Uetake H (1980) Effects of receptor destruction by Salmonella bacteriophages epsilon 15 and c341. Virology 105:328–337
Bayer ME, Bayer MH (1981) Fast responses of bacterial membranes to virus adsorption: a fluorescence study. Proc Natl Acad Sci USA 78:5618–5622
Benson NR, Roth J (1997) A Salmonella phage-P22 mutant defective in abortive transduction. Genetics 145:17–27
Berg HC, Purcell EM (1977) Physics of chemoreception. Biophys J 20:193–219
Berget PB, Poteete AR (1980) Structure and functions of the bacteriophage P22 tail protein. J Virol 34:234–243
Bhardwaj A, Olia AS, Walker-Kopp N, Cingolani G (2007) Domain organization and polarity of tail needle gp26 in the portal vertex structure of bacteriophage P22. J Mol Biol 371:374–387
Bienkowska-Szewczyk K, Taylor A (1980) Murein transglycosylase from phage lambda lysate. Purification and properties. Biochim Biophys Acta 615:489–496
Botstein D, Waddell CH, King J (1973) Mechanism of head assembly and DNA encapsulation in Salmonella phage P22. I. Genes, proteins, structures and DNA maturation. J Mol Biol 80:669–695
Bradley DE (1967) Ultrastructure of bacteriophage and bacteriocins. Bacteriol Rev 31:230–314
Bull JJ, Vimr ER, Molineux IJ (2010) A tale of tails: Sialidase is key to success in a model of phage therapy against K1-capsulated Escherichia coli. Virology 398:79–86
Canchaya C, Desiere F, McShan WM, Ferretti JJ, Parkhill J, Brussow H (2002) Genome analysis of an inducible prophage and prophage remnants integrated in the Streptococcus pyogenes strain SF370. Virology 302:245–258
Cardarelli L, Lam R, Tuite A, Baker LA, Sadowski PD, Radford DR, Rubinstein JL, Battaile KP, Chirgadze N, Maxwell KL, Davidson AR (2010) The crystal structure of bacteriophage HK97 gp6: defining a large family of head-tail connector proteins. J Mol Biol 395:754–768
Casjens S, King J (1974) P22 morphogenesis. I: Catalytic scaffolding protein in capsid assembly. J Supramol Struct 2:202–224
Casjens S, Wyckoff E, Hayden M, Sampson L, Eppler K, Randall S, Moreno E, Serwer P (1992) Bacteriophage P22 portal protein is part of the gauge that regulates packing density of intravirion DNA. J Mol Biol 224:1055–1074
Casjens S, Thuman-Commike P (2011) Evolution of mosaically related tailed phage genomes seen through the lens of phage P22 virion assembly. Virology 411:393–415
Cerritelli ME, Cheng N, Rosenberg AH, McPherson CE, Booy FP, Steven AC (1997) Encapsidated conformation of bacteriophage T7 DNA. Cell 91:271–280
Chang CY, Kemp P, Molineux IJ (2010) Gp15 and gp16 cooperate in translocating bacteriophage T7 DNA into the infected cell. Virology 398:176–186
Chang J, Weigele P, King J, Chiu W, Jiang W (2006) Cryo-EM asymmetric reconstruction of bacteriophage P22 reveals organization of its DNA packaging and infecting machinery. Structure 14:1073–1082
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
Chopin A, Deveau H, Ehrlich SD, Moineau S, Chopin MC (2007) KSY1, a lactococcal phage with a T7-like transcription. Virology 365:1–9
Cohen DN, Erickson SE, Xiang Y, Rossmann MG, Anderson DL (2008) Multifunctional roles of a bacteriophage φ29 morphogenetic factor in assembly and infection. J Mol Biol 378:804–817
Comolli LR, Spakowitz AJ, Siegerist CE, Jardine PJ, Grimes S, Anderson DL, Bustamante C, Downing KH (2008) Three-dimensional architecture of the bacteriophage φ29 packaged genome and elucidation of its packaging process. Virology 371:267–277
Dai W, Hodes A, Hui WH, Gingery M, Miller JF, Zhou ZH (2010) Three-dimensional structure of tropism-switching Bordetella bacteriophage. Proc Natl Acad Sci USA 107:4347–4352
de Frutos M, Letellier L, Raspaud E (2005) DNA ejection from bacteriophage T5: analysis of the kinetics and energetics. Biophys J 88:1364–1370
Dobbins AT, George M Jr, Basham DA, Ford ME, Houtz JM, Pedulla ML, Lawrence JG, Hatfull GF, Hendrix RW (2004) Complete genomic sequence of the virulent Salmonella bacteriophage SP6. J Bacteriol 186:1933–1944
Doulatov S, Hodes A, Dai L, Mandhana N, Liu M, Deora R, Simons RW, Zimmerly S, Miller JF (2004) Tropism switching in Bordetella bacteriophage defines a family of diversity-generating retroelements. Nature 431:476–481
Drexler K, Dannull J, Hindennach I, Mutschler B, Henning U (1991) Single mutations in a gene for a tail fiber component of an Escherichia coli phage can cause an extension from a protein to a carbohydrate as a receptor. J Mol Biol 219:655–663
Earnshaw W, Casjens S (1980) DNA packaging by the double-stranded DNA bacteriophages. Cell 21:319–331
Ebel-Tsipis J, Botstein D (1971) Superinfection exclusion by P22 prophage in lysogens of Salmonella typhimurium. 1. Exclusion of generalized transducing particles. Virology 45:629–637
Effantin G, Boulanger P, Neumann E, Letellier L, Conway JF (2006) Bacteriophage T5 structure reveals similarities with HK97 and T4 suggesting evolutionary relationships. J Mol Biol 361:993–1002
Emrich J, Streisinger G (1968) The role of phage lysozyme in the life cycle of phage T4. Virology 36:387–391
Evilevitch A, Lavelle L, Knobler CM, Raspaud E, Gelbart WM (2003) Osmotic pressure inhibition of DNA ejection from phage. Proc Natl Acad Sci USA 100:9292–9295
Falco SC, Laan KV, Rothman-Denes LB (1977) Virion-associated RNA polymerase required for bacteriophage N4 development. Proc Natl Acad Sci USA 74:520–523
Falco SC, Zehring W, Rothman-Denes LB (1980) DNA-dependent RNA polymerase from bacteriophage N4 virions. Purification and characterization. J Biol Chem 255:4339–4347
Feynman RP (1963) The Feynman lectures on physics. Addison-Wesley, Reading, MA
Filali Maltouf A, Labedan B (1983) Host cell metabolic energy is not required for injection of bacteriophage T5 DNA. J Bacteriol 153:124–133
Filali Maltouf AK, Labedan B (1985) The energetics of the injection process of bacteriophage lambda DNA and the role of the ptsM/pel-encoded protein. Biochem Biophys Res Commun 130:1093–1101
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 USA 101:6003–6008
Fraser JS, Yu Z, Maxwell KL, Davidson AR (2006) Ig-like domains on bacteriophages: a tale of promiscuity and deceit. J Mol Biol 359:496–507
Garcia L, Molineux I (1995) Incomplete entry of bacteriophage T7 DNA into F plasmid-containing Escherichia coli. J Bacteriol 177:4077–4083
Garcia LR, Molineux IJ (1996) Transcription-independent DNA translocation of bacteriophage T7 DNA into Escherichia coli. J Bacteriol 178:6921–6929
Garcia LR, Molineux IJ (1999) Translocation and specific cleavage of bacteriophage T7 DNA in vivo by EcoKI. Proc Natl Acad Sci USA 96:12430–12435
George DG, Yeh LS, Barker WC (1983) Unexpected relationships between bacteriophage lambda hypothetical proteins and bacteriophage T4 tail-fiber proteins. Biochem Biophys Res Commun 115:1061–1068
Goldberg EB, Grinius L, Letellier L (1994) Recognition, attachment and injection. In: Karam J (ed) The molecular biology of bacteriophage T4. ASM Press, Washiington, DC, pp 347–356
Gonzalez-Huici V, Alcorlo M, Salas M, Hermoso JM (2004a) Binding of phage φ29 architectural protein p6 to the viral genome: evidence for topological restriction of the phage linear DNA. Nucleic Acids Res 32:3493–3502
Gonzalez-Huici V, Salas M, Hermoso JM (2004b) The push-pull mechanism of bacteriophage φ29 DNA injection. Mol Microbiol 52:529–540
Gonzalez-Huici V, Salas M, Hermoso JM (2006) Requirements for Bacillus subtilis bacteriophage φ29 DNA ejection. Gene 374:19–25
Grayson P, Evilevitch A, Inamdar MM, Purohit PK, Gelbart WM, Knobler CM, Phillips R (2006) The effect of genome length on ejection forces in bacteriophage lambda. Virology 348:430–436
Grayson P, Han L, Winther T, Phillips R (2007) Real-time observations of single bacteriophage lambda DNA ejections in vitro. Proc Natl Acad Sci USA 104:14652–14657
Grayson P, Molineux IJ (2007) Is phage DNA ‘injected’ into cells – biologists and physicists can agree. Curr Opin Microbiol 10:401–409
Haggard-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
Hanfling P, Shashkov AS, Jann B, Jann K (1996) Analysis of the enzymatic cleavage (beta elimination) of the capsular K5 polysaccharide of Escherichia coli by the K5-specific coliphage: reexamination. J Bacteriol 178:4747–4750
Haynes LL, Rothman-Denes LB (1985) N4 virion RNA polymerase sites of transcription initiation. Cell 41:597–605
Heller K, Braun V (1979) Accelerated adsorption of bacteriophage T5 to Escherichia coli F, resulting from reversible tail fiber-lipopolysaccharide binding. J Bacteriol 139:32–38
Hendrix R, Casjens S (2005) Podoviridae. In: Fauquet C, Mayo M, Maniloff J, Desselberger U, Ball A (eds) Virus taxonomy. Elsevier, Amsterdam, pp 71–79
Hendrix RW, Duda RL (1992) Bacteriophage lambda PaPa: not the mother of all lambda phages. Science 258:1145–1148
Hershey AD, Chase M (1952) Independent functions of viral protein and nucleic acid in growth of bacteriophge. J Gen Physiol 36:39–56
Hershey AD (1955) An upper limit to the protein content of the germinal substance of bacteriophage T2. Virology 1:108–127
Hofer B, Ruge M, Dreiseikelmann B (1995) The superinfection exclusion gene (sieA) of bacteriophage P22: identification and overexpression of the gene and localization of the gene product. J Bacteriol 177:3080–3086
Hoffman B, Levine M (1975a) Bacteriophage P22 virion protein which performs an essential early function. I. Analysis of 16-ts mutants. J Virol 16:1536–1546
Hoffman B, Levine M (1975b) Bacteriophage P22 virion protein which performs an essential early function. II. Characterization of the gene 16 function. J Virol 16:1547–1559
Hud NV, Downing KH (2001) Cryoelectron microscopy of lambda phage DNA condensates in vitreous ice: the fine structure of DNA toroids. Proc Natl Acad Sci USA 98:14925–14930
Hugel T, Michaelis J, Hetherington CL, Jardine PJ, Grimes S, Walter JM, Falk W, Anderson DL, Bustamante C (2007) Experimental test of connector rotation during DNA packaging into bacteriophage φ29 capsids. PLoS Biol 5:e59
Isidro A, Santos MA, Henriques AO, Tavares P (2004) The high-resolution functional map of bacteriophage SPP1 portal protein. Mol Microbiol 51:949–962
Israel V (1976) Role of the bacteriophage P22 tail in the early stages of infection. J Virol 18:361–364
Israel V (1977) E proteins of bacteriophage P22. I. Identification and ejection from wild-type and defective particles. J Virol 23:91–97
Israel V (1978) A model for the adsorption of phage P22 to Salmonella typhimurium. J Gen Virol 40:669–673
Iwashita S, Kanegasaki S (1976) Deacetylation reaction catalyzed by Salmonella phage c341 and its baseplate parts. J Biol Chem 251:5361–5365
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 395:1079–1087
Jiang W, Li Z, Zhang Z, Baker ML, Prevelige PE Jr, Chiu W (2003) Coat protein fold and maturation transition of bacteriophage P22 seen at subnanometer resolutions. Nat Struct Biol 10:131–135
Jiang W, Chang J, Jakana J, Weigele P, King J, Chiu W (2006) Structure of epsilon15 bacteriophage reveals genome organization and DNA packaging/injection apparatus. Nature 439:612–616
Jiang W, Baker ML, Jakana J, Weigele PR, King J, Chiu W (2008) Backbone structure of the infectious epsilon15 virus capsid revealed by electron cryomicroscopy. Nature 451:1130–1134
Johnson JE, Chiu W (2007) DNA packaging and delivery machines in tailed bacteriophages. Curr Opin Struct Biol 17:237–243
Joshi A, Siddiqi JZ, Rao GR, Chakravorty M (1982) MB78, a virulent bacteriophage of Salmonella typhimurium. J Virol 41:1038–1043
Kanamaru S, Gassner NC, Ye N, Takeda S, Arisaka F (1999) The C-terminal fragment of the precursor tail lysozyme of bacteriophage T4 stays as a structural component of the baseplate after cleavage. J Bacteriol 181:2739–2744
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
Kanegasaki S, Wright A (1973) Studies on the mechanism of phage adsorption: interaction between phage epsilon15 and its cellular receptor. Virology 52:160–173
Kazmierczak K, Rothman-Denes L (2006) Bacteriophage N4. In: Calendar R (ed) The bacteriophages. Oxford University Press, Oxford, pp 302–314
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 21:5815–5823
Kemp P, Gupta M, Molineux IJ (2004) Bacteriophage T7 DNA ejection into cells is initiated by an enzyme-like mechanism. Mol Microbiol 53:1251–1265
Kemp P, Garcia LR, Molineux IJ (2005) Changes in bacteriophage T7 virion structure at the initiation of infection. Virology 340:307–317
Kiino DR, Rothman-Denes LB (1989) Genetic analysis of bacteriophage N4 adsorption. J Bacteriol 171:4595–4602
Kiino DR, Licudine R, Wilt K, Yang DH, Rothman-Denes LB (1993a) A cytoplasmic protein, NfrC, is required for bacteriophage N4 adsorption. J Bacteriol 175:7074–7080
Kiino DR, Singer MS, Rothman-Denes LB (1993b) Two overlapping genes encoding membrane proteins required for bacteriophage N4 adsorption. J Bacteriol 175:7081–7085
King J, Lenk EV, Botstein D (1973) Mechanism of head assembly and DNA encapsulation in Salmonella phage P22. II. Morphogenetic pathway. J Mol Biol 80:697–731
King MR, Vimr RP, Steenbergen SM, Spanjaard L, Plunkett G 3rd, Blattner FR, Vimr ER (2007) Escherichia coli K1-specific bacteriophage CUS-3 distribution and function in phase-variable capsular polysialic acid O acetylation. J Bacteriol 189:6447–6456
Krawiec S, Jimenez F, Garcia JA, Villanueva N, Sogo J, Salas M (1981) The orderly, in vitro emergence of DNA from bacteriophage φ29 particles. Virology 111:440–454
Kropinski AM (2000) Sequence of the genome of the temperate, serotype-converting, Pseudomonas aeruginosa bacteriophage D3. J Bacteriol 182:6066–6074
Kropinski AM, Kovalyova IV, Billington SJ, Patrick AN, Butts BD, Guichard JA, Pitcher TJ, Guthrie CC, Sydlaske AD, Barnhill LM, Havens KA, Day KR, Falk DR, McConnell MR (2007) The genome of epsilon15, a serotype-converting, Group E1 Salmonella enterica-specific bacteriophage. Virology 369:234–244
Kuhn A, Kellenberger E (1985) Productive phage infection in Escherichia coli with reduced internal levels of the major cations. J Bacteriol 163:906–912
Kuhn HM, Meier-Dieter U, Mayer H (1988) ECA, the enterobacterial common antigen. FEMS Microbiol Rev 4:195–222
Labedan B, Goldberg EB (1979) Requirement for membrane potential in injection of phage T4 DNA. Proc Natl Acad Sci USA 76:4669–4673
Labedan B, Heller KB, Jasaitis AA, Wilson TH, Goldberg EB (1980) A membrane potential threshold for phage T4 DNA injection. Biochem Biophys Res Commun 93:625–630
Lander GC, Tang L, Casjens SR, Gilcrease EB, Prevelige P, Poliakov A, Potter CS, Carragher B, Johnson JE (2006) The structure of an infectious P22 virion shows the signal for headful DNA packaging. Science 312:1791–1795
Lander GC, Khayat R, Li R, Prevelige PE, Potter CS, Carragher B, Johnson JE (2009) The P22 tail machine at subnanometer resolution reveals the architecture of an infection conduit. Structure 17:789–799
Landstrom J, Nordmark EL, Eklund R, Weintraub A, Seckler R, Widmalm G (2008) Interaction of a Salmonella enteritidis O-antigen octasaccharide with the phage P22 tailspike protein by NMR spectroscopy and docking studies. Glycoconj J 25:137–143
Lanni YT (1968) First-step-transfer deoxyribonucleic acid of bacteriophage T5. Bacteriol Rev 32:227–242
Lavigne R, Burkal’tseva MV, Robben J, Sykilinda NN, Kurochkina LP, Grymonprez B, Jonckx B, Krylov VN, Mesyanzhinov VV, Volckaert G (2003) The genome of bacteriophage φKMV, a T7-like virus infecting Pseudomonas aeruginosa. Virology 312:49–59
Lavigne R, Briers Y, Hertveldt K, Robben J, Volckaert G (2004) Identification and characterization of a highly thermostable bacteriophage lysozyme. Cell Mol Life Sci 61:2753–2759
Lavigne R, Seto D, Mahadevan P, Ackermann HW, Kropinski AM (2008) Unifying classical and molecular taxonomic classification: analysis of the Podoviridae using BLASTP-based tools. Res Microbiol 159:406–414
Lebedev AA, Krause MH, Isidro AL, Vagin AA, Orlova EV, Turner J, Dodson EJ, Tavares P, Antson AA (2007) Structural framework for DNA translocation via the viral portal protein. EMBO J 26:1984–1994
Leforestier A, Brasiles S, de Frutos M, Raspaud E, Letellier L, Tavares P, Livolant F (2008) Bacteriophage T5 DNA ejection under pressure. J Mol Biol 384:730–739
Leforestier A, Livolant F (2009) Structure of toroidal DNA collapsed inside the phage capsid. Proc Natl Acad Sci USA 106:9157–9162
Leforestier A, Livolant F (2010) The bacteriophage genome undergoes a succession of intracapsid phase transitions upon DNA ejection. J Mol Biol 396:384–395
Leiman PG, Battisti AJ, Bowman VD, Stummeyer K, Muhlenhoff M, Gerardy-Schahn R, Scholl D, Molineux 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
Leiman PG, Molineux IJ (2008) Evolution of a new enzyme activity from the same motif fold. Mol Microbiol 69:287–290
Lenk E, Casjens S, Weeks J, King J (1975) Intracellular visualization of precursor capsids in phage P22 mutant infected cells. Virology 68:182–199
Lin L (1992) Study of bacteriophage T7 gene 5.9 and gene 5.5. Ph.D. dissertation. SUNY, Sonybrook, New York
Lindberg AA, Sarvas M, Makela PH (1970) Bacteriophage attachment to the somatic antigen of Salmonella: Effect of O-specific structures in leaky R mutants and S, T1 Hybrids. Infect Immun 1:88–97
Lipinska B, Rao AS, Bolten BM, Balakrishnan R, Goldberg EB (1989) Cloning and identification of bacteriophage T4 gene 2 product gp2 and action of gp2 on infecting DNA in vivo. J Bacteriol 171:488–497
Liu M, Deora R, Doulatov SR, Gingery M, Eiserling FA, Preston A, Maskell DJ, Simons RW, Cotter PA, Parkhill J, Miller JF (2002) Reverse transcriptase-mediated tropism switching in Bordetella bacteriophage. Science 295:2091–2094
Liu M, Gingery M, Doulatov SR, Liu Y, Hodes A, Baker S, Davis P, Simmonds M, Churcher C, Mungall K, Quail MA, Preston A, Harvill ET, Maskell DJ, Eiserling FA, Parkhill J, Miller JF (2004) Genomic and genetic analysis of Bordetella bacteriophages encoding reverse transcriptase-mediated tropism-switching cassettes. J Bacteriol 186:1503–1517
Liu X, Shi M, Kong S, Gao Y, An C (2007) Cyanophage Pf-WMP4, a T7-like phage infecting the freshwater cyanobacterium Phormidium foveolarum: complete genome sequence and DNA translocation. Virology 366:28–39
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
Lu MJ, Henning U (1994) Superinfection exclusion by T-even-type coliphages. Trends Microbiol 2:137–139
Machida Y, Miyake K, Hattori K, Yamamoto S, Kawase M, Iijima S (2000) Structure and function of a novel coliphage-associated sialidase. FEMS Microbiol Lett 182:333–337
Mahony J, McGrath S, Fitzgerald GF, van Sinderen D (2008) Identification and characterization of lactococcal-prophage-carried superinfection exclusion genes. Appl Environ Microbiol 74:6206–6215
Mangenot S, Hochrein M, Radler J, Letellier L (2005) Real-time imaging of DNA ejection from single phage particles. Curr Biol 15:430–435
McGrath S, Fitzgerald GF, van Sinderen D (2002) Identification and characterization of phage-resistance genes in temperate lactococcal bacteriophages. Mol Microbiol 43:509–520
McPartland J, Rothman-Denes LB (2009) The tail sheath of bacteriophage N4 interacts with the Escherichia coli receptor. J Bacteriol 191:525–532
Meijer WJ, Horcajadas JA, Salas M (2001a) φ29 family of phages. Microbiol Mol Biol Rev 65:261–287
Meijer WJ, Serna-Rico A, Salas M (2001b) Characterization of the bacteriophage φ29-encoded protein p16.7: a membrane protein involved in phage DNA replication. Mol Microbiol 39:731–746
Miller JL, Le Coq J, Hodes A, Barbalat R, Miller JF, Ghosh P (2008) Selective ligand recognition by a diversity-generating retroelement variable protein. PLoS Biol 6:e131
Mishra P, Prem Kumar R, Ethayathulla AS, Singh N, Sharma S, Perbandt M, Betzel C, Kaur P, Srinivasan A, Bhakuni V, Singh TP (2009) Polysaccharide binding sites in hyaluronate lyase – crystal structures of native phage-encoded hyaluronate lyase and its complexes with ascorbic acid and lactose. FEBS J 276:3392–3402
Moak M, Molineux IJ (2000) Role of the Gp16 lytic transglycosylase motif in bacteriophage T7 virions at the initiation of infection. Mol Microbiol 37:345–355
Moak M, Molineux IJ (2004) Peptidoglycan hydrolytic activities associated with bacteriophage virions. Mol Microbiol 51:1169–1183
Moffatt BA, Studier FW (1988) Entry of bacteriophage T7 DNA into the cell and escape from host restriction. J Bacteriol 170:2095–2105
Molineux IJ (2001) No syringes please, ejection of phage T7 DNA from the virion is enzyme driven. Mol Microbiol 40:1–8
Molineux IJ (2006) Fifty-three years since Hershey and Chase; much ado about pressure but which pressure is it? Virology 344:221–229
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
Muller JJ, Barbirz S, Heinle K, Freiberg A, Seckler R, Heinemann U (2008) An intersubunit active site between supercoiled parallel beta helices in the trimeric tailspike endorhamnosidase of Shigella flexneri phage Sf6. Structure 16:766–775
Murray NE (2000) Type I restriction systems: sophisticated molecular machines (a legacy of Bertani and Weigle). Microbiol Mol Biol Rev 64:412–434
Olia AS, Al-Bassam J, Winn-Stapley DA, Joss L, Casjens SR, Cingolani G (2006) Binding-induced stabilization and assembly of the phage P22 tail accessory factor gp4. J Mol Biol 363:558–576
Olia AS, Bhardwaj A, Joss L, Casjens S, Cingolani G (2007a) Role of gene 10 protein in the hierarchical assembly of the bacteriophage P22 portal vertex structure. Biochemistry 46:8776–8784
Olia AS, Casjens S, Cingolani G (2007b) Structure of phage P22 cell envelope-penetrating needle. Nat Struct Mol Biol 14:1221–1227
Olia A, Prevelige P, Johnson J, Cingolani G (2011) Nat Struct Mol Biol 18:567–603
Olia AS, Casjens S, Cingolani G (2009) Structural plasticity of the phage P22 tail needle gp26 probed with xenon gas. Protein Sci 18:537–548
Olson NH, Gingery M, Eiserling FA, Baker TS (2001) The structure of isometric capsids of bacteriophage T4. Virology 279:385–391
Palva ET, Mäkelä PH (1980) Lipopolysaccharide heterogeneity in Salmonella typhimurium analyzed by sodium dodecyl sulfate polyacrylamide gel electrophoresis. Eur J Biochem 107:137–143
Panja D, Molineux IJ (2010) Dynamics of bacteriophage genome ejection in vitro and in vivo. Phys Biol 7:045006
Perez GL, Huynh B, Slater M, Maloy S (2009) Transport of phage P22 DNA across the cytoplasmic membrane. J Bacteriol 191:135–140
Petrov AS, Locker CR, Harvey SC (2009) Characterization of DNA conformation inside bacterial viruses. Phys Rev E Stat Nonlin Soft Matter Phys 80:021914
Petter JG, Vimr ER (1993) Complete nucleotide sequence of the bacteriophage K1F tail gene encoding endo-N-acylneuraminidase (endo-N) and comparison to an endo-N homolog in bacteriophage PK1E. J Bacteriol 175:4354–4363
Pope WH, Weigele PR, Chang J, Pedulla ML, Ford ME, Houtz JM, Jiang W, Chiu W, Hatfull GF, Hendrix RW, King J (2007) Genome sequence, structural proteins, and capsid organization of the cyanophage Syn5: a “horned” bacteriophage of marine synechococcus. J Mol Biol 368:966–981
Prehm P, Jann B, Jann K, Schmidt G, Stirm S (1976) On a bacteriophage T3 and T4 receptor region within the cell wall lipopolysaccharide of Escherichia coli B. J Mol Biol 101:277–281
Purohit PK, Inamdar MM, Grayson PD, Squires TM, Kondev J, Phillips R (2005) Forces during bacteriophage DNA packaging and ejection. Biophys J 88:851–866
Rao GR, Chakravorty-Burma M, Burma DP (1972) Transient depression in the active transport across the membrane of Salmonella typhimurium, after infection with bacteriophage P22. Virology 49:811–814
Rao RN (1968) Bacteriophage P22 controlled exclusion in Salmonella typhimurium. J Mol Biol 35:607–622
Raspaud E, Forth T, Sao-Jose C, Tavares P, de Frutos M (2007) A kinetic analysis of DNA ejection from tailed phages revealing the prerequisite activation energy. Biophys J 93:3999–4005
Rhoades M, Thomas CA Jr (1968) The P22 bacteriophage DNA molecule. II. Circular intracellular forms. J Mol Biol 37:41–61
Rickgauer JP, Fuller DN, Grimes S, Jardine PJ, Anderson DL, Smith DE (2008) Portal motor velocity and internal force resisting viral DNA packaging in bacteriophage φ29. Biophys J 94:159–167
Rohr TE, Troy FA (1980) Structure and biosynthesis of surface polymers containing polysialic acid in Escherichia coli. J Biol Chem 255:2332–2342
Saigo K (1975) Polar DNA ejection in bacteriophage T7. Virology 65:120–127
Saigo K (1978) Isolation of high-density mutants and identification of nonessential structural proteins in bacteriophage T5; dispensability of L-shaped tail fibers and a secondary major head protein. Virology 85:422–433
Sandmeier H, Iida S, Arber W (1992) DNA inversion regions Min of plasmid p15B and Cin of bacteriophage P1: evolution of bacteriophage tail fiber genes. J Bacteriol 174:3936–3944
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 374:346–355
Savalia D, Westblade LF, Goel M, Florens L, Kemp P, Akulenko N, Pavlova O, Padovan JC, Chait BT, Washburn MP, Ackermann HW, Mushegian A, Gabisonia T, Molineux I, Severinov K (2008) Genomic and proteomic analysis of φEco32, a novel Escherichia coli bacteriophage. J Mol Biol 377:774–789
Scholl D, Rogers S, Adhya S, Merril CR (2001) Bacteriophage K1-5 encodes two different tail fiber proteins, allowing it to infect and replicate on both K1 and K5 strains of Escherichia coli. J Virol 75:2509–2515
Scholl D, Kieleczawa J, Kemp P, Rush J, Richardson CC, Merril C, Adhya S, Molineux IJ (2004) Genomic analysis of bacteriophages SP6 and K1-5, an estranged subgroup of the T7 supergroup. J Mol Biol 335:1151–1171
Scholl D, Adhya S, Merril C (2005) Escherichia coli K1’s capsule is a barrier to bacteriophage T7. Appl Environ Microbiol 71:4872–4874
Schulz EC, Schwarzer D, Frank M, Stummeyer K, Muhlenhoff M, Dickmanns A, Gerardy-Schahn R, Ficner R (2010) Structural basis for the recognition and cleavage of polysialic acid by the bacteriophage K1F tailspike protein EndoNF. J Mol Biol 397:341–351
Schwarzer D, Stummeyer K, Gerardy-Schahn R, Muhlenhoff M (2007) Characterization of a novel intramolecular chaperone domain conserved in endosialidases and other bacteriophage tail spike and fiber proteins. J Biol Chem 282:2821–2831
Schwarzer D, Stummeyer K, Haselhorst T, Freiberger F, Rode B, Grove M, Scheper T, von Itzstein M, Muhlenhoff M, Gerardy-Schahn R (2009) Proteolytic release of the intramolecular chaperone domain confers processivity to endosialidase F. J Biol Chem 284:9465–9474
Serna-Rico A, Salas M, Meijer WJ (2002) The Bacillus subtilis phage φ29 protein p16.7, involved in φ29 DNA replication, is a membrane-localized single-stranded DNA-binding protein. J Biol Chem 277:6733–6742
Serwer P, Wright ET, Hakala KW, Weintraub ST (2008) Evidence for bacteriophage T7 tail extension during DNA injection. BMC Res Notes 1:36
Simon LD, Anderson TF (1967) The infection of Escherichia coli by T2 and T4 bacteriophages as seen in the electron microscope. I. Attachment and penetration. Virology 32:279–297
Simpson AA, Tao Y, Leiman PG, Badasso MO, He Y, Jardine PJ, Olson NH, Morais MC, Grimes S, Anderson DL, Baker TS, Rossmann MG (2000) Structure of the bacteriophage φ29 DNA packaging motor. Nature 408:745–750
Smith D, Tans J, Smith S, Grimes S, Anderson D, Bustamante C (2001) The bacteriophage φ29 portal motor can package DNA against a large internal force. Nature 413:748–752
Smith NL, Taylor EJ, Lindsay AM, Charnock SJ, Turkenburg JP, Dodson EJ, Davies GJ, Black GW (2005) Structure of a group A streptococcal phage-encoded virulence factor reveals a catalytically active triple-stranded beta-helix. Proc Natl Acad Sci USA 102:17652–17657
Steinbacher S, Seckler R, Miller S, Steipe B, Huber R, Reinemer P (1994) Crystal structure of P22 tailspike protein: interdigitated subunits in a thermostable trimer. Science 265:383–386
Steinbacher S, Baxa U, Miller S, Weintraub A, Seckler R, Huber R (1996) Crystal structure of phage P22 tailspike protein complexed with Salmonella sp. O-antigen receptors. Proc Natl Acad Sci USA 93:10584–10588
Steinbacher S, Miller S, Baxa U, Budisa N, Weintraub A, Seckler R, Huber R (1997) Phage P22 tailspike protein: crystal structure of the head-binding domain at 2.3 A, fully refined structure of the endorhamnosidase at 1.56 A resolution, and the molecular basis of O-antigen recognition and cleavage. J Mol Biol 267:865–880
Steven AC, Trus BL, Maizel JV, Unser M, Parry DA, Wall JS, Hainfeld JF, Studier FW (1988) Molecular substructure of a viral receptor-recognition protein. The gp17 tail-fiber of bacteriophage T7. J Mol Biol 200:351–365
Stojković E, Rothman-Denes L (2007) Coliphage N4 N-acetylmuramidase defines a new family of murien hydrolases. J Mol Biol 366:406–419
Strauss H, King J (1984) Steps in the stabilization of newly packaged DNA during phage P22 morphogenesis. J Mol Biol 172:523–543
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
Studier FW (1972) Bacteriophage T7. Science 176:367–376
Studier FW, Bandyopadhyay PK (1988) Model for how type I restriction enzymes select cleavage sites in DNA. Proc Natl Acad Sci USA 85:4677–4681
Stummeyer K, Dickmanns A, Muhlenhoff M, Gerardy-Schahn R, Ficner R (2005) Crystal structure of the polysialic acid-degrading endosialidase of bacteriophage K1F. Nat Struct Mol Biol 12:90–96
Stummeyer K, Schwarzer D, Claus H, Vogel U, Gerardy-Schahn R, Muhlenhoff M (2006) Evolution of bacteriophages infecting encapsulated bacteria: lessons from Escherichia coli K1-specific phages. Mol Microbiol 60:1123–1135
Susskind MM, Wright A, Botstein D (1971) Superinfection exclusion by P22 prophage in lysogens of Salmonella typhimurium. II. Genetic evidence for two exclusion systems. Virology 45:638–652
Susskind MM, Botstein D (1978) Molecular genetics of bacteriophage P22. Microbiol Rev 42:385–413
Takeda K, Uetake H (1973) In vitro interaction between phage and receptor lipopolysaccharide: a novel glycosidase associated with Salmonella phage epsilon15. Virology 52:148–159
Tan Y, Zhang K, Rao X, Jin X, Huang J, Zhu J, Chen Z, Hu X, Shen X, Wang L, Hu F (2007) Whole genome sequencing of a novel temperate bacteriophage of P. aeruginosa: evidence of tRNA gene mediating integration of the phage genome into the host bacterial chromosome. Cell Microbiol 9:479–491
Tang J, Olson N, Jardine PJ, Grimes S, Anderson DL, Baker TS (2008) DNA poised for release in bacteriophage φ29. Structure 16:935–943
Tang L, Marion WR, Cingolani G, Prevelige PE, Johnson JE (2005) Three-dimensional structure of the bacteriophage P22 tail machine. EMBO J 24:2087–2095
Tang L, Gilcrease EB, Casjens SR, Johnson JE (2006) Highly discriminatory binding of capsid-cementing proteins in bacteriophage L. Structure 14:837–845
Ter-Nikogosian VA, Vartanian MK, Trchunian AA (1991) Changes in membrane potential and transport of ions through the S. typhimurium LT2 membrane induced by bacteriophages. Biofizika 36:281–285
Tye BK, Huberman JA, Botstein D (1974) Non-random circular permutation of phage P22 DNA. J Mol Biol 85:501–528
Tzlil S, Kindt JT, Gelbart WM, Ben-Shaul A (2003) Forces and pressures in DNA packaging and release from viral capsids. Biophys J 84:1616–1627
Uetake H, Nakagawa T, Akiba T (1955) The relationship of bacteriophage to antigenic changes in Group E salmonellas. J Bacteriol 69:571–579
Uetake H, Hagiwara S (1969) Transfer of conversion gene(s) between different Salmonella phages g341 and epsilon-15. Virology 37:8–14
Umlauf B, Dreiseikelmann B (1992) Cloning, sequencing, and overexpression of gene 16 of Salmonella bacteriophage P22. Virology 188:495–501
Villafane R, Zayaz M, Gilcrease E, Kropinski A, Casjens S (2008) Genomic analysis of bacteriophage epsilon34 of Salmonella enterica serovar Anatum (15+). BMC Microbiol 8:e227
Vinga I, Sao-Jose C, Traveres P, Santos M (2006) Bacteriophage entry into the host cell. In: Wegrzyn G (ed) Modern bacteriophage biology and biotechnology. Research Signpost, Kerala, India, pp 165–205
Walkinshaw MD, Taylor P, Sturrock SS, Atanasiu C, Berge T, Henderson RM, Edwardson JM, Dryden DT (2002) Structure of Ocr from bacteriophage T7, a protein that mimics B-form DNA. Mol Cell 9:187–194
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
Wang HY, Elston T, Mogilner A, Oster G (1998a) Force generation in RNA polymerase. Biophys J 74:1186–1202
Wang MD, Schnitzer MJ, Yin H, Landick R, Gelles J, Block SM (1998b) Force and velocity measured for single molecules of RNA polymerase. Science 282:902–907
Willis SH, Kazmierczak KM, Carter RH, Rothman-Denes LB (2002) N4 RNA polymerase II, a heterodimeric RNA polymerase with homology to the single-subunit family of RNA polymerases. J Bacteriol 184:4952–4961
Wright A (1971) Mechanism of conversion of Salmonella O-antigen by bacteriophage epsilon 34. J Bacteriol 105:927–936
Xiang Y, Morais MC, Battisti AJ, Grimes S, Jardine PJ, Anderson DL, Rossmann MG (2006) Structural changes of bacteriophage φ29 upon DNA packaging and release. EMBO J 25:5229–5239
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 USA 105:9552–9557
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
Yin H, Wang MD, Svoboda K, Landick R, Block SM, Gelles J (1995) Transcription against an applied force. Science 270:1653–1657
Zarybnicky V (1969) Mechanism of T-even DNA ejection. J Theor Biol 22:33–42
Zavriev SK, Shemyakin MF (1982) RNA polymerase-dependent mechanism for the stepwise T7 phage DNA transport from the virion into E. coli. Nucleic Acids Res 10:1635–1652
Acknowledgments
We thank all our colleagues in this unusually collegial research field for many years of open and insightful discussions. We especially thank our own coworkers for their contributions to our respective research programs, which are supported by NIH grants GM32095 to IJM and AI074825 to SRC.
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Casjens, S.R., Molineux, I.J. (2012). Short Noncontractile Tail Machines: Adsorption and DNA Delivery by Podoviruses. In: Rossmann, M., Rao, V. (eds) Viral Molecular Machines. Advances in Experimental Medicine and Biology, vol 726. Springer, Boston, MA. https://doi.org/10.1007/978-1-4614-0980-9_7
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