Popping the cork: Mechanisms of phage genome ejection

Nature Reviews Microbiology

Volumn 11, Issue 3, 2013, Pages 194-204

  Molineux, Ian J ^a   Panja, Debabrata ^b,c  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

^c UTRECHT UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; BACTERIOPHAGE DNA; DEOXYRIBONUCLEASE; DNA BINDING PROTEIN; DOUBLE STRANDED DNA; DOUBLE STRANDED RNA; SINGLE STRANDED RNA;

BACILLUS SUBTILIS; BACTERIAL GENOME; BACTERIOPHAGE; BACTERIOPHAGE PRD1; BACTERIOPHAGE T3; BACTERIOPHAGE T4; BACTERIOPHAGE T5; CELL ENERGY; CRYOELECTRON MICROSCOPY; DNA BINDING; DNA HELIX; DNA PACKAGING; DNA STRUCTURE; DNA TRANSFECTION; ELECTRON MICROSCOPY; HYDROLYSIS; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR MECHANICS; NONHUMAN; OSMOTIC PRESSURE; PRIORITY JOURNAL; REVIEW; THERMODYNAMICS; VIRION; VIRUS CAPSID; WATER FLOW; X RAY DIFFRACTION;

MIRIDAE;

EID: 85027930977     PISSN: 17401526     EISSN: 17401534     Source Type: Journal    
DOI: 10.1038/nrmicro2988     Document Type: Review

References (156)

1. Kallmeyer, J., Pockalny, R., Adhikaria, R. R., Smith, D. C. & D'Hondt, S. Global distribution of microbial abundance and biomass in subseafloor sediment. Proc. Natl Acad. Sci. USA 109, 16213-16216 (2012).
2. Suttle, C. A., Marine viruses -major players in the global ecosystem. Nature Rev. Microbiol. 5, 801-812 (2007).
3. Hershey, A. D. & M. Chase, M. Independent functions of viral protein and nucleic acid in growth of bacteriophage. J. Gen. Physiol. 36, 39-56 (1952).
4. Avery, O. T., McLeod, C. M. & McCarty, M. Studies on the chemical nature of the substance inducing transformation of pneumococcal types. Induction of transformation by a desoxyribonucleic acid fraction isolated from Pneumococcus type III. J. Exp. Med. 79, 137-158 (1944).
5. Hershey, A. D. An upper limit to the protein content of the germinal substance of bacteriophage T2. Virology 1, 108-127 (1955).
6. Miller, E. S. et al. Bacteriophage T4 genome. Microbiol. Mol. Biol. Rev. 67, 86-156 (2003).
7. Rossman, M. G. & Rao, V. B. Viruses: sophisticated biological machines. Adv. Exp. Med. Biol. 726, 1-3 (2012).
8. Leiman, P. G. & Shneider, M. M. Contractile tail machines of bacteriophages. Adv. Exp. Med. Biol. 726, 93-114 (2012).
9. Davidson, A. R., Cardarelli, L., Pell, L. G., Radford, D. R. & Maxwell, K. L. Long noncontractile tail machines of bacteriophages. Adv. Exp. Med. Biol. 726, 115-142 (2012).
10. Casjens, S. R. &, Molineux, I. J. Short noncontractile tail machines: adsorption & DNA delivery by podoviruses. Adv. Exp. Med. Biol. 726, 143-179 (2012).
11. MacKay, D. J. & Bode, V. C. Events in lambda injection between phage adsorption & DNA entry. Virology 72, 154-166 (1976).
12. Kemp, P., Gupta, M. & Molineux, I. J. Bacteriophage T7 DNA ejection into cells is initiated by an enzymelike mechanism. Mol. Microbiol. 53, 1251-1265 (2004).
13. de Frutos, M., Letellier, L. & Raspaud, E. DNA ejection from bacteriophage T5: analysis of the kinetics and energetics. Biophys. J. 88, 1364-1370 (2005).
14. Raspaud, E., Forth, T., So-José, C., Tavares, P. & de Frutos, M. A kinetic analysis of DNA ejection from tailed phages revealing the prerequisite activation energy. Biophys. J. 93, 3999-4005 (2007).
15. Chiaruttini, N. et al. Is the in vitro ejection of bacteriophage DNA quasistatic? A bulk to single virus study. Biophys. J. 99, 447-455 (2010).
16. Anderson, T. F. in Phage and the Origins of Molecular Biology (eds Cairns, J., Stent, G. S. & Watson, J. D.) 63-78 (Cold Spring Harbor Laboratory Press, 1966)
17. Hershey, A. D. in Phage and the Origins of Molecular Biology (eds Cairns, J., Stent, G. S. & Watson, J. D.) 100-108 (Cold Spring Harbor Laboratory Press, 1966)
18. Stent, G. S. Molecular Biology of Bacterial Viruses (W. H. Freeman, 1963).
19. Ore, A. & Pollard, E. Physical mechanism of bacteriophage injection. Science 124, 430-432 (1956).
20. Zárybnický, V. Mechanism of T-even DNA ejection. J. Theor. Biol. 22, 33-42 (1969).
21. Bloomfield, V. A. DNA condensation by multivalent cations. Biopolymers 44, 269-282 (1998).
22. Grigorieff, N. & Harrison, S. C. Near-Atomic resolution reconstructions of icosahedral viruses from electron cryo-microscopy. Curr. Opin. Struct. Biol. 21, 265-273 (2011).
23. Smith, D. E. et al. The bacteriophage straight 29 portal motor can package DNA against a large internal force. Nature 413, 748-752 (2001).
24. Raspaud, E., Durand, D. & Livolant, F. Interhelical spacing in liquid crystalline spermine and spermidine-DNA precipitates. Biophys. J. 88, 392-403 (2005).
25. Todd, B. A., Parsegian, V. A., Shirahata, A., Thomas, T. J. & Rau, D. C. Attractive forces between condensed DNA double helices. Biophys. J. 94, 4775-4782 (2008).
26. Casjens, S. R. The DNA-packaging nanomotor of tailed bacteriophages. Nature Rev. Microbiol. 9, 647-657 (2011).
27. Chemla, Y. R. et al. Mechanism of force generation of a viral DNA packaging motor. Cell 122, 683-692 (2005).
28. Moffitt, J. R. et al. Intersubunit coordination in a homomeric ring ATPase. Nature 457, 446-450 (2009).
29. Fuller, D. N., Raymer, D. M., Kottadiel, V. I., Rao, V. B. & Smith, D. E. Single phage T4 DNA packaging motors exhibit large force generation, high velocity, and dynamic variability. Proc. Natl Acad. Sci. USA 104, 16868-16873 (2007).
30. Fuller, D. N. et al. Measurements of single DNA molecule packaging dynamics in bacteriophage λ reveal high forces, high motor processivity, and capsid transformations. J. Mol. Biol. 373, 1113-1122 (2007).
31. Rickgauer, J. P. et al. Portal motor velocity and internal force resisting viral DNA packaging in bacteriophage φ29. Biophys. J. 94, 159-167 (2008).
32. Black, L. W. & Silverman, D. J. Model for DNA packaging into bacteriophage T4 heads. J. Virol. 28, 643-655 (1978).
33. Chattoraj, D. K. & Inman, R. B. Location of DNA ends in P2, 186, P4, and lambda bacteriophage heads. J. Mol. Biol. 87, 11-22 (1974).
34. Saigo, K. Polar DNA ejection in bacteriophage T7. Virology 65, 120-127 (1975).
35. Shaw, A. R. & Davison, J. Polarized injection of the bacteriophage T5 chromosome. J. Virol. 30, 933-935 (1979).
36. Tavares, P., Lurz, R., Stiege, A., Ruckert, B. & Trautner, T. A. Sequential headful packaging and fate of the cleaved DNA ends in bacteriophage SPP1. J. Mol. Biol. 264, 954-967 (1996).
37. González-Huici, V., Salas, M. & Hermoso, J. M. The push-pull mechanism of bacteriophage 29 DNA injection. Mol. Microbiol. 52, 529-540 (2004).
38. Chang, J., Weigele, P., King, J., Chiu, W. & Jiang, W. Cryo-EM asymmetric reconstruction of bacteriophage P22 reveals organization of its DNA packaging and infecting machinery. Structure 14, 1073-1082 (2006).
39. Tang, J.et al. DNA poised for release in bacteriophage 29. Structure 16, 935-943 (2008).
40. Liu, X. et al. Structural changes in a marine podovirus associated with release of its genome into Prochlorococcus. Nature Struct. Mol. Biol. 17, 830-836 (2010).
41. Tang, J. et al. Peering down the barrel of a bacteriophage portal: the genome packaging and release valve in P22. Structure 19, 496-502 (2011).
42. Jiang, W. et al. Structure of epsilon15 bacteriophage reveals genome organization and DNA packaging/ injection apparatus. Nature 439, 612-616 (2006).
43. North, A. C. & Rich, A. X-ray diffraction studies of bacterial viruses. Nature 191, 1242-1245 (1961).
44. Richards, K. E., Williams, R. C. & Calendar, R. Mode of DNA packaging within bacteriophage heads. J. Mol. Biol. 78, 255-259 (1973).
45. Earnshaw, W. C. & Casjens, S. R. DNA packaging by the double-stranded DNA bacteriophages. Cell 21, 319-331 (1980).
46. Earnshaw, W. C. & Harrison, S. C. DNA arrangement in isometric phage heads. Nature 268, 598-602 (1977).
47. Earnshaw, W. C., King, J., Harrison, S. C. & Eiserling, F. A. The structural organization of DNA packaged within the heads of T4 wild-type, isometric and giant bacteriophages. Cell 14, 559-568 (1978).
48. Cerritelli, M. E. et al. Encapsidated conformation of bacteriophage T7 DNA. Cell 91, 271-280 (1997).
49. Agirrezabala, X. et al. Maturation of phage T7 involves structural modification of both shell and inner core components. EMBO J. 24, 3820-3829 (2005).
50. Leiman, P. G. et al. 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 (2007).
51. Choi, K. H. et al. Insight into DNA and protein transport in double-stranded DNA viruses: the structure of bacteriophage N4. J. Mol. Biol. 378, 726-736 (2008).
52. Chang, J. T. et al. Visualizing the structural changes of bacteriophage epsilon15 and its Salmonella host during infection. J. Mol. Biol. 402, 731-740 (2010).
53. Dai, W. et al. Three-dimensional structure of tropism switching Bordetella bacteriophage. Proc. Natl Acad. Sci. USA 107, 4347-4352 (2010).
54. Comolli, L. R. et al. Three-dimensional architecture of the bacteriophage 29 packaged genome and elucidation of its packaging process. Virology 371, 267-277 (2008).
55. Lander, G. C. et al. The structure of an infectious P22 virion shows the signal for headful DNA packaging. Science 312, 1791-1795 (2006).
56. Effantin, G., Boulanger, P., Neumann, E., Letellier, L. & Conway, J. F. Bacteriophage T5 structure reveals similarities with HK97 and T4 suggesting evolutionary relationships. J. Mol. Biol. 361, 993-1002 (2006).
57. Olson, N. H., Gingery, M., Eiserling, F. A. & Baker, T. S. The structure of isometric capsids of bacteriophage T4. Virology 279, 385-391 (2001).
58. Fokine, A. et al. Molecular architecture of the prolate head of bacteriophage T4. Proc. Natl Acad. Sci. USA 101, 6003-6008 (2004).
59. Duda, R. L., Hendrix, R. W., Huang, W. M. & Conway, J. F. Shared architecture of bacteriophage SPO1 and herpesvirus capsids. Curr. Biol. 16, R11-R13 (2006).
60. Leforestier, A. & Livolant, F. The bacteriophage genome undergoes a succession of intracapsid phase transitions upon DNA ejection. J. Mol. Biol. 396, 384-395 (2010).
61. Petrov, A. S. & Harvey, S. C. Structural and thermodynamic principles of viral packaging. Structure 15, 21-27 (2007).
62. Petrov, A. S., Boz, M. B. & Harvey, S. C. The conformation of double-stranded DNA inside bacteriophages depends on capsid size and shape. J. Struct. Biol. 160, 241-248 (2007).
63. Fuller, D. N. et al. Ionic effects on viral DNA packaging and portal motor function in bacteriophage. Proc. Natl Acad. Sci. USA 104, 11245-11250 (2007).
64. Evilevitch, E. et al. Effects of salt concentrations and bending energy on the extent of ejection of phage genomes. Biophys. J. 94, 1110-1120 (2008).
65. Wu, D., Van Valen, D., Hu, Q. & Phillips, R. Iondependent dynamics of DNA ejections for bacteriophage λ. Biophys. J. 99, 1101-1109 (2010).
66. Aubrey, K. L., Casjens, S. R. & Thomas, G. J. Jr. Secondary structure and interactions of the packaged dsDNA genome of bacteriophage P22 investigated by Raman difference spectroscopy. Biochemistry 31, 11835-11842 (1992).
67. Overman, S. A. et al. Conformation and interactions of the packaged double-stranded DNA of bacteriophage T7. Biospectroscopy 4, S47-S56 (1998).
68. Panja, D. & Molineux, I. J. Dynamics of bacteriophage genome ejection in vitro and in vivo. Phys. Biol. 7, 045006 (2010).
69. Vafabakhsh, R. & Ha, T. Extreme bendability of DNA less than 100 base pairs long revealed by singlemolecule cyclization. Science 337, 1097-1101 (2012).
70. Qiu, X. et al. Salt-dependent DNA-DNA spacings in intact bacteriophage λ reflect relative importance of DNA self-repulsion and bending energies. Phys. Rev. Lett. 106, 028102 (2011).
71. Saenger, W. Principles of Nucleic Acid Structure. (Springer, 1984).
72. Leikin, S., Parsegian, V. A. & Rau, D. C. Hydration forces. Annu. Rev. Phys. Chem. 44, 369-395 (1993).
73. Brovchenko, I., Krukau, A., Oleinikova, A. & Mazur, A. K. Water clustering and percolation in low hydration DNA shells. J. Phys. Chem. B. 111, 3258-3266 (2007).
74. Wolf, B. & Hanlon, S. Structural transitions of deoxyribonucleic acid in aqueous electrolyte solutions. II. The role of hydration. Biochemistry 14, 1661-1670 (1975).
75. Evilevitch, A., Castelnovo, M., Knobler, C. M. & Gelbart, W. M. Measuring the force ejecting DNA from phage. J. Phys. Chem. B 108, 6838-6843 (2004).
76. Grayson, P. et al. The effect of genome length on ejection forces in bacteriophage lambda. Virology 348, 430-436 (2006).
77. So-José, C., de Frutos, M., Raspaud, E., Santos, M. A. & Tavares, P. 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 (2007). This study extends the observations of reference 76 by investigating osmotic suppression of genome ejection in phage SPP1.
78. Leforestier, A. et al. Bacteriophage T5 DNA ejection under pressure. J. Mol. Biol. 384, 730-739 (2008).
79. Kindt, J., Tzlil, S., Ben-Shaul, A. & Gelbart, W. M. DNA packaging and ejection forces in bacteriophage. Proc. Natl Acad. Sci. USA 98, 13671-13674 (2001).
80. Tzlil, S., Kindt, J. T., Gelbart, W. M. & Ben-Shaul, A. Forces and pressures in DNA packaging and release from viral capsids. Biophys. J. 84, 1616-1627 (2003).
81. Purohit, P. K. et al. Forces during bacteriophage DNA packaging and ejection. Biophys. J. 88, 851-866 (2005).
82. Purohit, P. K., Kondev, J. & Phillips, R. Mechanisms of DNA packaging in viruses. Proc. Natl Acad. Sci. USA 100, 3173-3178 (2005).
83. Inamdar, M. M., Gelbart, W. M. & Phillips, R. Dynamics of DNA ejection from bacteriophages. Biophys. J. 91, 411-420 (2006).
84. Evilevitch, A., Lavelle, L., Knobler, C. M., Raspaud, E. & Gelbart, W. M. Osmotic pressure inhibition of DNA ejection from phage. Proc. Natl Acad. Sci. USA 100, 9292-9295 (2003).
85. Löf, D., Schillén, K., Jönsson, B. & Evilevitch, A. Forces controlling the rate of DNA ejection from phage λ. J. Mol. Biol. 368, 55-65 (2007).
86. Molineux, I. J. Fifty-three years since Hershey and Chase; much ado about pressure but which pressure is it? Virology 344, 221-229 (2006).
87. Grayson, P. & Molineux, I. J. Is phage DNA injected into cells -biologists and physicists can agree. Curr. Opin. Microbiol. 10, 401-409 (2007).
88. Lemay, S. G., Panja, D. & Molineux, I. J. Role of osmotic and hydrostatic pressures in bacteriophage genome ejection. Preprint at arXiv [online] http://arxiv.org/pdf/1207.3418v1.pdf (2012).
89. Grayson, P., Han, L., Winther, T. & Phillips, R. Realtime observations of single bacteriophage λ DNA ejections in vitro. Proc. Natl Acad. Sci. USA 104, 14652-14657 (2007).
90. Mangenot, S., Hochrein, M., Radler, J. & Letellier, L. Real-time imaging of DNA ejection from single phage particles. Curr. Biol. 15, 430-435 (2005).
91. Fang, P. A. et al. Visualization of bacteriophage T3 capsids with DNA incompletely packaged in vivo. J. Mol. Biol. 384, 1384-1399 (2008).
92. Koch, A. L. The biophysics of Gram-negative periplasmic space. Crit. Rev. Microbiol. 24, 23-59 (1998).
93. Whatmore, A. M. & Reed, R. H. Determination of turgor pressure in Bacillus subtilis: a possible role for K+ in turgor regulation. J. Gen. Microbiol. 136, 2521-2526 (1990).
94. Pruss, G., Goldstein, R. N. & Calendar, R. In vitro packaging of satellite phage P4 DNA. Proc. Natl Acad. Sci. USA 71, 2367-2371 (1974).
95. Zavriev, S. K. & Shemyakin, M. F. RNA polymerasedependent mechanism for the stepwise T7 phage DNA transport from the virion into E. coli. Nucleic Acids Res. 10, 1635-1652 (1982).
96. Moffatt, B. A. & Studier, F. W. Entry of bacteriophage T7 DNA into the cell and escape from host restriction. J. Bacteriol. 170, 2095-2105 (1988).
97. Garca, L. R. & Molineux, I. J. Rate of translocation of bacteriophage T7 DNA across the membranes of Escherichia coli. J. Bacteriol. 177, 4066-4076 (1995).
98. Garca, L. R. & Molineux, I. J. Translocation and cleavage of bacteriophage T7 DNA by the type I restriction enzyme EcoKI in vivo. Proc. Natl Acad. Sci. USA 96, 12430-12435 (1999).
99. Kazmierczak, K. & Rothman-Denes, L. in The Bacteriophages 2nd edn Ch. 21 (ed. Calendar, R.) 302-314 (Oxford Univ. Press, 2006).
100. Gonzalez-Huici, V., Salas, M. & Hermoso, J. M. Requirements for Bacillus subtilis bacteriophage 29 DNA ejection. Gene 374, 19-25 (2006).
101. Alcorlo, M., Gonzalez-Huici, V. & Hermoso, J. M. 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 (2007).
102. Lanni, Y. T. First-step-transfer deoxyribonucleic acid of bacteriophage T5. Bacteriol. Rev. 32, 227-242 (1968).
103. McCorquodale, D. J. & Warner, H. R. in The Bacteriophages 1st edn Vol. 1 (ed. Calendar, R.) 439-475 (Plenum, 1988).
104. Filali Maltouf, A. F. & Labedan, B. Host cell metabolic energy is not required for injection of bacteriophage T5 DNA. J. Bacteriol. 153, 124-133 (1983).
105. Kemp, P., Garcia, L. R. & Molineux, I. J. Changes in bacteriophage T7 virion structure at the initiation of infection. Virology 340, 307-317 (2005).
106. Chang, C.-Y., Kemp, P. & Molineux, I. J. Gp15 and gp16 cooperate in translocating bacteriophage T7 DNA into the infected cell. Virology 398, 176-186 (2010).
107. Molineux, I. J. No syringes please, ejection of T7 DNA from the virion is enzyme-driven. Mol. Microbiol. 40, 1-8 (2001).
108. Molineux, I. J. in The Bacteriophages 2nd edn Ch. 20 (ed. Calendar, R.) 277-301 (Oxford Univ. Press, 2006).
109. Garca, L. R. & Molineux, I. J. Transcriptionindependent DNA translocation of bacteriophage T7 DNA into Escherichia coli. J. Bacteriol. 178, 6921-6929 (1996).
110. Struthers-Schlinke, J. S., Robins, W. P., Kemp, P. & Molineux, I. J. The internal head protein gp16 of bacteriophage T7 controls DNA ejection from the virion. J. Mol. Biol. 301, 35-45 (2000).
111. Roessner, C. A. & Ihler, G. M. Formation of transmembrane channels in liposomes during injection of λ DNA. J. Biol. Chem. 261, 386-390 (1986).
112. Roessner, C. A., Struck, D. & Ihler, G. M. Injection of DNA into liposomes by bacteriophage λ. J. Biol. Chem. 258, 643-648 (1983).
113. Böhm, J. et al. FhuA-mediated phage genome transfer into liposomes: a cryo-electron tomography study. Curr. Biol. 11, 1168-1175 (2001).
114. Simon, L. D. & Anderson, T. F. The infection of Escherichia coli by T2 and T4 bacteriophages as seen in the electron microscope. I. Attachment and penetration. Virology 32, 279-297 (1967).
115. Tarahovsky, Y. S., Khusainov, A. A., Deev, A. A. & Kim, Y. V. Membrane fusion during infection of E. coli cells by phage T4. FEBS Lett. 289, 18-22 (1991).
116. Liu, J., Chen, C. Y. Shiomi, D. Niki, H. & Margolin, W. Visualization of bacteriophage P1 infection by cryoelectron tomography of tiny Escherichia coli. Virology 417, 304-311 (2011).
117. Hu, B., Margolin, W., Molineux, I. J. & Liu, J. The bacteriophage T7 virion undergoes extensive structural remodeling during infection. Science 10 Jan 2013 (doi:10.1126/science.1231887).
118. Labrie, S. J., Samson, J. E. & Moineau, S. Bacteriophage resistance mechanisms. Nature Rev. Microbiol. 8, 317-327 (2010).
119. Newbold, J. E. & Sinsheimer, R. L. The process of infection with bacteriophage φX174. XXXII. Early steps in the infection process: attachment, eclipse and DNA penetration. J. Mol. Biol. 49, 49-66 (1970).
120. Parenchych, W. in RNA Phages (ed. Zinder, N.) 85-112 (Cold Spring Harbor Laboratory Press, 1975).
121. Zsigray, R. M., Miss, A. L. & Landman, O. E. Penetration of a bacteriophage into Bacillus subtilis: blockage of infection by deoxyribonuclease. J. Virol. 11, 69-77 (1973).
122. Santos, M. A., De Lencastre, H. & Archer, L. J. Homology between phages SPP1, 41c, 22a, ρ15 and SF6 of Bacillus subtilis. J. Gen. Virol. 65, 2067-2072 (1984).
123. Grinius, L. Nucleic acid transport driven by ion gradient across cell membrane. FEBS Lett. 113, 1-10 (1980).
124. Kalasauskaite, E. V., Kadišaite, D. L., Daugelavičius, R. J., Grinius, L. &. Jasaitis, A. A. Studies on energy supply for genetic processes. Eur. J. Biochem. 130, 123-130 (1983).
125. Grinius, L. & Daugelavičius, R. Depolarization of Escherichia coli cytoplasmic membrane by bacteriophages T4 and lambda: evidence for induction of ion-permeable channels. Bioelectrochem. Bioenerg. 19, 235-245 (1988).
126. Kuhn, A. & Kellenberger, E. Productive phage infection in Escherichia coli with reduced internal levels of the major cations. J. Bacteriol. 163, 906-912 (1985).
127. Boulanger, P. & Letellier, L. Characterization of ion channels involved in the penetration of T4 DNA into Escherichia coli cells. J. Biol. Chem. 263, 9767-9775 (1988).
128. Boulanger, P. & Letellier, L. Ion channels are likely to be involved in the two steps of phage T5 DNA penetration into Escherichia coli cells. J. Biol. Chem. 267, 3168-3172 (1992).
129. Guihard, G., Benedetti, H. Besnard, M. & Letellier, L. Phosphate efflux through the channels formed by colicins and phage T5 in Escherichia coli cells is responsible for the fall in cytoplasmic ATP. J. Biol. Chem. 268, 17775-17780 (1993).
130. Daugelavičius, R., Bamford, J. K. & Bamford, D. H. Changes in host cell energetics in response to bacteriophage PRD1 DNA entry. J. Bacteriol. 179, 5203-5210 (1997).
131. Jakutyte, L. et al. First steps of bacteriophage SPP1 entry into Bacillus subtilis. Virology 422, 425-434 (2012).
132. Grahn, A. M., Daugelavičius, R. & Bamford, D. H. Sequential model of phage PRD1 DNA delivery: active involvement of the viral membrane. Mol. Microbiol. 46, 1199-1209 (2002).
133. Labedan, B. & Goldberg, E. B. Requirement for membrane potential in injection of phage T4 DNA. Proc. Natl Acad. Sci. USA 76, 4669-4673 (1979).
134. Labedan, B., Heller, K. B., Jasaitis, A. A., Wilson, T. H. & Goldberg, E. B. A membrane potential threshold for phage T4 DNA injection. Biochem. Biophys. Res. Comm. 93, 625-630 (1980).
135. McAllister, W. T. Bacteriophage infection: which end of the SP82G genome goes in first? J. Virol. 5, 194-198 (1970).
136. Labedan, B., Crochet, M., Legault-Demme, J. & Stevens, B. J. Location of the first step transfer fragment and single strand interruptions in T5st0 bacteriophage DNA. J. Mol. Biol. 75, 213-234 (1973).
137. Labedan, B. & Legault-Demare, J. Penetration into host cells of naked partially injected (post FST) DNA of bacteriophage T5. J. Virol. 12, 226-229 (1973).
138. Van Valen, D. et al. A single-molecule Hershey-Chase experiment. Curr. Biol. 22, 1339-1343 (2012).
139. Elliott, J. & Arber, W. E. coli K-12 pel mutants, which block phage λ DNA injection, coincide with ptsM, which determines a component of a sugar transport system. Mol. Gen. Genet. 161, 1-8 (1978).
140. Kiino, D. R. & Rothman-Denes, L. B. Genetic analysis of bacteriophage N4 adsorption. J. Bacteriol. 171, 4595-4602 (1989).
141. Baptista, C., Santos, M. A. & So-José, C. Phage SPP1 reversible adsorption to Bacillus subtilis cell wall teichoic acids accelerates virus recognition of membrane receptor YueB. J. Bacteriol. 190, 4989-4996 (2008).
142. Geller, B. L., Ivey, R. G., Trempy, J. E. & Hettinger-Smith, B. Cloning of a chromosomal gene required for phage infection of Lactococcus lactis subsp. lactis C2. J. Bacteriol. 175, 5510-5519 (1993).
143. Räisänen, L., Schubert, K., Jaakonsaari, T. & Alatossava, T. Characterization of lipoteichoic acids as Lactobacillus delbrueckii phage receptor components. J. Bacteriol. 186, 5529-5532 (2004).
144. Räisänen, L. et al. Molecular interaction between lipoteichoic acids and Lactobacillus delbrueckii phages depends on d-Alanyl and α-glucose substitution of poly(glycerophosphate) backbones. J. Bacteriol. 189, 4135-4140 (2007).
145. Baumann, L., Benz, W. C. Wright, A. & Goldberg, E. B. Inactivation of urea-treated phage T4 by phosphatidylglycerol. Virology 41, 356-364 (1970).
146. Boulanger, P. et al. Phage T5 straight tail fiber is a multifunctional protein acting as a tape measure and carrying fusogenic and muralytic activities. J. Biol. Chem. 283, 13556-13564 (2008).
147. Hancock, R. E. W. & Braun, V. Nature of the energy requirement for the irreversible adsorption of bacteriophages T1 and 80 to Escherichia coli. J. Bacteriol. 125, 409-415 (1976).
148. Filali Maltouf, A. & Labedan, B. The energetics of the injection process of bacteriophage lambda DNA and the role of the ptsM/pel-encoded protein. Biochem. Biophys. Res. Comm. 130, 1093-1101 (1985).
149. Cvirkaite-Krupovič, V., Krupovič, M. Daugelavičius, R. & Bamford, D. H. Calcium ion-dependent entry of the membrane-containing bacteriophage PM2 into its Pseudoalteromonas host. Virology 405, 120-128 (2010).
150. Molineux, I. J. Host-parasite interactions: recent developments in the genetics of abortive phage infections. New Biol. 3, 230-236 (1991).
151. Snyder, L. Phage-exclusion enzymes: a bonanza of biochemical and cell biology reagents? Mol. Microbiol. 15, 415-423 (1995).
152. Coren, J., Pierce, J. & Sternberg, N. Headful packaging revisited: the packaging of more than one DNA molecule into a bacteriophage P1 head. J. Mol. Biol. 249, 176-184 (1995).
153. Leffers, G. & Rao, V. B. A discontinuous headful packaging model for packaging less than headful length DNA molecules by bacteriophage T4. J. Mol. Biol. 258, 839-850 (1996).
154. Schrader, H. S. et al. Bacteriophage infection and multiplication occur in Pseudomonas aeruginosa starved for 5 years. Can. J. Microbiol. 43, 1157-1163 (1997).
155. Calendar, R. (ed.) The Bacteriophages 2nd edn (Oxford Univ. Press, 2006).
156. Black, L. W. & Thomas, J. A. Condensed genome structure. Adv. Exp. Med. Biol. 726, 469-487 (2012).