Abstract
Large, tailed dsDNA-containing bacteriophage genomes are packaged to a conserved and high density (∼500 mg/ml), generally in ∼2.5-nm, duplex-to-duplex, spaced, organized DNA shells within icosahedral capsids. Phages with these condensate properties, however, differ markedly in their inner capsid structures: (1) those with a naked condensed DNA, (2) those with many dispersed unstructured proteins embedded within the DNA, (3) those with a small number of localized proteins, and (4) those with a reduced or DNA-free internal protein structure of substantial volume. The DNA is translocated and condensed by a high-force ATPase motor into a procapsid already containing the proteins that are to be ejected together with the DNA into the infected host. The condensed genome structure of a single-phage type is unlikely to be precisely determined and can change without loss of function to fit an altered capsid size or internal structure. Although no such single-phage condensed genome structure is known exactly, it is known that a single general structure is unlikely to apply to all such phages.
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References
Ackermann H-W, Tremblay D, Moineau S (2004) Long-term bacteriophage preservation. WFCC Newslett 38:35–40
Aebi U, Bijlenga RKL, Bt H et al (1976) Comparison of the structural and chemical composition of giant T-even phage heads. J Supramol Struct 5:475–495
Agirrezabala X, Martin-Benito J, Caston JR et al (2005) Maturation of phage T7 involves structural modification of both shell and inner core components. EMBO J 24:3820–3829
Arsuaga J, Vázquez M, Trigueros S et al (2002) Knotting probability of DNA molecules confined in restricted volumes: DNA knotting in phage capsids. Proc Natl Acad Sci USA 99:5373–5377
Bair CL, Rifat D, Black LW (2007) Exclusion of glucosyl-hydroxymethylcytosine DNA containing bacteriophages is overcome by the injected protein inhibitor IPI*. J Mol Biol 366:779–789
Bijlenga RKL, Aebi U, Kellenberger E (1976) Properties and structure of a gene 24-controlled T4 giant phage. J Mol Biol 103:469–498
Black LW (1989) DNA packaging in dsDNA bacteriophages. Annu Rev Microbiol 43:267–292
Black LW, Silverman DJ (1978) Model for DNA packaging into bacteriophage T4 heads. J Virol 28:643–655
Black LW, Newcomb WW, Boring JW et al (1985) Ion etching bacteriophage T4: support for a spiral-fold model of packaged DNA. Proc Natl Acad Sci USA 82:7960–7964
Black LW, Showe MK, Steven AC (1993) Morphogenesis of the T4 head. In: Karam JD (ed) Molecular biology of bacteriophage T4. ASM, Washington, DC, pp 218–258
Cardarelli L, Lam R, Tuite A et al (2010) The crystal structure of bacteriophage HK97 gp6: defining a large family of head-tail connector proteins. J Mol Biol 395:754–768
Cermakian N, Ikeda TM, Cedergren R et al (1996) Sequences homologous to yeast mitochondrial and bacteriophage T3 and T7 RNA polymerases are widespread throughout the eukaryotic lineage. Nucleic Acids Res 24:648–654
Cerritelli ME, Cheng N, Rosenberg AH et al (1997) Encapsidated conformation of bacteriophage T7 DNA. Cell 91:271–280
Cerritelli ME, Conway JF, Cheng N et al (2003a) Molecular mechanisms in bacteriophage T7 procapsid assembly, maturation, and DNA containment. Adv Protein Chem 64:301–323
Cerritelli ME, Trus BL, Smith CS et al (2003b) A Second Symmetry Mismatch at the Portal Vertex of Bacteriophage T7: 8-fold Symmetry in the Procapsid Core. J Mol Biol 327:1–6
Chang J, Weigele P, King J et al (2006) Cryo-EM asymmetric reconstruction of bacteriophage P22 reveals organization of its DNA packaging and infecting machinery. Structure 14:1073–1082
Chang C-Y, Kemp P, Molineux IJ (2010a) Gp15 and gp16 cooperate in translocating bacteriophage T7 DNA into the infected cell. Virology 398:176–186
Chang JT, Schmid MF, Haase-Pettingell C et al (2010b) Visualizing the structural changes of bacteriophage Epsilon15 and its Salmonella host during infection. J Mol Biol 402:731–740
Chattoraj DK, Inman RB (1974) Location of DNA ends in P2, 186, P4 and lambda bacteriophage heads. J Mol Biol 87:11–22
Chen J, Lu Z, Sakon J et al (2000) Increasing the thermostability of staphylococcal nuclease: implications for the origin of protein thermostability. J Mol Biol 303:125–130
Choi KH, McPartland J, Kaganman I et al (2008) Insight into DNA and protein transport in double-stranded DNA viruses: the structure of bacteriophage N4. J Mol Biol 378:726–736
Comolli LR, Spakowitz AJ, Siegerist CE et al (2008) Three-dimensional architecture of the bacteriophage phi29 packaged genome and elucidation of its packaging process. Virology 371:267–277
Depping R, Lohaus C, Meyer HE et al (2005) The mono-ADP-ribosyltransferases Alt and ModB of bacteriophage T4: target proteins identified. Biochem Biophys Res Commun 335:1217–1223
Duda RL, Ross PD, Cheng N et al (2009) Structure and energetics of encapsidated DNA in bacteriophage HK97 studied by scanning calorimetry and cryo-electron microscopy. J Mol Biol 391:471–483
Earnshaw WC, Casjens SR (1980) DNA packaging by the double-stranded DNA bacteriophages. Cell 21:319–331
Earnshaw WC, Harrison SC (1977) DNA arrangement in isometric phage heads. Nature 268:598–602
Earnshaw WC, King J, Harrison SC et al (1978) The structural organization of DNA packaged within the heads of T4 wild-type, isometric and giant bacteriophages. Cell 14:559–568
Ebisawa T, Yamamura A, Kameda Y et al (2010) The structure of mAG, a monomeric mutant of the green fluorescent protein Azami-Green, reveals the structural basis of its stable green emission. Acta Crystallogr Sect F Struct Biol Cryst Commun 66:485–489
Effantin G, Boulanger P, Neumann E et al (2006) Bacteriophage T5 structure reveals similarities with HK97 and T4 suggesting evolutionary relationships. J Mol Biol 361:993–1002
Fang P-A, Wright ET, Weintraub ST et al (2008) Visualization of bacteriophage T3 capsids with DNA incompletely packaged in vivo. J Mol Biol 384:1384–1399
Fuller DN, Rickgauer JP, Jardine PJ et al (2007) Ionic effects on viral DNA packaging and portal motor function in bacteriophage phi 29. Proc Natl Acad Sci USA 104:11245–11250
Garcia L, Molineux I (1996) Transcription-independent DNA translocation of bacteriophage T7 DNA into Escherichia coli. J Bacteriol 178:6921–6929
Gleghorn ML, Davydova EK, Rothman-Denes LB et al (2008) Structural basis for DNA-hairpin promoter recognition by the bacteriophage N4 virion RNA polymerase. Mol Cell 32:707–717
Glucksmann MA, Markiewicz P, Malone C et al (1992) Specific sequences and a hairpin structure in the template strand are required for N4 virion RNA polymerase promoter recognition. Cell 70:491–500
Gowen B, Bamford JKH, Bamford DH et al (2003) The tailless icosahedral membrane virus PRD1 localizes the proteins involved in genome packaging and injection at a unique vertex. J Virol 77:7863–7871
Hartman PS, Eisenstark A, Pauw PG (1979) Inactivation of phage T7 by near-ultraviolet radiation plus hydrogen peroxide: DNA-protein crosslinks prevent DNA injection. Proc Natl Acad Sci USA 76:3228–3232
Hertveldt K, Lavigne R, Pleteneva E et al (2005) Genome comparison of Pseudomonas aeruginosa large phages. J Mol Biol 354:536–545
Hong Y-R, Black LW (1993) Protein folding studies in vivo with a bacteriophage T4 expression-packaging-processing vector that delivers encapsidated fusion proteins into bacteria. Virology 194:481–490
Iida S, Streiff MB, Bickle TA et al (1987) Two DNA antirestriction systems of bacteriophage P1, darA, and darB: characterization of darA- phages. Virology 157:156–166
Jiang W, Chang J, Jakana J et al (2006) Structure of epsilon15 bacteriophage reveals genome organization and DNA packaging/injection apparatus. Nature 439:612–616
Johnson JE, Chiu W (2007) DNA packaging and delivery machines in tailed bacteriophages. Curr Opin Struct Biol 17:237–243
Juers DH, Jacobson RH, Wigley D et al (2000) High resolution refinement of beta-galactosidase in a new crystal form reveals multiple metal-binding sites and provides a structural basis for alpha-complementation. Protein Sci 9:1685–1699
Kalasauskaite EV, Kadisaite DL, Daugelavicius RJ et al (1983) Studies on energy supply for genetic processes. Eur J Biochem 130:123–130
Karhu NJ, Ziedaite G, Bamford DH et al (2007) Efficient DNA packaging of bacteriophage PRD1 requires the unique vertex protein P6. J Virol 81:2970–2979
Kazmierczak KM, Davydova EK, Mustaev AA et al (2002) The phage N4 virion RNA polymerase catalytic domain is related to single-subunit RNA polymerases. EMBO J 21:5815–5823
Kemp P, Garcia LR, Molineux IJ (2005) Changes in bacteriophage T7 virion structure at the initiation of infection. Virology 340:307–317
Koonin EV, Senkevich TG, Dolja VV (2006) The ancient Virus World and evolution of cells. Biol Direct 1:29
Kropinski AM, Kovalyova IV, Billington SJ et al (2007) The genome of Epsilon15, a serotype-converting, Group E1 Salmonella enterica-specific bacteriophage. Virology 369:234–244
Krylov VN, Smirnova TA, Minenkova IB et al (1984) Pseudomonas bacteriophage phiKZ contains an inner body in its capsid. Can J Microbiol 30:758–762
Lander GC, Tang L, Casjens SR et al (2006) The structure of an infectious P22 virion shows the signal for headful DNA packaging. Science 312:1791–1795
Lavigne R, Seto D, Mahadevan P et al (2008) Unifying classical and molecular taxonomic classification: analysis of the Podoviridae using BLASTP-based tools. Res Microbiol 159:406–414
Lecoutere E, Ceyssens P-J, Miroshnikov K et al (2009) Identification and comparative analysis of the structural proteomes of phiKZ and EL, two giant Pseudomonas aeruginosa bacteriophages. Proteomics 9:3215–3219
Leforestier A, Livolant F (2010) The bacteriophage genome undergoes a succession of intracapsid phase transitions upon DNA ejection. J Mol Biol 396:384–395
Lepault J, Dubochet J, Baschong W et al (1987) Organization of double-stranded DNA in bacteriophages: a study by cryo-electron microscopy of vitrified samples. EMBO J 6:1507–1512
Lhuillier S, Gallopin M, Gilquin B et al (2009) Structure of bacteriophage SPP1 head-to-tail connection reveals mechanism for viral DNA gating. Proc Natl Acad Sci USA 106:8507–8512
Lipinska B, Rao AS, Bolten BM et al (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 X, Zhang Q, Murata K et al (2010) Structural changes in a marine podovirus associated with release of its genome into Prochlorococcus. Nat Struct Mol Biol 17:830–836
Marenduzzo D, Orlandini E, Stasiak A et al (2009) DNA-DNA interactions in bacteriophage capsids are responsible for the observed DNA knotting. Proc Natl Acad Sci USA 106:22269–22274
Matsko N, Klinov D, Manykin A et al (2001) Atomic force microscopy analysis of bacteriophages PhiKZ and T4. J Electron Microsc (Tokyo) 50:417–422
McAllister WT, Wu HL (1978) Regulation of transcription of the late genes of bacteriophage T7. Proc Natl Acad Sci USA 75:804–808
Mendelson EC, Newcomb WW, Brown JC (1992) Ar+ plasma-induced damage to DNA in bacteriophage lambda: implications for the arrangement of DNA in the phage head. J Virol 66:2226–2231
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 I (2004) Peptidoglycan hydrolytic activities associated with bacteriophage virions. Mol Microbiol 51:1169–1183
Molineux IJ (2001) No syringes please, ejection of phage T7 DNA from the virion is enzyme driven. Mol Microbiol 40:1–8
Mullaney JM, Black LW (1996) Capsid targeting sequence targets foreign proteins into bacteriophage T4 and permits proteolytic processing. J Mol Biol 261:372–385
Mullaney JM, Black LW (1998) Activity of foreign proteins targeted within the bacteriophage T4 head and prohead: implications for packaged DNA structure. J Mol Biol 283:913–929
Mullaney JM, Thompson RB, Gryczynski Z et al (2000) Green fluorescent protein as a probe of rotational mobility within bacteriophage T4. J Virol Methods 88:35–40
Overman SA, Aubrey KL, Reilly KE et al (1998) Conformation and interactions of the packaged double-stranded DNA genome of bacteriophage T7. Biospectroscopy 4(5 Suppl):S47–S56
Peñalva MA, Salas M (1982) Initiation of phage phi 29 DNA replication in vitro: formation of a covalent complex between the terminal protein, p3, and 5′-dAMP. Proc Natl Acad Sci USA 79:5522–5526
Petrov AS, Boz MB, Harvey SC (2007) The conformation of double-stranded DNA inside bacteriophages depends on capsid size and shape. J Struct Biol 160:241–248
Rao V, Black L (2010) Structure and assembly of bacteriophage T4 head. Virol J 7:356
Rao VB, Feiss M (2008) The bacteriophage DNA packaging motor. Annu Rev Genet 42:647–681
Ray K, Ma JX, Oram M et al (2010) Single-molecule and FRET fluorescence correlation spectroscopy analyses of phage DNA packaging: colocalization of packaged phage T4 DNA ends within the capsid. J Mol Biol 395:1102–1113
Repoila F, Tetart F, Bouet J-Y et al (1994) Genomic polymorphism in the T-even phages. EMBO J 13:4181–4192
Rickgauer JP, Fuller DN, Grimes S et al (2008) Portal motor velocity and internal force resisting viral DNA packaging in bacteriophage phi29. Biophys J 94:159–167
Rifat D, Wright NT, Varney KM et al (2008) Restriction endonuclease inhibitor IPI* of bacteriophage T4: a novel structure for a dedicated target. J Mol Biol 375:720–734
Saigo K (1975) Tail-DNA connection and chromosome structure in bacteriophage T5. Virology 68:154–165
Saigo K, Uchida H (1974) Connection of the right-hand terminus of DNA to the proximal end of the tail in bacteriophage lambda. Virology 61:524–536
Salmon B, Baines JD (1998) Herpes simplex virus DNA cleavage and packaging: association of multiple forms of U (L) 15-encoded proteins with B capsids requires at least the U(L)6, U(L)17, and U(L)28 genes. J Virol 72:3045–3050
Scraba DG, Bradley RD, Leyritz-Wills M et al (1983) Bacteriophage phi W-14: the contribution of covalently bound putrescine to DNA packing in the phage head. Virology 124:152–160
Serwer P (1986) Arrangement of double-stranded DNA packaged in bacteriophage capsids: an alternative model. J Mol Biol 190:509–512
Serwer P, Wright ET, Hakala KW et al (2008) Evidence for bacteriophage T7 tail extension during DNA injection. BMC Res Notes 1:36
Sheaffer AK, Newcomb WW, Gao M et al (2001) Herpes simplex virus DNA cleavage and packaging proteins associate with the procapsid prior to its maturation. J Virol 75:687–698
Smith DE, Tans SJ, Smith SB et al (2001) The bacteriophage Phi29 portal motor can package DNA against a large internal force. Nature 413:748–752
Sternberg N, Weisberg R (1975) Packaging of prophage and host DNA by coliphage lambda. Nature 256:97–103
Steven AC, Heymann JB, Cheng N et al (2005) Virus maturation: dynamics and mechanism of a stabilizing structural transition that leads to infectivity. Curr Opin Struct Biol 15:227–236
Stiege AC, Isidro A, Dröge A et al (2003) Specific targeting of a DNA-binding protein to the SPP1 procapsid by interaction with the portal oligomer. Mol Microbiol 49:1201–1212
Streiff MB, Iida S, Bickle TA (1987) Expression and proteolytic processing of the darA antirestriction gene product of bacteriophage P1. Virology 157:167–171
Sun M, Serwer P (1997) The conformation of DNA packaged in bacteriophage G. Biophys J 72:958–963
Tang J, Lander Gabriel C, Olia A et al (2011) Peering down the barrel of a bacteriophage portal: the genome packaging and release valve in P22. Structure 19(4):496–502
Thomas JO (1974) Chemical linkage of the tail to the right-hand end of bacteriophage lambda DNA. J Mol Biol 87:1–9
Thomas JA, Rolando MR, Carroll CA et al (2008) Characterization of Pseudomonas chlororaphis myovirus 201phi2-1 via genomic sequencing, mass spectrometry, and electron microscopy. Virology 376:330–338
Thomas JA, Weintraub ST, Hakala K et al (2010) Proteome of the large Pseudomonas myovirus 201φ2-1: delineation of proteolytically processed virion proteins. Mol Cell Proteomics 9:940–951
Wang GR, Vianelli A, Goldberg EB (2000) Bacteriophage T4 self-assembly: in vitro reconstitution of recombinant gp2 into infectious phage. J Bacteriol 182:672–679
Watabe K, Shin M, Ito J (1983) Protein-primed initiation of phage phi 29 DNA replication. Proc Natl Acad Sci USA 80:4248–4252
Witkiewicz H, Schweiger M (1985) A model of lambda DNA arrangement in the viral particle. J Theor Biol 116:587–605
Xiang Y, Morais MC, Battisti AJ et al (2006) Structural changes of bacteriophage phi29 upon DNA packaging and release. EMBO J 25:5229–5239
Yu TY, Schaefer J (2008) REDOR NMR characterization of DNA packaging in bacteriophage T4. J Mol Biol 382:1031–1042
Zachary A, Black LW (1991) Isolation and characterization of a portal protein-DNA complex from dsDNA bacteriophage. Intervirology 33:6–16
Zhang Z, Greene B, Thuman-Commike PA et al (2000) Visualization of the maturation transition in bacteriophage P22 by electron cryomicroscopy. J Mol Biol 297:615–626
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The authors thank Julienne Mullaney, Ian Molineux, and Alasdair Steven for their reading of this manuscript and their helpful suggestions.
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Black, L.W., Thomas, J.A. (2012). Condensed Genome Structure. 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_21
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