Bacteriophages: Structure

Abstract

Bacterial viruses, or bacteriophages, are ubiquitous organisms spanning very different ecological niches. Although genome comparison fails to show extensive relationship among bacteriophages, recent structural studies reveal a high degree of similarities. Most bacteriophages present an icosahedral proteinaceous head, which contains the nucleic acid, either deoxyribonucleic acid (DNA) or ribonucleic acid (RNA). Exceptions to this rule are few cases where a lipid envelope forms part of the head, and those other cases where the head presents a filamentous geometry. The way bacteriophages infect the host cell is the basis of a main difference among them: one group (Caudovirales) has a specialised structure (the tail) that is responsible for the recognition of the host cell and the viral genome delivery, whereas those bacteriophages without tail present a variety of infecting strategies. In this study we will deal with the main common characteristics of bacteriophage heads and tails supporting their common evolutionary origin.

Key Concepts:

  • Bacteriophages share extended structural and functional similarities.

  • Bacteriophages are excellent examples of optimisation of genetic information to carry out complex functions.

  • Most bacteriophages enclose their nucleic acid in a protein container (built by multiple copies of one (or a few) proteins), and in a few cases they may include lipid envelopes.

  • The most conserved geometry in bacteriophage heads is icosahedral.

  • Double stranded DNA icosahedral bacteriophages follow a common assembly pathway.

  • The Caudovirales group (bacteriophages with icosahedral heads, dsDNA and a tail) are the most abundant virus type.

  • The packaging of dsDNA inside Caudovirales requires energy conversion (ATP hydrolysis) into mechanical translocation, and it is carried out by a dedicated viral machinery.

  • The maturation of icosahedral proheads into viral heads involves drastic reorganisations of the capsid components leading to more stable particles.

  • The tail of Caudovirales is a sophisticated machinery involved in cell recognition and nucleic acids delivery.

  • There are three main architectural designs of bacteriophage tails, each one adapting to different host interaction strategies.

Keywords: bacteriophage; structure; phage assembly; bacterial virus; maturation

Figure 1.

Structure of bacteriophage proheads. (a) Three‐dimensional reconstruction of bacteriophage T7 proheads, this research was originally published in Ionel et al., the American Society for Biochemistry and Molecular Biology Inc. (b) Structure of P22 prohead at 0.4 nm resolution (Chen et al., ). (c) P22 prohead showing the singular 5‐fold vertex where the portal attaches (Reproduced with permission from Chen et al., copyright, PNAS). (d) Central section of the P22 prohead showing the internal scaffold (red) and the portal‐core complex (grey) (Reproduced with permission from Chen et al., copyright, PNAS). The bar represents 20 nm. (e), ribbon representation from the structures of the major shell protein of bacteriophages HK97 (PDB 1ohg) (upper), T7 (PDB 3izg) (middle) and T4 (PDB 1yue) (lower).

Figure 2.

Structure of connector complexes. (a) P22 connector. Reproduced with permission from Tang et al. copyright, Elsevier. (b) T7 connector. Reproduced with permission from Agirrezabala et al. copyright, Elsevier. (c) Ribbon representation of the connector proteins of phage ϕ29, SPP1 and C‐terminal truncated P22 (from left to right). Reproduced with permission from Cuervo and Carrascosa copyright, Elsevier. The dotted area marks the common α helical structural signature of the connector protein.

Figure 3.

Structure of mature bacteriophage. (a) Structure of P22 mature virion. Reproduced with permission from Tang et al. copyright, Elsevier. Head is depicted in blue, and the tail components in yellow, pink and cyan. (b) Central section of the P22 virion showing the outline of the shell (blue), DNA layers (green), portal complex (red) and tail components (yellow, pink, blue and orange). Reproduced with permission from Tang et al. copyright, Elsevier. (c) Detail of the interaction between the connector (grey) and the capsid shell (blue). The DNA is depicted in green along the portal channel (Reproduced with permission from Tang et al., copyright, Elsevier). (d) High resolution (0.45 nm) model of the ɛ‐15 bacteriophage shell. The seven subunits of the asymmetric unit are labelled with different colours. Reproduced with permission from Jiang et al., copyright, Nature Publishing Group.

Figure 4.

Structural modifications involved in the maturation of the bacteriophage shell. (a) and (b) Central sections of, respectively, the prohead and mature head shells of phage T7. Reproduced with permission from Ionel et al., copyright, The American Society for Biochemistry and Molecular Biology Inc. (c) Relative movements of the structural domains of the major shell protein of phage HK97 which take place during head maturation. Prohead subunit is yellow and head subunit is green. The invariant P‐domain in both subunits is depicted in blue. Reproduced with permission from Gertsman et al., copyright, Naure Publishing Group. (d) and (e) Asymmetric units of prohead and mature head of T7, respectively. The translucent electron density model is fitted in each case with the ribbon representation of the major shell protein. Reproduced with permission from Ionel et al., copyright, The American Society for Biochemistry and Molecular Biology Inc.

Figure 5.

(a) Negative staining electron microscopy images of bacteriophages belonging to the three Caudovirales families from left to right SPP1 (Syphoviridae). Reproduced with permission from Plisson et al., copyright, Nature Publishing Group. T4 (Myoviridae) and ϕ29 (Podoviridae). The bar represents 50 nm. (b) Three‐dimensional electron microscopy reconstructions obtained from different bacteriophage tails. Upper left panel, fragment of P2 tail (Syphoviridae) showing the tail tube (blue) and the baseplate (yellow). Reproduced with permission from Veesler and Cambillau , copyright, The American Society of Microbiology. Bottom left panel, final part of the SPP1 tail (Syphoviridae), the tail cap (green) and the tail tip (pink) are shown. Reproduced with permission from Plisson et al., copyright, Nature Publishing Group. Central panel, T4 tail (Myoviridae) in a contracted conformation showing the sheath (gp18 in green), the tail tube (gp19 in pink), the baseplate (gp7–12, in red, dark blue, yellow, light green, light blue and purple, respectively), the fibres (gp14 in white) and the neck (gp13‐15 in light purple and orange, respectively). Reproduced with permission from Leiman et al., copyright, Elsevier. Upper right panel, ϕ29 tail (Podoviridae), showing the appendages in purple, the collar in green and the knob in blue. Reproduced with permission from Tang et al., copyright, Elsevier. Bottom panel, P22 tail (Podoviridae) showing the tail adaptor protein (pink), the tail knob (green), the spikes (blue) and the needle (yellow). Reproduced with permission from Lander et al., copyright, Elsevier.

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References

Ackermann HW (2007) 5500 Phages examined in the electron microscope. Archives of Virology 152(2): 227–243.

Agirrezabala X, Martin‐Benito J, Caston JR et al. (2005a) Maturation of phage T7 involves structural modification of both shell and inner core components. EMBO Journal 24(21): 820–829.

Agirrezabala X, Martin‐Benito J, Valle M et al. (2005b) Structure of the connector of bacteriophage T7 at 8A resolution: structural homologies of a basic component of a DNA translocating machinery. Journal of Molecular Biology 347(5): 895–902.

Aksyuk AA and Rossmann MG (2011) Bacteriophage assembly. Viruses 3: 172–203.

Bartual SG, Otero JM, Garcia‐Doval C et al. (2010) Structure of the bacteriophage T4 long tail fiber receptor‐binding tip. Proceedings of the National Academy of Sciences of the USA 107(47): 20287–20292.

Cardarelli L, Pell LG, Neudecker P et al. (2010) Phages have adapted the same protein fold to fulfill multiple functions in virion assembly. Proceedings of the National Academy of Sciences of the USA 107(32): 14384–14389.

Caspar DL and Klug A (1962) Physical principles in the construction of regular viruses. Cold Spring Harbor Symposia on Quantitative Biology 27: 1–24.

Cerritelli ME, Conway JF, Cheng N, Trus BL and Steven AC (2003) Molecular mechanisms in bacteriophage T7 procapsid assembly, maturation, and DNA containment. Advances in Protein Chemistry 64: 301–323.

Chen DH, Baker ML, Hryc CF et al. (2011) Structural basis for scaffolding‐mediated assembly and maturation of a dsDNA virus. Proceedings of the National Academy of Sciences of the USA 108(4): 1355–1360.

Conway JF, Wikoff WR, Cheng N et al. (2001) Virus maturation involving large subunit rotations and local refolding. Science 292(5517): 744–748.

Crick FH and Watson JD (1956) Structure of small viruses. Nature 177(4506): 473–475.

Cuervo A and Carrascosa JL (2011) Viral connectors for DNA encapsulation. Current Opinion in Biotechnology.

Fokine A, Chipman PR, Leiman PG et al. (2004) Molecular architecture of the prolate head of bacteriophage T4. Proceedings of the National Academy of Sciences of the USA 101(16): 6003–6008.

Gertsman I, Gan L, Guttman M et al. (2009) An unexpected twist in viral capsid maturation. Nature 458(7238): 646–650.

Guasch A, Pous J, Ibarra B et al. (2002) Detailed architecture of a DNA translocating machine: the high‐resolution structure of the bacteriophage phi29 connector particle. Journal of Molecular Biology 315(4): 663–676.

Hendrix RW (2002) Bacteriophages: evolution of the majority. Theoretical Population Biology 61(4): 471–480.

Ionel A, Velazquez‐Muriel JA, Luque D et al. (2011) Molecular rearrangements involved in the capsid shell maturation of bacteriophage T7. Journal of Biological Chemistry 286(1): 234–242.

Jiang W, Baker ML, Jakana J et al. (2008) Backbone structure of the infectious epsilon15 virus capsid revealed by electron cryomicroscopy. Nature 451(7182): 1130–1134.

Johnson JE (2010) Virus particle maturation: insights into elegantly programmed nanomachines. Current Opinion in Structural Biology 20(2): 210–216.

Lander GC, Khayat R, Li R et al. (2009) The P22 tail machine at subnanometer resolution reveals the architecture of an infection conduit. Structure 17(6): 789–799.

Lebedev AA, Krause MH, Isidro AL et al. (2007) Structural framework for DNA translocation via the viral portal protein. EMBO Journal 26(7): 1984–1994.

Leiman PG, Chipman PR, Kostyuchenko VA, Mesyanzhinov VV and Rossmann MG (2004) Three‐dimensional rearrangement of proteins in the tail of bacteriophage T4 on infection of its host. Cell 118(4): 419–429.

Leiman PG, Arisaka F, van Raaij MJ et al. (2010) Morphogenesis of the T4 tail and tail fibers. Virology Journal 7: 355.

Lhuillier S, Gallopin M, Gilquin B et al. (2009) Structure of bacteriophage SPP1 head‐to‐tail connection reveals mechanism for viral DNA gating. Proceedings of the National Academy of Sciences of the USA 106(21): 8507–8512.

Lorenzen K, Olia AS, Uetrecht C, Cingolani G and Heck AJ (2008) Determination of stoichiometry and conformational changes in the first step of the P22 tail assembly. Journal of Molecular Biology 379(2): 385–396.

Maxwell KL , Yee AA, Arrowsmith CH, Gold M and Davidson AR (2002) The solution structure of the bacteriophage lambda head‐tail joining protein, gpFII. Journal of Molecular Biology 318(5): 1395–1404.

Muller JJ, Barbirz S, Heinle K et al. (2008) An intersubunit active site between supercoiled parallel beta helices in the trimeric tailspike endorhamnosidase of Shigella flexneri Phage Sf6. Structure 16(5): 766–775.

Murphy FA, Fauquet CM, Bishop DHL et al. (1995) Virus Taxonomy. Wien, New York: Springer‐Verlag.

Olia AS, Casjens S and Cingolani G (2007) Structure of phage P22 cell envelope‐penetrating needle. Nature Structural & Molecular Biology 14(12): 1221–1226.

Olia AS, Prevelige PE Jr, Johnson JE and Cingolani G (2011) Three‐dimensional structure of a viral genome‐delivery portal vertex. Nature Structural & Molecular Biology 18(5): 597–603.

Parent KN, Khayat R, Tu LH et al. (2010) P22 coat protein structures reveal a novel mechanism for capsid maturation: stability without auxiliary proteins or chemical crosslinks. Structure 18(3): 390–401.

Pell LG, Kanelis V, Donaldson LW, Howell PL and Davidson AR (2009) The phage lambda major tail protein structure reveals a common evolution for long‐tailed phages and the type VI bacterial secretion system. Proceedings of the National Academy of Sciences of the USA 106(11): 4160–4165.

Plisson C, White HE, Auzat I et al. (2007) Structure of bacteriophage SPP1 tail reveals trigger for DNA ejection. EMBO Journal 26(15): 3720–3728.

Poranen MM, Daugelavicius R and Bamford DH (2005) Common principles in viral entry. Annual Review of Microbiology 56: 521–538.

Rossmann MG and Rao VB (2012) Viruses: sophisticated biological machines. Advances in Experimental Medicine and Biology 726: 1–3.

Sciara G, Bebeacua C, Bron P et al. (2010) Structure of lactococcal phage p2 baseplate and its mechanism of activation. Proceedings of the National Academy of Sciences of the USA 107(15): 6852–6857.

Simpson AA, Tao Y, Leiman PG et al. (2000) Structure of the bacteriophage phi29 DNA packaging motor. Nature 408(6813): 745–750.

Steven AC and Carrascosa JL (1979) Proteolytic cleavage and structural transformation: their relationship in bacteriophage T4 capsid maturation. Journal of Supramolecular Structure 10(1): 1–11.

Sun S, Rao VB and Rossmann MG (2010) Genome packaging in viruses. Current Opinion in Structural Biology 20(1): 114–120.

Tang J, Olson N, Jardine PJ et al. (2008) DNA poised for release in bacteriophage phi29. Structure 16(6): 935–943.

Tang J, Lander GC, Olia AS et al. (2011) Peering down the barrel of a bacteriophage portal: the genome packaging and release valve in p22. Structure 19(4): 496–502.

Valpuesta JM and Carrascosa JL (1994) Structure of viral connectors and their function in bacteriophage assembly and DNA packaging. Quarterly Reviews of Biophysics 27: 107–155.

Valpuesta JM, Fernandez JJ, Carazo JM and Carrascosa JL (1999) The three‐dimensional structure of a DNA translocating machine at 10 A resolution. Structure 7(3): 289–296.

Veesler D and Cambillau C (2011) A common evolutionary origin for tailed‐bacteriophage functional modules and bacterial machineries. Microbiology and Molecular Biology Reviews 75(3): 423–433.

Wikoff WR, Liljas L, Duda RL et al. (2000) Topologically linked protein rings in the bacteriophage HK97 capsid. Science 289(5487): 2129–2133.

Xiang Y, Morais MC, Battisti AJ et al. (2006) Structural changes of bacteriophage phi29 upon DNA packaging and release. EMBO Journal 25(21): 5229–5239.

Xiang Y, Leiman PG, Li L et al. (2009) Crystallographic insights into the autocatalytic assembly mechanism of a bacteriophage tail spike. Molecular Cell 34(3): 375–386.

Yang F, Forrer P, Dauter Z et al. (2000) Novel fold and capsid‐binding properties of the lambda‐phage display platform protein gpD. Nature Structural Biology 7(3): 230–237.

Further Reading

Bamford DH, Grimes JM and Stuart DI (2005) What does structure tell us about virus evolution? Current Opinion in Structural Biology 15: 655–663.

Black LW (1989) DNA packaging in dsDNA bacteriophages. Annual Review of Microbiology 43: 267–292.

Casjens S and Hendrix RW (1988) Control mechanisms in dsDNA bacteriophage assembly. In: Calendar R (ed.) The Bacteriophages, pp. 15–90. New York: Plenum Press.

Casjens SR (2011) The DNA‐packaging nanomotor of tailed bacteriophages. Nature Review of Microbiology 9: 647–657.

Catalano CE (2005) In Viral Genome Packaging Machines: Genetics, Structure and Mechanism. New York: Kluwer Academic/Plenum Publishers.

Hendrix RW, Smith MC, Burns RN, Ford ME and Hatfull GF (1999) Evolutionary relationships among diverse bacteriophages and prophages: all the world's a phage. Proceedings of the National Academy of Sciences of the USA 96: 2192–2197.

Steven AC, Heymann JB, Cheng N, Trus BL and Conway JF (2005) Virus maturation: dynamics and mechanism of a stabilizing structural transition that leads to infectivity. Current Opinion in Structural Biology 15: 227–236.

Vinga I, Sao‐José C, Tavares P and Santos M (2006) Bacteriophage entry in the host cell. In: Wegrzn G (ed.) Modern Bacteriophage Biology and Biotechnology, pp. 165–205. Kerala: Research SignPost.

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Cuervo, Ana, and Carrascosa, José L(Jun 2012) Bacteriophages: Structure. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0024053]