Advertisement

Biophysical Reviews

, Volume 10, Issue 2, pp 463–471 | Cite as

Bacteriophage T4 long tail fiber domains

  • Paul Hyman
  • Mark van Raaij
Review

Abstract

Bacteriophage T4 initially recognizes its host cells using its long tail fibers. Long tail fibers consist of a phage-proximal and a phage-distal rod, each around 80 nm long and attached to each other at a slight angle. The phage-proximal rod is formed by a homo-trimer of gene product 34 (gp34) and is attached to the phage-distal rod by a monomer of gp35. The phage-distal rod consists of two protein trimers: a trimer of gp36, attached to gp35, although most of the phage-distal rod, including the receptor-binding domain, is formed by a trimer of gp37. In this review, we discuss what is known about the detailed structure and function of the different long tail fiber domains. Partial crystal structures of gp34 and gp37 have revealed the presence of new protein folds, some of which are present in several repeats, while others are apparently unique. Gp38, a phage chaperone protein necessary for folding of gp37, is thought to act on an α-helical coiled-coil region in gp37. Future studies should reveal the remaining structure of the long tail fibers, how they assemble into a functional unit, and how the long tail fibers trigger the infection process after successful recognition of a suitable host bacterium.

Keywords

Bacteriophage T4 Long tail fiber Assembly Protein folds α-Helical coiled-coil β-Structure 

Notes

Acknowledgements

The authors wish to thank the reviewers for their comments which helped improved the paper. We also want to thank Fred Eiserling for the drawing of bacteriophage T4 that appears in the upper part of Fig. 1a.

Compliance with ethical standards

Conflicts of interest

Paul Hyman declares that he has no conflicts of interest. Mark van Raaij declares that he has no conflicts of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

References

  1. Ackermann HW (2003) Bacteriophage observations and evolution. Res Microbiol 154:245–251CrossRefPubMedGoogle Scholar
  2. Alva V, Nam SZ, Soding J, Lupas AN (2016) The MPI bioinformatics toolkit as an integrative platform for advanced protein sequence and structure analysis. Nucleic Acids Res 44:W410–W415CrossRefPubMedPubMedCentralGoogle Scholar
  3. Ares P, Garcia-Doval C, Llauro A, Gomez-Herrero J, van Raaij MJ, de Pablo PJ (2014) Interplay between the mechanics of bacteriophage fibers and the strength of virus-host links. Phys Rev E Stat Nonlinear Soft Matter Phys 89:052710CrossRefGoogle Scholar
  4. Bartual SG, Garcia-Doval C, Alonso J, Schoehn G, van Raaij MJ (2010a) Two-chaperone assisted soluble expression and purification of the bacteriophage T4 long tail fibre protein gp37. Protein Expr Purif 70:116–121CrossRefPubMedGoogle Scholar
  5. Bartual SG, Otero JM, Garcia-Doval C, Llamas-Saiz AL, Kahn R, Fox GC, van Raaij MJ (2010b) Structure of the bacteriophage T4 long tail fiber receptor-binding tip. Proc Natl Acad Sci USA 107:20287–20292CrossRefPubMedPubMedCentralGoogle Scholar
  6. Bishop RJ, Conley MP, Wood WB (1974) Assembly and attachment of bacteriophage T4 tail fibers. J Supramol Struct 2:196–201CrossRefPubMedGoogle Scholar
  7. Bishop RJ, Wood WB (1976) Genetic analysis of T4 tail fiber assembly. I. A gene 37 mutation that allows bypass of gene 38 function. Virology 72:244–254CrossRefPubMedGoogle Scholar
  8. Branden C, Tooze J (1999) Introduction to protein structure. Garland Publishing, New YorkGoogle Scholar
  9. Cerritelli ME, Wall JS, Simon MN, Conway JF, Steven AC (1996) Stoichiometry and domainal organization of the long tail-fiber of bacteriophage T4: a hinged viral adhesin. J Mol Biol 260:767–780CrossRefPubMedGoogle Scholar
  10. Crawford JT, Goldberg EB (1980) The function of tail fibers in triggering baseplate expansion of bacteriophage T4. J Mol Biol 139:679–690CrossRefPubMedGoogle Scholar
  11. Earnshaw WC, Goldberg EB, Crowther RA (1979) The distal half of the tail fibre of bacteriophage T4. Rigidly linked domains and cross-beta structure. J Mol Biol 132:101–113CrossRefPubMedGoogle Scholar
  12. Goldberg E, Grinius L, Letellier L (1994) Recognition, attachment, and injection. In: Karam JD, Kutter E, Carlson K, Guttman B (eds) The molecular biology of bacteriophage T4. ASM Press, Washington, DC, pp 347–356Google Scholar
  13. Granell M, Namura M, Alvira S, Garcia-Doval C, Singh AK, Gutsche I, van Raaij MJ, Kanamaru S (2014) Crystallization of the carboxy-terminal region of the bacteriophage T4 proximal long tail fibre protein gp34. Acta Crystallogr F Struct Biol Commun 70:970–975CrossRefPubMedPubMedCentralGoogle Scholar
  14. Granell M, Namura M, Alvira S, Kanamaru S, van Raaij MJ (2017) Crystal structure of the carboxy-terminal region of the bacteriophage T4 proximal long tail fiber protein Gp34. Viruses 9.  https://doi.org/10.3390/v9070168
  15. Hashemolhosseini S, Montag D, Kramer L, Henning U (1994) Determinants of receptor specificity of coliphages of the T4 family. A chaperone alters the host range. J Mol Biol 241:524–533CrossRefPubMedGoogle Scholar
  16. Henikoff S, Henikoff JG (1992) Amino acid substitution matrices from protein blocks. Proc Natl Acad Sci USA 89:10915–10919CrossRefPubMedPubMedCentralGoogle Scholar
  17. Hu B, Margolin W, Molineux IJ, Liu J (2015) Structural remodeling of bacteriophage T4 and host membranes during infection initiation. Proc Natl Acad Sci USA 112:E4919–E4928CrossRefPubMedPubMedCentralGoogle Scholar
  18. Hyman P, Harrah T (2014) Bacteriophage T4 tail fibers as a basis for structured assemblies. American Society of Mechanical Engineers, New YorkGoogle Scholar
  19. Hyman P, Valluzzi R, Goldberg E (2002) Design of protein struts for self-assembling nanoconstructs. Proc Natl Acad Sci USA 99:8488–8493CrossRefPubMedPubMedCentralGoogle Scholar
  20. King J, Laemmli UK (1971) Polypeptides of the tail fibres of bacteriophage T4. J Mol Biol 62:465–477CrossRefPubMedGoogle Scholar
  21. Koc C, Xia G, Kuhner P, Spinelli S, Roussel A, Cambillau C, Stehle T (2016) Structure of the host-recognition device of Staphylococcus aureus phage varphi11. Sci Rep 6:27581CrossRefPubMedPubMedCentralGoogle Scholar
  22. Kreuzer K, Morrical SW (1994) Initiation of DNA replication. In: Karam JD, Drake JW, Kreuzer KN (eds) Molecular biology of bacteriophage T4. ASM Press, Washington, DC, pp 28–42Google Scholar
  23. Kuwabara N, Manya H, Yamada T, Tateno H, Kanagawa M, Kobayashi K, Akasaka-Manya K, Hirose Y, Mizuno M, Ikeguchi M, Toda T, Hirabayashi J, Senda T, Endo T, Kato R (2016) Carbohydrate-binding domain of the POMGnT1 stem region modulates O-mannosylation sites of alpha-dystroglycan. Proc Natl Acad Sci USA 113:9280–9285Google Scholar
  24. Leiman PG, Arisaka F, van Raaij MJ, Kostyuchenko VA, Aksyuk AA, Kanamaru S, Rossmann MG (2010) Morphogenesis of the T4 tail and tail fibers. Virol J 7:355CrossRefPubMedPubMedCentralGoogle Scholar
  25. Leiman PG, Chipman PR, Kostyuchenko VA, Mesyanzhinov VV, Rossmann MG (2004) Three-dimensional rearrangement of proteins in the tail of bacteriophage T4 on infection of its host. Cell 118:419–429CrossRefPubMedGoogle Scholar
  26. Leiman PG, Kostyuchenko VA, Shneider MM, Kurochkina LP, Mesyanzhinov VV, Rossmann MG (2000) Structure of bacteriophage T4 gene product 11, the interface between the baseplate and short tail fibers. J Mol Biol 301:975–985CrossRefPubMedGoogle Scholar
  27. Leiman PG, Shneider MM, Mesyanzhinov VV, Rossmann MG (2006) Evolution of bacteriophage tails: structure of T4 gene product 10. J Mol Biol 358:912–921CrossRefPubMedGoogle Scholar
  28. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE (2004) UCSF chimera—a visualization system for exploratory research and analysis. J Comput Chem 25:1605–1612CrossRefPubMedGoogle Scholar
  29. Prasad BV, Schmid MF (2012) Principles of virus structural organization. Adv Exp Med Biol 726:17–47CrossRefPubMedPubMedCentralGoogle Scholar
  30. Qu Y, Hyman P, Harrah T, Goldberg E (2004) In vivo bypass of chaperone by extended coiled-coil motif in T4 tail fiber. J Bacteriol 186:8363–8369CrossRefPubMedPubMedCentralGoogle Scholar
  31. Riede I, Drexier K, Eschbach ML (1985) The nucleotide sequences of the tail fiber gene 36 of bacteriophage T2 and of genes 36 of the T-even type Escherichia coli phages K3 and Ox2. Nucleic Acids Res 13:605–616CrossRefPubMedPubMedCentralGoogle Scholar
  32. Riek R, Choe S, Greenwald J, Roosild T, Vega M (2007) Compositions and methods for producing recombinant proteins. The Salk Institute for Biological Studies, La Jolla, CA. Patent application EP20050855418. WITO International Application No. PCT/US2005/046853. Date of application (USA) 21 December 2005Google Scholar
  33. Sainz-Polo MA, Gonzalez B, Menendez M, Pastor FI, Sanz-Aparicio J (2015) Exploring multimodularity in plant cell wall deconstruction: structural and functional analysis of Xyn10C containing the Cbm22-1-Cbm22-2 tandem. J Biol Chem 290:17116–17130CrossRefPubMedPubMedCentralGoogle Scholar
  34. 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 32:279–297CrossRefPubMedGoogle Scholar
  35. Snyder M, Wood WB (1989) Genetic definition of two functional elements in a bacteriophage T4 host-range “cassette”. Genetics 122:471–479PubMedPubMedCentralGoogle Scholar
  36. Taylor NM, Prokhorov NS, Guerrero-Ferreira RC, Shneider MM, Browning C, Goldie KN, Stahlberg H, Leiman PG (2016) Structure of the T4 baseplate and its function in triggering sheath contraction. Nature 533:346–352CrossRefPubMedGoogle Scholar
  37. Thomassen E, Gielen G, Schutz M, Schoehn G, Abrahams JP, Miller S, van Raaij MJ (2003) The structure of the receptor-binding domain of the bacteriophage T4 short tail fibre reveals a knitted trimeric metal-binding fold. J Mol Biol 331:361–373CrossRefPubMedGoogle Scholar
  38. van Raaij MJ, Mitraki A (2004) Beta-structured viral fibres: assembly, structure and implications for materials design. Curr Opinion Solid State Mater Sci 8:151–156CrossRefGoogle Scholar
  39. van Raaij MJ, Schoehn G, Burda MR, Miller S (2001) Crystal structure of a heat and protease-stable part of the bacteriophage T4 short tail fibre. J Mol Biol 314:1137–1146CrossRefPubMedGoogle Scholar
  40. Ward S, Luftig RB, Wilson JH, Eddleman H, Lyle H, Wood WB (1970) Assembly of bacteriophage T4 tail fibers. II. Isolation and characterization of tail fiber precursors. J Mol Biol 54:15–31CrossRefPubMedGoogle Scholar
  41. Washizaki A, Yonesaki T, Otsuka Y (2016) Characterization of the interactions between Escherichia coli receptors, LPS and OmpC, and bacteriophage T4 long tail fibers. Microbiology 5:1003–1015Google Scholar
  42. Wood WB, Bishop RJ (1973) Bacteriophage T4 tail fibers: structure and assembly of a viral organelle. In: Fox CF, Robinson WS (eds) Virus research. Academic Press, New York, pp 303–304Google Scholar
  43. Wood WB, Crowther RA (1983) Long tail fibers: genes, proteins, assembly, and structure. In: Mathews CK, Kutter EM, Mosig G, Berget PB (eds) Bacteriophage T4. American Society for Microbiology, Washington, DC, pp 259–269Google Scholar

Copyright information

© International Union for Pure and Applied Biophysics (IUPAB) and Springer-Verlag GmbH Germany, part of Springer Nature 2017

Authors and Affiliations

  1. 1.Department of Biology/ToxicologyAshland UniversityAshlandUSA
  2. 2.Departamento de Estructura de MacromoleculasCentro Nacional de Biotecnologia (CNB–CSIC)MadridSpain

Personalised recommendations