The bacteriophage T4 DNA injection machine

https://doi.org/10.1016/j.sbi.2004.02.001 Get rights and content

Abstract

The tail of bacteriophage T4 consists of a contractile sheath surrounding a rigid tube and terminating in a multiprotein baseplate, to which the long and short tail fibers of the phage are attached. Upon binding of the fibers to their cell receptors, the baseplate undergoes a large conformational switch, which initiates sheath contraction and culminates in transfer of the phage DNA from the capsid into the host cell through the tail tube. The baseplate has a dome-shaped sixfold-symmetric structure, which is stabilized by a garland of six short tail fibers, running around the periphery of the dome. In the center of the dome, there is a membrane-puncturing device, containing three lysozyme domains, which disrupts the intermembrane peptidoglycan layer during infection.

Introduction

Bacterial viruses, or bacteriophages, have developed various strategies through which to infect a susceptible bacterial host. Unlike many other viruses (especially those that infect eukaryotic organisms), most of which enter the host by endocytosis, bacteriophages remain attached to the outer cell surface during infection. A vast majority of phages have evolved to use a special organelle, called a ‘tail’, for host recognition, attachment and genome delivery into the cell [1]. The tail is attached to the capsid (or head), containing the phage genome, which is packaged in a process that requires energy derived from ATP hydrolysis.

The order of tailed bacteriophages, Caudovirales, contains three families: Myoviridae, Siphoviridae and Podoviridae [1]. Phages belonging to these three families have contractile, long non-contractile and short non-contractile tails, respectively. Although the tails from all three families are complex macromolecular assemblies, the Myoviridae contractile tails are especially elaborate (Figure 1). For example, more than 20 proteins, each present in multiple copies, comprise the 1200 Å long and 250 Å wide tail of the Myoviridae phage T4 (Table 1) [2]. During infection, the baseplate of the tail attaches the phage particle to the cell surface and undergoes a global conformational change from the ‘hexagonal’ to the ‘star’ conformation. This initiates contraction of the sheath, which drives the tail tube through the cell envelope. Subsequently, the phage genome is passed through the tail tube into the host cytoplasm.

A 12 Å resolution structure of the phage T4 baseplate, obtained by electron cryomicroscopy (cryo-EM), shows that it is a dome-shaped object, approximately 520 Å in diameter and 270 Å high, composed primarily of fibrous proteins [3••]. Crystal structures of six baseplate proteins have been determined by X-ray crystallography and fitted into the cryo-EM map 4., 5.••, 6., 7.•, 8.• (Figure 2). Among these is the tail lysozyme, encoded by gene 5, which is responsible for digesting the intermembrane peptidoglycan layer during infection [5••]. The locations and shapes of other baseplate proteins have also been established, through analysis of the uninterpreted cryo-EM density after fitting the known crystal structures. Based on these structural data and earlier genetic and biochemical results, a mechanism of infection of a Myoviridae phage has been proposed.

Section snippets

Assembly

The protein composition of the tail and the pathway of its assembly have been established (Table 1) 9., 10.; mutants that produce incomplete phage particles have been especially useful in these studies 11., 12., 13.. Assembly of the T4 tail begins with formation of the baseplate, and proceeds with polymerization of the tail tube and the tail sheath. The baseplate is required for initiation of tube assembly. Both the baseplate and the tube are essential for the sheath to adopt the extended

Infection mechanism of a Myoviridae phage T4

Infection is initiated when the long tail fibers interact with the cell surface receptors [lipopolysaccharide molecules or OmpC (surface antigen) proteins]. This interaction is reversible, but when a minimum of three long tail fibers have bound to the host cell receptors, the fibers change their conformation, thereby signaling to the baseplate through gp9 that binding has been successful. Concomitantly, the baseplate is brought into proximity with the cell surface and the short tail fibers

Conclusions

Studies of the bacteriophage T4 baseplate have shown that assembly of large macromolecular complexes can be regulated by sequential interactions of the component proteins but not by the order of gene expression. These experiments have also demonstrated that the multiprotein baseplate, comparable in size and complexity to an average-size icosahedral virus, can undergo large, concerted conformational changes, which coordinate several steps of the phage infection process. Recent structural

References and recommended reading

Papers of particular interest, published within the annual period of review, have been highlighted as:

  • of special interest

  • ••

    of outstanding interest

Acknowledgements

We thank Paul Chipman for providing a cryo-EM photograph of phage T4.

References (52)

  • F Arisaka et al.

    Reassembly of the bacteriophage T4 tail from the core-baseplate and the monomeric sheath protein P18: a co-operative association process

    J Mol Biol

    (1979)
  • J King

    Assembly of the tail of bacteriophage T4

    J Mol Biol

    (1968)
  • N.R Watts et al.

    Structure of the bacteriophage T4 baseplate as determined by chemical cross-linking

    J Virol

    (1990)
  • O.D Veprintseva et al.

    Aberrant form of T4 phage reorganization

    Dokl Akad Nauk SSSR

    (1980)
  • P Chacon et al.

    Multi-resolution contour-based fitting of macromolecular structures

    J Mol Biol

    (2002)
  • R.A Crowther et al.

    Molecular reorganization in the hexagon to star transition of the baseplate of bacteriophage T4

    J Mol Biol

    (1977)
  • L Zhao et al.

    Stoichiometry and inter-subunit interaction of the wedge initiation complex, gp10-gp11, of bacteriophage T4

    Biochim Biophys Acta

    (2000)
  • E Kellenberger et al.

    Functions and properties related to the tail fibers of bacteriophage T4

    Virology

    (1965)
  • E Kellenberger et al.

    Mechanism of the long tail-fiber deployment of bacteriophages T-even and its role in adsorption, infection and sedimentation

    Biophys Chem

    (1996)
  • Eiserling FA, Black LW: Pathways in T4 morphogenesis. In Molecular Biology of Bacteriophage T4. Edited by Karam JD....
  • S Kanamaru et al.

    The C-terminal fragment of the precursor tail lysozyme of bacteriophage T4 stays as a structural component of the baseplate after cleavage

    J Bacteriol

    (1999)
  • A.G Murzin et al.

    Protein architecture: new superfamilies

    Curr Opin Struct Biol

    (1992)
  • G Mosig et al.

    Functional relationships and structural determinants of two bacteriophage T4 lysozymes: a soluble (gene e) and a baseplate-associated (gene 5) protein

    New Biol

    (1989)
  • B.W Matthews et al.

    The three dimensional structure of the lysozyme from bacteriophage T4

    Proc Natl Acad Sci USA

    (1974)
  • F Tetart et al.

    Phylogeny of the major head and tail genes of the wide-ranging T4-type bacteriophages

    J Bacteriol

    (2001)
  • M.J van Raaij et al.

    Crystal structure of a heat and protease-stable part of the bacteriophage T4 short tail fibre

    J Mol Biol

    (2001)
  • Cited by (147)

    • Host range and cell recognition of archaeal viruses

      2024, Current Opinion in Microbiology
    • Bacterial adhesion

      2023, Molecular Medical Microbiology, Third Edition
    • Major tail proteins of bacteriophages of the order Caudovirales

      2022, Journal of Biological Chemistry
      Citation Excerpt :

      The portal complex is sealed off by the binding of the gp13–gp14 neck complex completing the head (44). Tail assembly commences by the association of the baseplate that consists of six wedges joined around a central tube (45, 46). The baseplate is appended at the proximal end by hexameric rings of gp48 and gp54, which act as hub for tail tube polymerization (47), and by gp27, gp5, and gp5.4 at the distal end forming the tail tip.

    • Principles of Virus Structure

      2020, Encyclopedia of Virology: Volume 1-5, Fourth Edition
    View all citing articles on Scopus
    View full text