Bacteriophages: Tailed

Abstract

Tailed bacteriophages are a widely distributed order of viruses that infect bacteria and Archaea. They all have a double‐stranded deoxyribonucleic acid (DNA) chromosome that is protected by an icosahedral capsid with a tail attached to one vertex. The tail is a specialised organelle that recognises the host and transfers the phage chromosome from inside the capsid to the host cytoplasm. Tails exhibit diverse morphologies that are divided into the three main classes: (1) short, (2) long and flexible and (3) long and contractile, that are used to define the three families of phage. The DNA‐filled capsids are icosahedral in shape, come in a range of sizes and are sometimes elongated along the tail axis. During infection, a phage may immediately take over the host to make new virions and lyse the cell (lytic cycle), or it may enter a dormant state, often by integrating its genome into the host genome (lysogenic cycle).

Key Concepts

  • Tailed bacteriophages are widespread in nature, but quite variable in size, shape and genetic content.
  • During infection, phages may deliver both their DNA chromosome and proteins into the infected cell in order to take over the cell and replicate.
  • Phage DNA replication mechanisms vary widely, but they usually make a large molecule that contains multiple copies of the phage genome that is used for packaging.
  • New phage particles are built using separate assembly pathways for capsids, tails and tail fibers.
  • Capsids are built as empty precursors using a scaffold that is discarded and tails are only added after the capsids are filled with DNA.
  • Tailed bacteriophages very likely evolved from a common ancestor.

Keywords: virus; bacteriophage; tail; icosahedral capsid; assembly pathway; DNA packaging; scaffolding protein; terminase

Figure 1. The three families of tailed bacteriophage. (a) Schematic of the structure of Siphoviridae (left), Myoviridae (middle) and Podoviridae (right) phages. The difference is based on the tail morphology (see text). Some of the structural components for each type of tail are indicated in the figure. It should be noted that the side tail fibers could also be present on Siphoviridae or Podoviridae phages. (b) Observation of representative members of each family by electron microscopy. The phages T4 (Myoviridae), T5 (Siphoviridae) and T7 (Podoviridae) have been negatively stained by uranyl acetate and imaged on the same grid. The three insets show the three phages at a higher magnification.
Figure 2. Analysis of the sequenced genomes of the tailed bacteriophage. The genome information was obtained from the National Center for Biotechnology (NCBI), http://www.ncbi.nlm.nih.gov/genomes/GenomesGroup.cgi?taxid=28883. About 1700 tailed bacteriophage genomes were used for this analysis. (a) Proportion of each family of phages among the sequence phages. (b) Distribution of genome sizes in the three tailed phage families. The genome size is correlated to the capsid size as illustrated by the 3D reconstruction of the capsids of the phages T4 (EMD‐1414), T5 (Effantin et al., ) and T7 (EMD‐1810). (EMD, Electron Microscopy Data Bank). The colours indicate the family: blue (Siphoviridae), orange (Myoviridae) and green (Podoviridae).
Figure 3. Assembly scheme of a tailed bacteriphage: example for a Siphoviridae. On the top, assembly of the capsid starting from the required elements that are the major capsid protein (that can make both the penton and the hexon), the scaffold (that can be an independent protein or fused to the major capsid protein), a protease and the portal (present in every bacteriophage in 12 copies at only one vertex). The final capsid can bind a ‘head to tail connector’ that allows the binding of the assembled tail (bottom). The assembly of Siphoviridae tails requires chaperones, tape measure proteins, an assembled tail tip and the major tail protein as shown in the figure and described in the text. Assembly of Myoviridae tails exhibits many similarities as described in the text while Podoviridae tail assembly is very different as it takes place directly on the portal complex.
Figure 4. Proteins of tailed bacteriophages often have similarities with other biological species, but sometimes the similarities cannot be detected by comparing the protein sequences and can only be discovered by comparing the structures of the protein. The comparison in the figure shows an example of conserved structural similarities of this type. The ‘HK97 fold’, initially found in the HK97 bacteriophage major capsid protein, has been also found in the capsids of eukaryotic viruses of the Herpesvirus family as well as in the protein shells of the bacterial and archeal compartments called encapsulins. These results suggest that they are all derived from a common ancestor.
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Further Reading

Cairns J, Stent GS and Watson JD (eds) (1992) Phage and the Origins of Molecular Biology, expanded edition. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.

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Rossmann MG and Rao VB (eds) (2012) Viral Molecular Machines. New York: Springer.

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Duda, Robert L, and Huet, Alexis(Jun 2016) Bacteriophages: Tailed. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0000782.pub3]