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The DNA-packaging nanomotor of tailed bacteriophages

Nature Reviews Microbiology volume 9, pages 647–657 (2011)Cite this article

Subjects

Key Points

  • Tailed bacteriophages package their double-stranded DNA chromosomes into preformed protein containers called procapsids.

  • The DNA-packaging process condenses the DNA several-hundred-fold and requires chemical energy. The result of this condensation is DNA that is arranged as a tightly wound, imperfect solenoid that is held within the virion with no proteins holding the DNA strands close together.

  • The molecular motor that packages DNA within the procapsid is a DNA translocase that is composed of three proteins: portal protein, which forms the hole through which DNA enters the procapsid, and also senses when the capsid is full of DNA; small terminase subunit (TerS), which recognizes the DNA that will be packaged; and large terminase subunit (TerL), the ATPase that converts the chemical energy of ATP hydrolysis into physical motion of the DNA.

  • In the phages that package over-length or circular DNA, TerL also contains a nuclease activity that cuts the DNA to form the unit-length, linear DNA molecules that are found in completed virions.

  • Single-molecule experiments have shown that the DNA-packaging motor can insert DNA into the procapsid at rates of up to ∼1,800 bp per second, generates forces of up to 100 piconewtons, and translocates the DNA in steps of 10 bp that in turn consist of four rapid 2.5-bp substeps.

  • TerL and probably TerS are physical components of the packaging motor that are released from the nascent virion upon completion of packaging, so they are not present in completed virions.

  • After DNA packaging and TerL release, other proteins stabilize the packaged DNA by plugging the channel through which the DNA entered the procapsid and by binding the outside of the capsid shell to strengthen it.

  • Recently obtained atomic structures of packaging motor proteins, channel plug proteins and shell-strengthening proteins, as well as subnanometer-resolution, cryo-electron microscopy-derived three-dimensional reconstructions of virions and procapsids, have shed new light on the mechanism of the motor and its control.

Abstract

Tailed bacteriophages use nanomotors, or molecular machines that convert chemical energy into physical movement of molecules, to insert their double-stranded DNA genomes into virus particles. These viral nanomotors are powered by ATP hydrolysis and pump the DNA into a preformed protein container called a procapsid. As a result, the virions contain very highly compacted chromosomes. Here, I review recent progress in obtaining structural information for virions, procapsids and the individual motor protein components, and discuss single-molecule in vitro packaging reactions, which have yielded important new information about the mechanism by which these powerful molecular machines translocate DNA.

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Figure 1: Tailed bacteriophages and their DNA-packaging motor.
Figure 2: Arrangement of DNA and the portal protein in bacteriophage P22 virions.
Figure 3: Structures of the three DNA-packaging motor proteins.
Figure 4: The procapsid of phage P22.
Figure 5: DNA-packaging motor of phage T4.

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Acknowledgements

I thank M. Feiss, V. Rao and S. Grimes for thoughtful reading of this manuscript before publication. My research is supported by the US National Institutes of Health grant RO1 AI074825.

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  1. Division of Microbiology and Immunology, Pathology Department, University of Utah School of Medicine, 15 North Medical Drive East, Salt Lake City, Utah 84112, USA. e-mail: sherwood.casjens@path.utah.edu,

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Glossary

Tailed bacteriophages

Double-stranded-DNA bacteriophages with a protein tail that attaches to a susceptible bacterium. DNA is injected into the host through the tail.

Prophages

Bacteriophage genomes that are physically integrated into the chromosome of the host bacterium.

Nanomotor

A molecular motor that functions on a nanometre scale to convert energy into directed physical movement of molecules.

Procapsid

The preformed protein container into which DNA is packaged during virion assembly.

Portal protein

The part of the DNA-packaging nanomotor that forms the hole or portal through the phage capsid; DNA enters and exits the virion through this portal.

Portal vertex

The unique vertex to which the portal protein and tails are attached. Icosahedral structures such as phage heads have 12 five-fold rotationally symmetrical vertices.

Low-angle X-ray scattering

A technique that is used to determine the radially averaged electron density of particles that make up an unoriented (as opposed to crystalline) sample. It is based on the deflection of a beam of X-rays away from its straight trajectory after it interacts with the particles in the sample.

Terminase

The DNA nanomotor protein complex that recognizes the DNA which will be packaged. The terminase contains the ATPase activity that converts chemical energy into mechanical movement, and also contains the active site for cleavage of double-stranded DNA (when such a site is present).

Concatemers

Long DNA molecules that contain multiple head-to-tail repeats of the phage genome sequence. Concatemers are often formed as the result of the DNA synthesis machinery replicating around a circular template multiple times without terminating.

Occam's razor

A line of reasoning that argues that the simplest explanation should be favoured until a more complex one is required by the observed data (attributed to the Franciscan friar Father William of Ockham).

Late-gene transcription factors

The phage-encoded early proteins (which are expressed early during infection) that cause transcription of the genes which are expressed at late times after infection.

IHF

(Integration host factor). An Escherichia coli protein that binds DNA and bends it at a sharp angle. IHF was first discovered as a cofactor of the phage λ enzyme integrase.

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Casjens, S. The DNA-packaging nanomotor of tailed bacteriophages. Nat Rev Microbiol 9, 647–657 (2011). https://doi.org/10.1038/nrmicro2632

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