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Three-dimensional structure of a viral genome-delivery portal vertex

Nature Structural & Molecular Biology volume 18, pages 597–603 (2011)Cite this article

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Abstract

DNA viruses such as bacteriophages and herpesviruses deliver their genome into and out of the capsid through large proteinaceous assemblies, known as portal proteins. Here, we report two snapshots of the dodecameric portal protein of bacteriophage P22. The 3.25-Å-resolution structure of the portal-protein core bound to 12 copies of gene product 4 (gp4) reveals a ~1.1-MDa assembly formed by 24 proteins. Unexpectedly, a lower-resolution structure of the full-length portal protein unveils the unique topology of the C-terminal domain, which forms a ~200-Å-long α-helical barrel. This domain inserts deeply into the virion and is highly conserved in the Podoviridae family. We propose that the barrel domain facilitates genome spooling onto the interior surface of the capsid during genome packaging and, in analogy to a rifle barrel, increases the accuracy of genome ejection into the host cell.

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Figure 1: Crystal structure of the bacteriophage P22 portal protein and the portal-protein core–gp4 complex.
Figure 2: Fitting of P22 portal protein and gp4 X-ray models into the cryo-EM reconstructions of the mature virion and isolated portal vertex structure.
Figure 3: The portal-protein fold.
Figure 4: Three-dimensional structure of the middle ring factor gp4.
Figure 5: Structural conservation of the middle ring factor gp4.
Figure 6: Architecture of the DNA-translocating channel.

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Acknowledgements

We thank V. Stojanoff and staff at the National Synchrotron Light Source beamlines X6A, X25 and X29A and the staff of the Macromolecular Diffraction Facility at the Cornell High Energy Synchrotron Source (macCHESS) for beam time and assistance in data collection. This work was supported by US National Institutes of Health grants 1R56 AI076509-01A1 (to G.C.) and RO1 AI40101 (to J.E.J.).

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Authors and Affiliations

  1. Department of Biological Sciences, Purdue University, West Lafayette, Indiana, USA

    Adam S Olia

  2. Department of Microbiology, University of Alabama at Birmingham, Birmingham, Alabama, USA

    Peter E Prevelige Jr

  3. Department of Molecular Biology, The Scripps Research Institute, La Jolla, California, USA

    John E Johnson

  4. Department of Biochemistry and Molecular Biology, Thomas Jefferson University, Philadelphia, Pennsylvania, USA

    Gino Cingolani

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  1. Adam S Olia
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Contributions

A.S.O. and G.C. crystallized the full-length portal and portal-protein core–gp4 complex, collected the X-ray data and determined the structures. P.E.P. isolated the gene encoding P22 portal protein and helped with data analysis. J.E.J. supervised the crystallization and data collection of full-length portal protein and helped with data analysis. G.C. coordinated the overall project and wrote the manuscript with A.S.O.

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Correspondence to Gino Cingolani.

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Olia, A., Prevelige, P., Johnson, J. et al. Three-dimensional structure of a viral genome-delivery portal vertex. Nat Struct Mol Biol 18, 597–603 (2011). https://doi.org/10.1038/nsmb.2023

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