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Structure and assembly of large lipid-containing dsDNA viruses

Nature Structural Biology volume 7, pages 101–103 (2000)Cite this article

Two large, lipid-containing, double-stranded DNA (dsDNA) icosahedral viruses, each ∼1 GDa (1×109 daltons) and unlikely to be amenable to crystallization, have been studied by cryo-electron microscopy (cryo-EM) and three-dimensional image reconstruction. The first, the 1,850 Å diameter Chilo iridescent virus (CIV: genus Iridovirus, family Iridoviridae ) infects the rice stem borer insect1. The second, the 1,900 Å diameter Paramecium bursaria chlorella virus, type 1 (PBCV-1: genus Chlorovirus, family Phycodnaviridae) infects certain unicellular, eukaryotic, chlorella-like green algae2. Despite differences in their pathogenicity and genome size, both viruses exhibit common structural features, suggesting a common evolutionary origin and therefore serve as a paradigm for other large viruses, such as African swine fever virus, frog virus-3 and many others (for example, see ref. 3). Both viruses have a layered structure consisting of a dsDNA–protein core, surrounded in turn by a lipid bilayer and one or more icosahedral capsid shells consisting of thousands of protein subunits4,5,6,7. Furthermore, the external capsid is essentially consistent with the quasi symmetry predictions of Caspar and Klug8. This is unexpected in view of the now well-documented departure from quasi symmetry in much smaller virusses such as polyoma9 or the inner core of the double-stranded RNA viruses (for example, see ref. 10).

CIV has a 209 kbp linear, circularly permuted (a linear molecule that maps as a circle) genome, whereas PBCV-1 has a 330 kbp linear, non-permuted genome with covalently closed, hairpin ends11,12. Some iridoviruses, like CIV, also contain fibers that protrude 350 Å or more from the outer surface of the capsid5,13 and this was confirmed in this study. In contrast to the iridoviruses, little is known about the chlorovirus structure. The chlorovirus capsids accommodate a wide range of genome sizes14,15 from 295 kbp16 to 380 kbp14. The PBCV-1 virion contains ∼50 proteins, with the 54 kDa surface glycoprotein, VP54, accounting for ∼40% of the total virion protein mass17. PBCV-1 and its close relatives are common in freshwater collected worldwide2,12. Like the tailed bacteriophages, PBCV-1 infects its host, Chlorella NC64A, by attaching to the cell wall, possibly through a unique vertex or a tail-like structure. The cell wall is then degraded at the point of attachment and viral DNA is released into the cell2,18. Analysis of the 330,740 bp PBCV-1 genome predicts that it contains 377 protein-encoding genes and 10 tRNA genes, including many interesting and unexpected genes12. To put the PBCV-1 genome size in perspective, the smallest free-living organism, a mycoplasma, encodes ∼470 proteins19.

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Figure 1: Comparison of CIV and PBCV-1 virions.
Figure 2: Close-up views of the trimers of CIV and PBCV-1.

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Acknowledgements

We thank J. C. Veyrunes and D. Burbank for their help in purifying CIV and PBCV-1, respectively, R. Ashmore for programming, and A. Friedman, M. Graves, L. Lane, A. Simpson, S. Walker, and W. Zhang for helpful discussions. This work was supported in part by NIH grants to T.S.B., M.G.R. and J.V.E., and NSF Grand Challenge and Shared Instrumentation grants to T.S.B. and M.G.R. A grant from the Lucille P. Markey Foundation and reinvestment funds from the office of the University Executive Vice President for Academic Affairs have benefited T.S.B. and M.G.R.

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Authors and Affiliations

  1. Department of Biological Sciences, Purdue University, West Lafayette, 47907-1392, Indiana, USA

    Xiaodong Yan, Norman H. Olson, Michael G. Rossmann & Timothy S. Baker

  2. Department of Plant Pathology, University of Nebraska, Lincoln, 68583-0722, Nebraska, USA

    James L. Van Etten

  3. Laboratory of Comparative Pathology, University of Montpellier II, Montpellier cedex 5, 34095, France

    Max Bergoin

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  1. Xiaodong Yan
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Correspondence to Timothy S. Baker.

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Yan, X., Olson, N., Van Etten, J. et al. Structure and assembly of large lipid-containing dsDNA viruses. Nat Struct Mol Biol 7, 101–103 (2000). https://doi.org/10.1038/72360

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