Skip to main content
Log in

Statistical analysis of sizes and shapes of virus capsids and their resulting elastic properties

  • Original Paper
  • Published:
Journal of Biological Physics Aims and scope Submit manuscript

Abstract

From the analysis of sizes of approximately 130 small icosahedral viruses we find that there is a typical structural capsid protein, having a mean diameter of 5 nm and a mean thickness of 3 nm, with more than two thirds of the analyzed capsid proteins having thicknesses between 2 nm and 4 nm. To investigate whether, in addition to the fairly conserved geometry, capsid proteins show similarities in the way they interact with one another, we examined the shapes of the capsids in detail. We classified them numerically according to their similarity to sphere and icosahedron and an interpolating set of shapes in between, all of them obtained from the theory of elasticity of shells. In order to make a unique and straightforward connection between an idealized, numerically calculated shape of an elastic shell and a capsid, we devised a special shape fitting procedure, the outcome of which is the idealized elastic shape fitting the capsid best. Using such a procedure we performed statistical analysis of a series of virus shapes and we found similarities between the capsid elastic properties of even very different viruses. As we explain in the paper, there are both structural and functional reasons for the convergence of protein sizes and capsid elastic properties. Our work presents a specific quantitative scheme to estimate relatedness between different proteins based on the details of the (quaternary) shape they form (capsid). As such, it may provide an information complementary to the one obtained from the studies of other types of protein similarity, such as the overall composition of structural elements, topology of the folded protein backbone, and sequence similarity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Notes

  1. This is the basis of the Caspar-Klug classification scheme [14] that classifies different capsid icosahedra in terms of the triangulation number T, which is, roughly, a way to divide the icosahedron in similar, nearly equivalent parts that represent individual proteins.

  2. The triangulation numbers denoted with p (pseudo) do not completely conform to the Caspar-Klug principle of quasi-equivalence since the basic unit is composed of different (but morphologically similar) proteins.

  3. The positions of the amino acids are represented either by the positions of their centers-of-mass (see also [18]), or, where this data was unavailable, by the positions of their C α atoms.

  4. There are 60T proteins in a virus of a given T-number.

  5. The analysis of available space and restricted length of the genome is somewhat different in ssRNA viruses, where the ssRNA molecule is held within the capsid mostly by electrostatic interactions with the capsid proteins. In this case, the quantity of information that can be stored in the capsid scales as \(\overline{R}^2\) [4], so that the production of large proteins always requires the same percentage of the ssRNA information, irrespectively of the radius of the virus.

References

  1. Suttle, C.: Marine viruses – major players in the global ecosystem. Nat. Rev. Microbiol. 5, 801–812 (2007)

    Article  Google Scholar 

  2. Trifonov, E.N.: Definition of life: navigation through uncertainties. Biomol. J. Struct. Dyn. 29, 647–650 (2012)

    Article  Google Scholar 

  3. Roos, W.H., Bruinsma, R., Wuite, G.J.L.: Physical virology. Nat. Phys. 6, 733–743 (2010)

    Article  Google Scholar 

  4. Šiber, A., Lošdorfer Božič, A., Podgornik, R.: Energies and pressures in viruses: contribution of nonspecific electrostatic interactions. Phys. Chem. Chem. Phys. 14, 3746–3765 (2012)

    Article  Google Scholar 

  5. Zandi, R., Reguera, D., Bruinsma, R.F., Gelbart, W.M., Rudnick, J.: Origin of icosahedral symmetry in viruses. Proc. Natl. Acad. Sci. USA 101, 15556–15560 (2004)

    Article  ADS  Google Scholar 

  6. Cello, J., Paul, A., Wimmer, E.: Chemical synthesis of poliovirus cDNA: Generation of infectious virus in the absence of natural template. Science 97, 1016–1018 (2002)

    Article  ADS  Google Scholar 

  7. Koonin, E.V., Martin, W.: On the origin of genomes and cells within inorganic compartments. Trends Genet. 647–654, 021910 (2005)

    Google Scholar 

  8. Pearson, H.: Virophage suggests viruses are alive. Nature 454, 677 (2008)

    Article  ADS  Google Scholar 

  9. Suzan-Monti, M., La Scola, B., Raoult, D.: Genomic and evolutionary aspects of mimivirus. Virus Res. 117, 135–155 (2006)

    Article  Google Scholar 

  10. Claverie, J.M., Abergel, C.: Mimivirus: the emerging paradox of quasi-autonomous viruses. Trends Genet. 26, 431–437 (2010)

    Article  Google Scholar 

  11. Arslan, D., Legendre, M., Seltzer, V., Abergel, C., Claverie, J.M.: Distant mimivirus relative with a larger genome highlights the fundamental features of megaviridae. Proc. Natl. Acad. Sci. USA 108, 17486 (2011). doi:10.1073/pnas.1110889108

    Article  ADS  Google Scholar 

  12. Holmes, E.C.: The Evolution and Emergence of RNA Viruses. Oxford University Press (2009)

  13. Koonin, E.V., Mushegian, A.R., Dolja, V.V.: Computer analysis of amino acid sequences. In: Foster, G.D., Taylor, S.C., Walker, J.M. (eds.) Plant Virology Protocols, vol. 81 of Methods in Molecular Biology, pp. 319–337, Humana Press (1998)

  14. Caspar, D.L.D., Klug, A.: Physical principles in the construction of regular viruses. Cold Spring Harbor Symp. 27, 1–24 (1962)

    Article  Google Scholar 

  15. Lidmar, J., Mirny, L., Nelson, D.R.: Virus shapes and buckling transitions in spherical shells. Phys. Rev. E68, 051910 (2003)

    ADS  Google Scholar 

  16. Carrillo-Tripp, M., Shepherd, C.M., Borelli, I.A., Venkataraman, S., Lander, G., Natarajan, P., Johnson, J.E., Brooks III, C.L., Reddy, V.S.: Viperdb2: an enhanced and web api enabled relational database for structural virology. Nucleic Acids Res. 37, D436–D442 (2009)

    Article  Google Scholar 

  17. Konevtsova, O.V., Rochal, S.B., Lorman, V.L.: Chiral quasicrystalline order and dodecahedral geometry in exceptional families of viruses. Phys. Rev. Lett. 108, 038102 (2012)

    Article  ADS  Google Scholar 

  18. Lošdorfer Božič, A., Šiber, A., Podgornik, R.: How simple can a model of an empty viral capsid be? charge distributions in viral capsids. J. Biol. Phys. 38, 657–671 (2012)

    Article  Google Scholar 

  19. Šiber, A.: Buckling transition in icosahedral shells subjected to volume conservation constraint and pressure: Relations to virus maturation. Phys. Rev. E E73, 061915 (2006)

    ADS  Google Scholar 

  20. Rossmann, M.G., Erickson, J.W.: Structure and assembly of icosahedral shells. In: Casjens, S. (ed.) Virus Structure and Assembly. Jones and Bartless Publishers (1985)

  21. Ting, C.L., Wu, J., Wang, Z.G.: Thermodynamic basis for the genome to capsid charge relationship in electrostatically-driven viral encapsidation. Proc. Natl. Acad. Sci. USA 108, 16986–16991 (2011)

    Article  ADS  Google Scholar 

  22. Griep, S., Hobohm, U.: PDBselect 1992–2009 and PDBfilter-select. Nucleic Acids Res. 38, D318–D319 (2010)

    Article  Google Scholar 

  23. Aznar, M., Luque, A., Reguera, D.: Relevance of capsid structure in the buckling and maturation of spherical viruses. Phys. Biol. 9, 036003 (2012)

    Article  ADS  Google Scholar 

  24. Kivela, H.M., Kalkkinen, N., Bamford, D.H.: Bacteriophage PM2 has a protein capsid surrounding a spherical proteinaceous lipid core. Virology J. 76, 8169–8178 (2002)

    Article  Google Scholar 

  25. Benson, S.D., Bamford, J.K.H., Bamford, D.H., Burnett, R.M.: Viral evolution revealed by bacteriophage PRD1 and human adenovirus coat protein structures. Cell 98, 825–833 (1999)

    Article  Google Scholar 

  26. Mannige, R.V., Brooks III, C.L..: Periodic table of virus capsids: implications for natural selection and design. PLoS ONE 5, e9423 (2010)

    Article  ADS  Google Scholar 

  27. May, E.R., Brooks III, C.: On the morphology of viral capsids: Elastic properties and buckling transitions. Phys. J. Chem. B116, 8604–8609 (2012)

    Google Scholar 

  28. Morgan, G.J.: Historical review: viruses, crystals and geodesic domes. Trends Biochem. Sci. 28, 86–90 (2003)

    Article  Google Scholar 

  29. Catalano, C.E.: In: Catalano, C.E. (ed.) Viral Genome Packaging Machines: Genetics, Structure, and Mechanism, pp. 1–4. Landes Bioscience, Georgetown, TX (2005)

    Chapter  Google Scholar 

  30. Gelbart, W.M., Knobler, C.M.: The physics of phages. Phys. Today 61, 42–47 (2008)

    Article  ADS  Google Scholar 

Download references

Acknowledgements

We thank Alberto Vianelli for informing us about [20]. We also thank the two anonymous reviewers for their suggestions on improving the manuscript. A.L.B. acknowledges the support from the Slovene Agency for Research and Development under the young researcher grant. A.Š. acknowledges support from the Ministry of Science, Education, and Sports of Republic of Croatia (Grant No. 035-0352828-2837). R.P. acknowledges the support from the Slovene Agency for Research and Development (Grant No. P1-0055 and J1-4297).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Anže Lošdorfer Božič.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lošdorfer Božič, A., Šiber, A. & Podgornik, R. Statistical analysis of sizes and shapes of virus capsids and their resulting elastic properties. J Biol Phys 39, 215–228 (2013). https://doi.org/10.1007/s10867-013-9302-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10867-013-9302-3

Keywords

Navigation