Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Opinion
  • Published:

Virus evolution: how far does the double β-barrel viral lineage extend?

Nature Reviews Microbiology volume 6, pages 941–948 (2008)Cite this article

Abstract

During the past few years one of the most astonishing findings in the field of virology has been the realization that viruses that infect hosts from all three domains of life are often structurally similar. The recent burst of structural information points to a need to create a new way to organize the virosphere that, in addition to the current classification, would reflect relationships between virus families. Using the vertical β-barrel major capsid proteins and ATPases related to known viral genome-packaging ATPases as examples, we can now re-evaluate the classification of viruses and virus-like genetic elements from a structural standpoint.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Structural features common to members of the PRD1–adenovirus lineage.
Figure 2: Genome organization of selected members of the PRD1–adenovirus lineage from all domains of life.
Figure 3: Possible origin and evolution of viruses that belong to the vertical β-barrel superlineage.

Similar content being viewed by others

References

  1. Bergh, O., Børsheim, K. Y., Bratbak, G. & Heldal, M. High abundance of viruses found in aquatic environments. Nature 340, 467–468 (1989).

    CAS  PubMed  Google Scholar 

  2. Jalasvuori, M. & Bamford, J. K. Structural co-evolution of viruses and cells in the primordial world. Orig. Life Evol. Biosph. 38, 165–181 (2008).

    Article  PubMed  Google Scholar 

  3. Filée, J. & Forterre, P. Viral proteins functioning in organelles: a cryptic origin? Trends Microbiol. 13, 510–513 (2005).

    Article  PubMed  Google Scholar 

  4. Forterre, P. The two ages of the RNA world, and the transition to the DNA world: a story of viruses and cells. Biochimie 87, 793–803 (2005).

    Article  CAS  PubMed  Google Scholar 

  5. Koonin, E. V., Senkevich, T. G. & Dolja, V. V. The ancient virus world and evolution of cells. Biol. Direct 1, 29 (2006).

    Article  PubMed  PubMed Central  Google Scholar 

  6. Fauquet, C. M., Mayo, M. A., Maniloff, J., Desselberger, U. & Ball, L. A. (eds) VIIIth Report of the International Committee on Taxonomy of Viruses (Elsevier–Academic, London, 2005).

    Google Scholar 

  7. Bamford, D. H., Grimes, J. M. & Stuart, D. I. What does structure tell us about virus evolution? Curr. Opin. Struct. Biol. 15, 655–663 (2005).

    Article  CAS  PubMed  Google Scholar 

  8. Harrison, S. C., Olson, A. J., Schutt, C. E., Winkler, F. K. & Bricogne, G. Tomato bushy stunt virus at 2.9 Å resolution. Nature 276, 368–373 (1978).

    Article  CAS  PubMed  Google Scholar 

  9. Rossmann, M. G. et al. Structure of a human common cold virus and functional relationship to other picornaviruses. Nature 317, 145–153 (1985).

    Article  CAS  PubMed  Google Scholar 

  10. Rossmann, M. G. & Johnson, J. E. Icosahedral RNA virus structure. Annu. Rev. Biochem. 58, 533–573 (1989).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  12. Abrescia, N. G. et al. Insights into assembly from structural analysis of bacteriophage PRD1. Nature 432, 68–74 (2004).

    Article  CAS  PubMed  Google Scholar 

  13. Zubieta, C., Schoehn, G., Chroboczek, J. & Cusack, S. The structure of the human adenovirus 2 penton. Mol. Cell 17, 121–135 (2005).

    Article  CAS  PubMed  Google Scholar 

  14. Baker, M. L., Jiang, W., Rixon, F. J. & Chiu, W. Common ancestry of herpesviruses and tailed DNA bacteriophages. J. Virol. 79, 14967–14970 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Fokine, A. et al. Structural and functional similarities between the capsid proteins of bacteriophages T4 and HK97 point to a common ancestry. Proc. Natl Acad. Sci. USA 102, 7163–7168 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Wikoff, W. R. et al. Topologically linked protein rings in the bacteriophage HK97 capsid. Science 289, 2129–2133 (2000).

    Article  CAS  PubMed  Google Scholar 

  17. Zhou, Z. H. et al. Seeing the herpesvirus capsid at 8.5 Å. Science 288, 877–880 (2000).

    Article  CAS  PubMed  Google Scholar 

  18. Grimes, J. M. et al. The atomic structure of the bluetongue virus core. Nature 395, 470–478 (1998).

    Article  CAS  PubMed  Google Scholar 

  19. Huiskonen, J. T. et al. Structure of the bacteriophage φ6 nucleocapsid suggests a mechanism for sequential RNA packaging. Structure 14, 1039–1048 (2006).

    Article  CAS  PubMed  Google Scholar 

  20. Mertens, P. The dsRNA viruses. Virus Res. 101, 3–13 (2004).

    Article  CAS  PubMed  Google Scholar 

  21. Bamford, D. H. Do viruses form lineages across different domains of life? Res. Microbiol. 154, 231–236 (2003).

    Article  CAS  PubMed  Google Scholar 

  22. Bamford, D. H., Burnett, R. M. & Stuart, D. I. Evolution of viral structure. Theor. Popul. Biol. 61, 461–470 (2002).

    Article  PubMed  Google Scholar 

  23. Benson, S. D., Bamford, J. K., Bamford, D. H. & Burnett, R. M. Does common architecture reveal a viral lineage spanning all three domains of life? Mol. Cell 16, 673–685 (2004).

    Article  CAS  PubMed  Google Scholar 

  24. Hendrix, R. W., Smith, M. C., Burns, R. N., Ford, M. E. & Hatfull, G. F. Evolutionary relationships among diverse bacteriophages and prophages: all the world's a phage. Proc. Natl Acad. Sci. USA 96, 2192–2197 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Grahn, M. A., Butcher, S. J., Bamford, J. K. & Bamford, D. H. in The Bacteriophages (ed. Calendar, R.) 161–170 (Oxford Univ. Press, 2006).

    Google Scholar 

  26. Cockburn, J. J. et al. Membrane structure and interactions with protein and DNA in bacteriophage PRD1. Nature 432, 122–125 (2004).

    Article  CAS  PubMed  Google Scholar 

  27. Saren, A. M. et al. A snapshot of viral evolution from genome analysis of the Tectiviridae family. J. Mol. Biol. 350, 427–440 (2005).

    Article  CAS  PubMed  Google Scholar 

  28. Ravantti, J. J., Gaidelytė, A., Bamford, D. H. & Bamford, J. K. Comparative analysis of bacterial viruses Bam35, infecting a gram-positive host, and PRD1, infecting gram-negative hosts, demonstrates a viral lineage. Virology 313, 401–414 (2003).

    Article  CAS  PubMed  Google Scholar 

  29. Laurinmäki, P. A., Huiskonen, J. T., Bamford, D. H. & Butcher, S. J. Membrane proteins modulate the bilayer curvature in the bacterial virus Bam35. Structure 13, 1819–1828 (2005).

    Article  PubMed  Google Scholar 

  30. Espejo, R. T. & Canelo, E. S. Properties of bacteriophage PM2: a lipid-containing bacterial virus. Virology 34, 738–747 (1968).

    Article  CAS  PubMed  Google Scholar 

  31. Abrescia, N. G. et al. The structure of PM2, a marine bacteriophage with a supercoiled genome and lipid membrane. Mol. Cell 31, 749–761 (2008).

    Article  CAS  PubMed  Google Scholar 

  32. Huiskonen, J. T., Kivelä, H. M., Bamford, D. H. & Butcher, S. J. The PM2 virion has a novel organization with an internal membrane and pentameric receptor binding spikes. Nature Struct. Mol. Biol. 11, 850–856 (2004).

    Article  CAS  Google Scholar 

  33. Rice, G. et al. The structure of a thermophilic archaeal virus shows a double-stranded DNA viral capsid type that spans all domains of life. Proc. Natl Acad. Sci. USA 101, 7716–7720 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Khayat, R. et al. Structure of an archaeal virus capsid protein reveals a common ancestry to eukaryotic and bacterial viruses. Proc. Natl Acad. Sci. USA 102, 18944–18949 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Krupovič, M. & Bamford, D. H. Archaeal proviruses TKV4 and MVV extend the PRD1–adenovirus lineage to the phylum Euryarchaeota. Virology 375, 292–300 (2008).

    Article  PubMed  Google Scholar 

  36. Stewart, P. L., Burnett, R. M., Cyrklaff, M. & Fuller, S. D. Image reconstruction reveals the complex molecular organization of adenovirus. Cell 67, 145–154 (1991).

    Article  CAS  PubMed  Google Scholar 

  37. San Martín, C. & Burnett, R. M. Structural studies on adenoviruses. Curr. Top. Microbiol. Immunol. 272, 57–94 (2003).

    PubMed  Google Scholar 

  38. Nandhagopal, N. et al. The structure and evolution of the major capsid protein of a large, lipid-containing DNA virus. Proc. Natl Acad. Sci. USA 99, 14758–14763 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Yan, X. et al. Structure and assembly of large lipid-containing dsDNA viruses. Nature Struct. Biol. 7, 101–103 (2000).

    Article  CAS  PubMed  Google Scholar 

  40. Dunigan, D. D., Fitzgerald, L. A. & Van Etten, J. L. Phycodnaviruses: a peek at genetic diversity. Virus Res. 117, 119–132 (2006).

    Article  CAS  PubMed  Google Scholar 

  41. Meints, R. H., Ivey, R. G., Lee, A. M. & Choi, T. J. Identification of two virus integration sites in the brown alga Feldmannia chromosome. J. Virol. 82, 1407–1413 (2008).

    Article  CAS  PubMed  Google Scholar 

  42. Iyer, L. M., Aravind, L. & Koonin, E. V. Common origin of four diverse families of large eukaryotic DNA viruses. J. Virol. 75, 11720–11734 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Iyer, L. M., Balaji, S., Koonin, E. V. & Aravind, L. Evolutionary genomics of nucleo-cytoplasmic large DNA viruses. Virus Res. 117, 156–184 (2006).

    Article  CAS  PubMed  Google Scholar 

  44. Rouiller, I., Brookes, S. M., Hyatt, A. D., Windsor, M. & Wileman, T. African swine fever virus is wrapped by the endoplasmic reticulum. J. Virol. 72, 2373–2387 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  45. Xiao, C. et al. Cryo-electron microscopy of the giant Mimivirus. J. Mol. Biol. 353, 493–496 (2005).

    Article  CAS  PubMed  Google Scholar 

  46. Moss, B. in Fields Virology (eds Knipe, D. M. & Howley, P. M.) 2905–2946 (Lippincott Williams and Wilkins, Philadelphia, 2005).

    Google Scholar 

  47. Risco, C. et al. Endoplasmic reticulum–Golgi intermediate compartment membranes and vimentin filaments participate in vaccinia virus assembly. J. Virol. 76, 1839–1855 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Sodeik, B., Griffiths, G., Ericsson, M., Moss, B. & Doms, R. W. Assembly of vaccinia virus: effects of rifampin on the intracellular distribution of viral protein p65. J. Virol. 68, 1103–1114 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  49. Szajner, P., Weisberg, A. S., Lebowitz, J., Heuser, J. & Moss, B. External scaffold of spherical immature poxvirus particles is made of protein trimers, forming a honeycomb lattice. J. Cell Biol. 170, 971–981 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Hyun, J. K. et al. The structure of a putative scaffolding protein of immature poxvirus particles as determined by electron microscopy suggests similarity with capsid proteins of large icosahedral DNA viruses. J. Virol. 81, 11075–11083 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Federici, B. A. et al. in VIIIth Report of the International Committee on Taxonomy of Viruses (eds Fauquet, C. M., Mayo, M. A., Maniloff, J., Desselberger, U. & Ball, L. A.) 269–274 (Elsevier–Academic, London, 2005).

    Google Scholar 

  52. Stasiak, K., Demattei, M. V., Federici, B. A. & Bigot, Y. Phylogenetic position of the Diadromus pulchellus ascovirus DNA polymerase among viruses with large double-stranded DNA genomes. J. Gen. Virol. 81, 3059–3072 (2000).

    Article  CAS  PubMed  Google Scholar 

  53. Stasiak, K., Renault, S., Demattei, M. V., Bigot, Y. & Federici, B. A. Evidence for the evolution of ascoviruses from iridoviruses. J. Gen. Virol. 84, 2999–3009 (2003).

    Article  CAS  PubMed  Google Scholar 

  54. Feschotte, C. & Pritham, E. J. Non-mammalian c-integrases are encoded by giant transposable elements. Trends Genet. 21, 551–552 (2005).

    Article  CAS  PubMed  Google Scholar 

  55. Kapitonov, V. V. & Jurka, J. Self-synthesizing DNA transposons in eukaryotes. Proc. Natl Acad. Sci. USA 103, 4540–4545 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Pritham, E. J., Putliwala, T. & Feschotte, C. Mavericks, a novel class of giant transposable elements widespread in eukaryotes and related to DNA viruses. Gene 390, 3–17 (2007).

    Article  CAS  PubMed  Google Scholar 

  57. Strömsten, N. J., Bamford, D. H. & Bamford, J. K. In vitro DNA packaging of PRD1: a common mechanism for internal-membrane viruses. J. Mol. Biol. 348, 617–629 (2005).

    Article  PubMed  Google Scholar 

  58. Iyer, L. M., Makarova, K. S., Koonin, E. V. & Aravind, L. Comparative genomics of the FtsK–HerA superfamily of pumping ATPases: implications for the origins of chromosome segregation, cell division and viral capsid packaging. Nucleic Acids Res. 32, 5260–5279 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Burroughs, A. M., Iyer, L. M. & Aravind, L. Comparative genomics and evolutionary trajectories of viral ATP dependent DNA-packaging systems. Genome Dyn. 3, 48–65 (2007).

    Article  CAS  PubMed  Google Scholar 

  60. Ginalski, K., Elofsson, A., Fischer, D. & Rychlewski, L. 3D-Jury: a simple approach to improve protein structure predictions. Bioinformatics 19, 1015–1018 (2003).

    Article  CAS  PubMed  Google Scholar 

  61. Krupovič, M. & Bamford, D. H. Putative prophages related to lytic tailless marine dsDNA phage PM2 are widespread in the genomes of aquatic bacteria. BMC Genomics 8, 236 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  62. Chappell, J. D., Prota, A. E., Dermody, T. S. & Stehle, T. Crystal structure of reovirus attachment protein σ1 reveals evolutionary relationship to adenovirus fiber. EMBO J. 21, 1–11 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Graham, S. C. et al. Structure of CrmE, a virus-encoded tumour necrosis factor receptor. J. Mol. Biol. 372, 660–671 (2007).

    Article  CAS  PubMed  Google Scholar 

  64. Krupovič, M., Cvirkait˙e-Krupoviˇc, V. & Bamford, D. H. Identification and functional analysis of the Rz/Rz1-like accessory lysis genes in the membrane-containing bacteriophage PRD1. Mol. Microbiol. 68, 492–503 (2008).

    Article  PubMed  Google Scholar 

  65. Hendrix, R. W., Lawrence, J. G., Hatfull, G. F. & Casjens, S. The origins and ongoing evolution of viruses. Trends Microbiol. 8, 504–508 (2000).

    Article  CAS  PubMed  Google Scholar 

  66. Raoult, D. & Forterre, P. Redefining viruses: lessons from Mimivirus. Nature Rev. Microbiol. 6, 315–319 (2008).

    Article  CAS  Google Scholar 

  67. Porter, K. et al. SH1: a novel, spherical halovirus isolated from an Australian hypersaline lake. Virology 335, 22–33 (2005).

    Article  CAS  PubMed  Google Scholar 

  68. Jaatinen, S. T., Happonen, L. J., Laurinmäki, P., Butcher, S. J. & Bamford, D. H. Biochemical and structural characterisation of membrane-containing icosahedral dsDNA bacteriophages infecting thermophilic Thermus thermophilus. Virology 379, 10–19 (2008).

    Article  CAS  PubMed  Google Scholar 

  69. Jäälinoja, H. T. et al. Structure and host-cell interaction of SH1, a membrane-containing, halophilic euryarchaeal virus. Proc. Natl Acad. Sci. USA 105, 8008–8013 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  70. Männistö, R. H., Kivelä, H. M., Paulin, L., Bamford, D. H. & Bamford, J. K. The complete genome sequence of PM2, the first lipid-containing bacterial virus to be isolated. Virology 262, 355–363 (1999).

    Article  PubMed  Google Scholar 

  71. Bamford, D. H. et al. Constituents of SH1, a novel lipid-containing virus infecting the halophilic euryarchaeon Haloarcula hispanica. J. Virol. 79, 9097–9107 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Epifano, C., Krijnse-Locker, J., Salas, M. L., Salas, J. & Rodríguez, J. M. Generation of filamentous instead of icosahedral particles by repression of African swine fever virus structural protein pB438L. J. Virol. 80, 11456–11466 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Rydman, P. S., Bamford, J. K. & Bamford, D. H. A minor capsid protein P30 is essential for bacteriophage PRD1 capsid assembly. J. Mol. Biol. 313, 785–795 (2001).

    Article  CAS  PubMed  Google Scholar 

  74. Raoult, D. et al. The 1.2-megabase genome sequence of Mimivirus. Science 306, 1344–1350 (2004).

    Article  CAS  PubMed  Google Scholar 

  75. Moreira, D. & Brochier-Armanet, C. Giant viruses, giant chimeras: the multiple evolutionary histories of Mimivirus genes. BMC Evol. Biol. 8, 12 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  76. Suhre, K. Gene and genome duplication in Acanthamoeba polyphaga Mimivirus. J. Virol. 79, 14095–14101 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Filée, J. & Chandler, M. Convergent mechanisms of genome evolution of large and giant DNA viruses. Res. Microbiol. 159, 325–331 (2008).

    Article  PubMed  Google Scholar 

  78. São-José, C., de Frutos, M., Raspaud, E., Santos, M. A. & Tavares, P. Pressure built by DNA packing inside virions: enough to drive DNA ejection in vitro, largely insufficient for delivery into the bacterial cytoplasm. J. Mol. Biol. 374, 346–355 (2007).

    Article  PubMed  Google Scholar 

  79. Jurka, J. et al. Repbase Update, a database of eukaryotic repetitive elements. Cytogenet. Genome Res. 110, 462–467 (2005).

    Article  CAS  PubMed  Google Scholar 

  80. Yan, X., Chipman, P. R., Castberg, T., Bratbak, G. & Baker, T. S. The marine algal virus PpV01 has an icosahedral capsid with T=219 quasisymmetry. J. Virol. 79, 9236–9243 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank J. Ravantti for his invaluable comments, and M. Jalasvuori and J.K. Bamford for sharing their unpublished data. This work was supported by the Finnish Center of Excellence Program (2006-2011) of the Academy of Finland (grants 1213467 and 1213992 to D.H.B. and grant 1210253). M.K. is supported by the Viikki Graduate School in Biosciences.

Author information

Authors and Affiliations

  1. Mart Krupovič and Dennis H. Bamford are at the Department of Biological and Environmental Sciences and Institute of Biotechnology, Biocenter 2, PO BOX 56 (Viikinkaari 5), 00014 University of Helsinki, Finland.,

    Mart Krupovič & Dennis H. Bamford

Authors
  1. Mart Krupovič
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dennis H. Bamford
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dennis H. Bamford.

Related links

Related links

DATABASES

Entrez Genome

Bam35

Orf virus

PBCV-1

PM2

PRD1

STIV

Protein Data Bank

adenovirus MCP

PBCV-1 MCP

PM2 MCP

STIV MCP

FURTHER INFORMATION

Dennis H. Bamford's homepage

BioinfoBank Meta Server

Repbase Update

Glossary

Biosphere

The global ecological system that integrates all living organisms.

Capsomer

The basic structural unit of the capsid of a virus.

Convergent evolution

The process by which organisms that are not monophyletic independently evolve similar traits as a result of adaptation to ecological niches or similar environments.

Divergent evolution

The accumulation of differences between groups that can lead to the formation of new species, usually as a result of the adaptation of different groups of the same species to different environments.

Transposon

A genetic element that can move from one locus of a chromosome to another through a recombinase-mediated reaction.

Triangulation number

(T). Used to describe the number of subunits that exist in a capsid: an icosahedral capsid of triangulation number T will possess 60 T subunits.

Virosphere

The total sum of all viruses.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Krupovič, M., Bamford, D. Virus evolution: how far does the double β-barrel viral lineage extend?. Nat Rev Microbiol 6, 941–948 (2008). https://doi.org/10.1038/nrmicro2033

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrmicro2033

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing