Protein Conservation in Virus Evolution

Mart Krupovic, Institut Pasteur, Paris, France
Dennis H Bamford, University of Helsinki, Helsinki, Finland

Published online: May 2011

DOI: 10.1002/9780470015902.a0023265

Evolution of viruses is considerably more rapid than that of the cellular organisms that they infect. The reach of sequence-based evolutionary studies on viruses is therefore rather limited. The tertiary protein structure is generally conserved over longer time periods than the primary one. Indeed, structural studies proved to be more informative for reconstructing deep evolutionary connections between distantly related viruses. It has become apparent that certain viruses infecting hosts from different domains of life are remarkably similar in their virion assembly and architecture, suggesting a common ancestry for these structurally related viruses. Furthermore, the presence of several distinct architectural principles employed by viruses suggested that the origin of the current virosphere has multiple evolutionary origins. Insights obtained from numerous structural studies may not only be successfully used to refine the existing virus classification scheme, but may also lead to a major shift in our understanding on the origin, evolution and organisation of the viral domain.

Key Concepts:

  • Tertiary protein structure is conserved over longer periods of time than the primary one and thus allows recognising deep evolutionary connections between viruses that have diverged in a distant past.
  • The ability to build virions (i.e., presence of capsid proteins) is a hallmark feature of viruses that distinguishes them from other mobile genetic elements, such as plasmids and transposons.
  • Structural studies suggest that certain viruses infecting bacteria, archaea and eukaryotes are evolutionarily related.
  • Viral lineage hypothesis predicts a common origin for structurally related viruses, infecting hosts from different domains of life.
  • There are several different viral lineages of structurally distinct viruses, suggesting that the contemporary virosphere has multiple evolutionary origins.
  • The molecular virion complexity shared by viruses in different domains of life suggests that at the time of the last universal cellular ancestor (LUCA) viruses were already very sophisticated.

Keywords: virus evolution; viral lineage; viral jelly roll fold; double -barrel fold; virus taxonomy and classification; membrane-containing viruses; structural virology; bacteriophage PRD1

Figure 1. Genomic differences between a virus and a plasmid. Viruses and plasmids belong to two distinct types of mobile genetic elements. Differences between these two types are best illuminated by comparing the simplest representatives of the two types. For this purpose, genome maps of the porcine circovirus 1 (PCV1; GenBank accession number ) and the Helicobacter pylori plasmid pAL236-5 (GenBank accession number ) are compared. Red arrows represent genes for the rolling-circle replication initiation proteins (Rep) in both mobile elements, whereas the capsid protein-coding gene of PCV1 is depicted by a green arrow. Note that even though 50% of the PCV1 genes (1 out of 2) have counterparts in pAL236-5 plasmid, only the former can be considered a genuine virus, capable of forming a virion. Adapted from Krupovi and Bamford (2010) with permission from American Society for Microbiology.
Figure 2. Viral jelly roll fold. (a) Topology diagram resembling the Swiss roll, also known as jelly roll, cake (hence the name of the fold) and (b) the X-ray structure of the capsid protein VP1 of human rhinovirus type 14 (PDB id: 4RHV) are shown. For the sake of clarity, only the eight-stranded -barrel is shown, whereas the N- and C-terminal regions of VP1 are trimmed.
Figure 3. Double jelly roll fold. (a) Virion architecture of PRD1 and adenovirus (triangulation number of 25). Apices of the red triangle combine the fivefold vertices (light shading) outlining the triangular virus facet. Grey hexagons depict the morphology of the double -barrel trimers. The insert shows the X-ray model of the major capsid protein trimer of PRD1 (top view). Individual monomers in the trimer are shown in different colours. Adapted from Krupovi and Bamford (2008). (b) Double jelly roll major capsid proteins of viruses infecting hosts from the three different domains of life. Left: P3 of bacterial tectivirus PRD1 (PDB id: 1HX6), centre: B345 of archaeal Sulfolobus turreted icosahedral virus (STIV; PDB id: 2BBD), right: Vp54 of eukaryotic Paramecium bursaria Chlorella virus type 1 (PBCV-1; PDB id: 1J5Q).
Figure 4. HK97-like major capsid protein fold. High-resolution structures of the major capsid proteins of tailed dsDNA bacteriophages from the three different families, Siphoviridae (HK97, X-ray, PDN id: 1OHG), Myoviridae (T4, X-ray, PDB id: 1YUE) and Podoviridae (15, cryo-EM, PDB id: 3C5B), are shown.
Figure 5. Antiquity and polyphyletic origin of viruses. Evolution of cellular organisms is represented with the blue tree-like diagram, whereas viral lineages that followed the diversification of their hosts are indicated with different colours (green, red and yellow) to highlight their polyphyletic origin. The origins of viral lineages extend deep into the prehistory of cellular life. Although only three viral lineages are shown, it should be noted that the precise number is unknown and may be much greater. Reproduced from Bamford (2003), with permission from Elsevier.
close
 References
    Abrescia NG, Cockburn JJ, Grimes JM et al. (2004) Insights into assembly from structural analysis of bacteriophage PRD1. Nature 432: 68–74.
    book Abrescia NG, Grimes JM, Fry EE et al. (2010) "What does it take to make a virus: the concept of the viral “self”". In: Stockley PG and Twarock R (eds) Emerging Topics in Physical Virology, pp. 35–58. London, UK: Imperial College Press.
    Abrescia NG, Grimes JM, Kivelä HM et al. (2008) Insights into virus evolution and membrane biogenesis from the structure of the marine lipid-containing bacteriophage PM2. Molecular Cell 31: 749–761.
    Ackermann HW (2007) 5500 Phages examined in the electron microscope. Archives in Virology 152: 227–243.
    Baker ML, Jiang W, Rixon FJ and Chiu W (2005) Common ancestry of herpesviruses and tailed DNA bacteriophages. Journal of Virology 79: 14967–14970.
    Bamford DH (2003) Do viruses form lineages across different domains of life? Research in Microbiology 154: 231–236.
    Bamford DH, Burnett RM and Stuart DI (2002) Evolution of viral structure. Theoretical Population Biology 61: 461–470.
    Bamford DH, Grimes JM and Stuart DI (2005) What does structure tell us about virus evolution? Current Opinion in Structural Biology 15: 655–663.
    Benson SD, Bamford JK, Bamford DH and Burnett RM (1999) Viral evolution revealed by bacteriophage PRD1 and human adenovirus coat protein structures. Cell 98: 825–833.
    Benson SD, Bamford JK, Bamford DH and Burnett RM (2004) Does common architecture reveal a viral lineage spanning all three domains of life? Molecular Cell 16: 673–685.
    Chapman MS and Liljas L (2003) Structural folds of viral proteins. Advances in Protein Chemistry 64: 125–196.
    book Fauquet CM, Mayo MA, Maniloff J, Desselberger U and Ball LA (2005) VIIIth Report of the International Committee on Taxonomy of Viruses. San Diego: Elsevier–Academic Press.
    Filée J and Chandler M (2008) Convergent mechanisms of genome evolution of large and giant DNA viruses. Research in Microbiology 159: 325–331.
    Fischer MG, Allen MJ, Wilson WH and Suttle CA (2010) Giant virus with a remarkable complement of genes infects marine zooplankton. Proceedings of the National Academy of Sciences of the USA 107: 19508–19513.
    Harrison SC, Olson AJ, Schutt CE, Winkler FK and Bricogne G (1978) Tomato bushy stunt virus at 2.9 Å resolution. Nature 276: 368–373.
    Hendrix RW (2009) Jumbo bacteriophages. Current Topics in Microbiology and Immunology 328: 229–240.
    Huiskonen JT and Butcher SJ (2007) Membrane-containing viruses with icosahedrally symmetric capsids. Current Opinion in Structural Biology 17: 229–236.
    Khayat R, Tang L, Larson ET et al. (2005) Structure of an archaeal virus capsid protein reveals a common ancestry to eukaryotic and bacterial viruses. Proceedings of the National Academy of Sciences of the USA 102: 18944–18949.
    Koonin EV, Wolf YI, Nagasaki K and Dolja VV (2008) The Big Bang of picorna-like virus evolution antedates the radiation of eukaryotic supergroups. Nature Reviews Microbiology 6: 925–939.
    Koonin EV and Yutin N (2010) Origin and evolution of eukaryotic large nucleo-cytoplasmic DNA viruses. Intervirology 53: 284–292.
    Krupovi M and Bamford DH (2008) Virus evolution: how far does the double beta-barrel viral lineage extend? Nature Reviews Microbiology 6: 941–948.
    Krupovi M and Bamford DH (2010) Order to the viral universe. Journal of Virology 84: 12476–12479.
    Krupovi M, Forterre P and Bamford DH (2010) Comparative analysis of the mosaic genomes of tailed archaeal viruses and proviruses suggests common themes for virion architecture and assembly with tailed viruses of bacteria. Journal of Molecular Biology 397: 144–160.
    Krupovi M, Ravantti JJ and Bamford DH (2009) Geminiviruses: a tale of a plasmid becoming a virus. BMC Evolutionary Biology 9: 112.
    Merckel MC, Huiskonen JT, Bamford DH, Goldman A and Tuma R (2005) The structure of the bacteriophage PRD1 spike sheds light on the evolution of viral capsid architecture. Molecular Cell 18: 161–170.
    Mertens P (2004) The dsRNA viruses. Virusus Research 101: 3–13.
    Nandhagopal N, Simpson AA, Gurnon JR et al. (2002) The structure and evolution of the major capsid protein of a large, lipid-containing DNA virus. Proceedings of the National Academy of Sciences of the USA 99: 14758–14763.
    Pietilä MK, Roine E, Paulin L, Kalkkinen N and Bamford DH (2009) An ssDNA virus infecting archaea: a new lineage of viruses with a membrane envelope. Molecular Microbiology 72: 307–319.
    Prangishvili D, Forterre P and Garrett RA (2006) Viruses of the Archaea: a unifying view. Nature Reviews Microbiology 4: 837–848.
    Rao VB and Feiss M (2008) The bacteriophage DNA packaging motor. Annual Review of Genetics 42: 647–681.
    Rohwer F and Thurber RV (2009) Viruses manipulate the marine environment. Nature 459: 207–212.
    Roine E, Kukkaro P, Paulin L et al. (2010) New, closely related haloarchaeal viral elements with different nucleic acid types. Journal of Virology 84: 3682–3689.
    Rossmann MG, Arnold E, Erickson JW et al. (1985) Structure of a human common cold virus and functional relationship to other picornaviruses. Nature 317: 145–153.
    Rossmann MG and Johnson JE (1989) Icosahedral RNA virus structure. Annual Review of Biochemistry 58: 533–573.
    Saren AM, Ravantti JJ, Benson SD et al. (2005) A snapshot of viral evolution from genome analysis of the Tectiviridae family. Journal of Molecular Biology 350: 427–440.
    Steven AC, Conway JF, Cheng N et al. (2005) Structure, assembly, and antigenicity of hepatitis B virus capsid proteins. Advances in Virus Research 64: 125–164.
    Strömsten NJ, Bamford DH and Bamford JK (2005) In vitro DNA packaging of PRD1: a common mechanism for internal-membrane viruses. Journal of Molecular Biology 348: 617–629.
    Suttle CA (2007) Marine viruses – major players in the global ecosystem. Nature Reviews Microbiology 5: 801–812.
    Tate J, Liljas L, Scotti P et al. (1999) The crystal structure of cricket paralysis virus: the first view of a new virus family. Nature Structural Biology 6: 765–774.
    Wikoff WR, Liljas L, Duda RL et al. (2000) Topologically linked protein rings in the bacteriophage HK97 capsid. Science 289: 2129–2133.
    Xiao C, Kuznetsov YG, Sun S et al. (2009) Structural studies of the giant mimivirus. PLoS Biology 7: e92.
    book Zhou ZH and Lo P (2008) "Structure and assembly of human herpesviruses: new insights from cryo-electron microscopy and tomography". In: Cheng RH and Miyamura T (eds) Structure-based Study of Viral Replication, pp. 483–516. Singapore: World Scientific Publishing.
    Zubieta C, Schoehn G, Chroboczek J and Cusack S (2005) The structure of the human adenovirus 2 penton. Molecular Cell 17: 121–135.
 Further Reading
    Bennett A, McKenna R and Agbandje-McKenna M (2008) A comparative analysis of the structural architecture of ssDNA viruses. Computational and Mathematical Methods in Medicine 9: 183–196.
    Cockburn JJ, Abrescia NG, Grimes JM et al. (2004) Membrane structure and interactions with protein and DNA in bacteriophage PRD1. Nature 432: 122–125.
    Duffy S, Shackelton LA and Holmes EC (2008) Rates of evolutionary change in viruses: patterns and determinants. Nature Reviews Genetics 9: 267–276.
    Forterre P and Prangishvili D (2009) The origin of viruses. Research in Microbiology 160: 466–472.
    Krupovi M and Bamford DH (2009) Does the evolution of viral polymerases reflect the origin and evolution of viruses? Nature Reviews Microbiology 7: 250.
    Poranen MM, Tuma R and Bamford DH (2005) Assembly of double-stranded RNA bacteriophages. Advances in Virus Research 64: 15–43.
    Raoult D and Forterre P (2008) Redefining viruses: lessons from Mimivirus. Nature Reviews Microbiology 6: 315–319.
    Van Etten JL, Lane LC and Dunigan DD (2010) DNA viruses: the really big ones (giruses). Annual Review of Microbiology 64: 83–99.
    Yan X, Olson NH, Van Etten JL et al. (2000) Structure and assembly of large lipid-containing dsDNA viruses. Nature Structural Biology 7: 101–103.

Related Sub-Topics:

Virus Structure | Virus Taxonomy | Virus Structure and Function | Adaptive Evolution | Reconstruction of Phylogeny | Protein Evolution
Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

Article Title: Protein Conservation in Virus Evolution
 
How to Cite close
Krupovic, Mart, and Bamford, Dennis H(May 2011) Protein Conservation in Virus Evolution. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0023265]