Protein Conservation in Virus Evolution

Abstract

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 β‐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 AY660574) and the Helicobacter pylori plasmid pAL236‐5 (GenBank accession number HM125989) 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 Krupovič and Bamford 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 β‐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 β‐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 Krupovič and Bamford . (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 (ɛ15, 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 , with permission from Elsevier.

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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]