Abstract
Viruses are a distinct type of replicators that encode structural proteins encasing virus genomes in virions. For some of the widespread virus capsid proteins and other major components of virions, likely ancestors encoded by cellular life forms are identifiable. In particular, one of the most common capsid proteins, with the single jelly-roll (SJR) fold, appears to have evolved from a particular family of cellular carbohydrate-binding proteins. However, the double jelly-roll major capsid protein (DJR-MCP), the hallmark of the enormously diverse viruses of the kingdom Bamfordvirae within the realm Varidnaviria, which includes bacterial and archaeal icosahedral viruses as well as eukaryotic giant viruses, has been perceived as a virus innovation that evolved by duplication and fusion of the SJR capsid proteins. Here we employ protein structure comparison to show that the DJR fold is represented in several widespread families of cellular proteins, including several groups of carbohydrate-active enzymes. We show that DJR-MCPs share a common ancestry with a distinct family of bacterial DJR proteins (DUF2961) involved in carbohydrate metabolism. Based on this finding, we propose a scenario in which bamfordviruses evolved from nonviral replicators, in particular plasmids, by recruiting a host protein for capsid formation. This sequence of events appears to be the general route of virus origin. The results of this work indicate that virus kingdoms Bamfordvirae, with the DJR-MCPs, and Helvetiavirae that possess two SJR-MCPs, have distinct origins, suggesting a reappraisal of the realm Varidnaviria.
Highlights
To cite this version: Mart Krupovic, Kira Makarova, Eugene Koonin
To investigate the provenance of the double jelly-roll major capsid protein (DJR-major capsid proteins (MCPs)), we searched the Protein Data Bank (PDB) database of protein structures using as queries the available double jelly-roll (DJR)-MCP structures of prokaryotic viruses, including bacteriophage PRD1 (Tectiviridae; PDB ID: 1hx6) [38], FLiP (Finnlakeviridae; PDB ID: 5oac) [39], and PM2 (Corticoviridae; PDB ID: 2vvf) [40], and archaeal virus Sulfolobus turreted icosahedral virus (STIV; Turriviridae; PDB ID: 3j31) [41]
The analysis reported here alters the parsimonious scenario for the origin of virus DJR-MCPs and, by inference, of bamfordviruses themselves
Summary
To cite this version: Mart Krupovic, Kira Makarova, Eugene Koonin. Cellular homologs of the double jelly-roll major capsid proteins clarify the origins of an ancient virus kingdom. L’archive ouverte pluridisciplinaire HAL, est destinée au dépôt et à la diffusion de documents scientifiques de niveau recherche, publiés ou non, émanant des établissements d’enseignement et de recherche français ou étrangers, des laboratoires publics ou privés. We show that DJR-MCPs share a common ancestry with a distinct family of bacterial DJR proteins (DUF2961) involved in carbohydrate metabolism Based on this finding, we propose a scenario in which bamfordviruses evolved from nonviral replicators, in particular plasmids, by recruiting a host protein for capsid formation. Of functionally diverse cellular proteins, in particular, those involved in carbohydrate metabolism [16, 21] Such recruitment appears to have occurred on multiple occasions during virus evolution, resulting in the acquisition of more than 20 distinct major capsid proteins (MCPs) [21]
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