Date Published: April 19, 2016
Publisher: Public Library of Science
Author(s): Christopher B. Buck, Koenraad Van Doorslaer, Alberto Peretti, Eileen M. Geoghegan, Michael J. Tisza, Ping An, Joshua P. Katz, James M. Pipas, Alison A. McBride, Alvin C. Camus, Alexa J. McDermott, Jennifer A. Dill, Eric Delwart, Terry F. F. Ng, Kata Farkas, Charlotte Austin, Simona Kraberger, William Davison, Diana V. Pastrana, Arvind Varsani, Denise A. Galloway.
Polyomaviruses are a family of DNA tumor viruses that are known to infect mammals and birds. To investigate the deeper evolutionary history of the family, we used a combination of viral metagenomics, bioinformatics, and structural modeling approaches to identify and characterize polyomavirus sequences associated with fish and arthropods. Analyses drawing upon the divergent new sequences indicate that polyomaviruses have been gradually co-evolving with their animal hosts for at least half a billion years. Phylogenetic analyses of individual polyomavirus genes suggest that some modern polyomavirus species arose after ancient recombination events involving distantly related polyomavirus lineages. The improved evolutionary model provides a useful platform for developing a more accurate taxonomic classification system for the viral family Polyomaviridae.
Murine polyomavirus (MPyV) was discovered in the mid-1950s as a filterable infectious agent that could induce salivary tumors in experimentally exposed mice [2, 3]. It was quickly established that the virus is potently carcinogenic, causing many different types of tumors (Greek poly + oma) in various experimental systems. When the first primate polyomavirus, simian vacuolating virus 40 (SV40), was discovered as an abundant contaminant in early poliovirus vaccines that had already been administered to millions of individuals, it posed significant cause for alarm (reviewed in ). The ensuing rush to study the molecular biology of polyomaviruses provided a great wealth of insights into basic cell biology and the fundamental mechanisms of tumorigenesis (reviewed in ).
In this report, we propose a comprehensive theoretical framework for understanding the evolutionary history of the viral family Polyomaviridae. Our model suggests that the last common ancestor of arthropods and vertebrates harbored at least one polyomavirus. In the ensuing roughly half billion years, polyomaviruses appear to have accumulated genetic change at a remarkably slow cumulative long-term pace, in a pattern consistent with the intrahost divergence model diagrammed in Fig 6. Qualitative comparisons of phylogenetic trees suggest the occurrence of ancient recombination events involving distantly related polyomavirus species.