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Novel Polyomaviruses in Mammals from Multiple Orders and Reassessment of Polyomavirus Evolution and Taxonomy

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Division 12 “Measles, Mumps, Rubella, and Viruses Affecting Immunocompromised Patients”, Robert Koch Institute, 13353 Berlin, Germany
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Laboratoire de Zoologie-Biologie, UFR Biosciences Université Félix Houphouët Boigny, Abidjan BP V 34, Cote D’Ivoire
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Centre de Recherche Pour le Développement, Université Alassane Ouattara, Bouaké BP V 1801, Cote D’Ivoire
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Laboratoire National D’appui au Développement Agricole/Laboratoire Central de Pathologie Animale, Bingerville BP 206, Cote D’Ivoire
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Institute of Biotechnology, Vilnius University, LT-10257 Vilnius, Lithuania
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Institut de Recerca i Tecnologia Agroalimentàries (IRTA), Centre de Recerca en Sanitat Animal (CReSA, IRTA-UAB), 08197 Barcelona, Spain
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EcoHealth Research Group, Conservation & Ecosystem Health Alliance (CEHA), Kampala 34153, Uganda
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College of Veterinary Medicine, Animal Resources & Biosecurity (COVAB), Makerere University, Kampala 34153, Uganda
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Institut National de Recherche Bio-Médicale, Kinshasa-Gombe BP 1197, Congo
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P3 “Epidemiology of highly pathogenic microorganisms”, Robert Koch Institute, 13353 Berlin, Germany
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Landscape Ecology & Environmental Systems Analysis, Institute of Geoecology, Technische Universität Braunschweig, 38106 Braunschweig, Germany
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Leibniz Institute for Zoo and Wildlife Research (IZW), 10315 Berlin, Germany
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Friedrich-Loeffler-Institut, Institute of Novel and Emerging Infectious Diseases, 17493 Greifswald-Insel Riems, Germany
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German Center for Infection Research (DZIF), Partner Site Hamburg-Lübeck-Borstel-Insel Riems, 17493 Greifswald-Insel Riems, Germany
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P3 “Viral Evolution”, Robert Koch Institute, 13353 Berlin, Germany
*
Author to whom correspondence should be addressed.
Viruses 2019, 11(10), 930; https://doi.org/10.3390/v11100930
Received: 29 August 2019 / Revised: 4 October 2019 / Accepted: 7 October 2019 / Published: 10 October 2019
(This article belongs to the Section Animal Viruses)
As the phylogenetic organization of mammalian polyomaviruses is complex and currently incompletely resolved, we aimed at a deeper insight into their evolution by identifying polyomaviruses in host orders and families that have either rarely or not been studied. Sixteen unknown and two known polyomaviruses were identified in animals that belong to 5 orders, 16 genera, and 16 species. From 11 novel polyomaviruses, full genomes could be determined. Splice sites were predicted for large and small T antigen (LTAg, STAg) coding sequences (CDS) and examined experimentally in transfected cell culture. In addition, splice sites of seven published polyomaviruses were analyzed. Based on these data, LTAg and STAg annotations were corrected for 10/86 and 74/86 published polyomaviruses, respectively. For 25 polyomaviruses, a spliced middle T CDS was observed or predicted. Splice sites that likely indicate expression of additional, alternative T antigens, were experimentally detected for six polyomaviruses. In contrast to all other mammalian polyomaviruses, three closely related cetartiodactyl polyomaviruses display two introns within their LTAg CDS. In addition, the VP2 of Glis glis (edible dormouse) polyomavirus 1 was observed to be encoded by a spliced transcript, a unique experimental finding within the Polyomaviridae family. Co-phylogenetic analyses based on LTAg CDS revealed a measurable signal of codivergence when considering all mammalian polyomaviruses, most likely driven by relatively recent codivergence events. Lineage duplication was the only other process whose influence on polyomavirus evolution was unambiguous. Finally, our analyses suggest that an update of the taxonomy of the family is required, including the creation of novel genera of mammalian and non-mammalian polyomaviruses. View Full-Text
Keywords: polyomavirus; genome; evolution; T antigen; VP2; splicing; taxonomy polyomavirus; genome; evolution; T antigen; VP2; splicing; taxonomy
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Ehlers, B.; Anoh, A.E.; Ben Salem, N.; Broll, S.; Couacy-Hymann, E.; Fischer, D.; Gedvilaite, A.; Ingenhütt, N.; Liebmann, S.; Martin, M.; Mossoun, A.; Mugisha, L.; Muyembe-Tamfum, J.-J.; Pauly, M.; Pérez de Val, B.; Preugschas, H.; Richter, D.; Schubert, G.; Szentiks, C.A.; Teichmann, T.; Walter, C.; Ulrich, R.G.; Wiersma, L.; Leendertz, F.H.; Calvignac-Spencer, S. Novel Polyomaviruses in Mammals from Multiple Orders and Reassessment of Polyomavirus Evolution and Taxonomy. Viruses 2019, 11, 930.

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