Comparative analysis reveals the long-term coevolutionary history of parvoviruses and vertebrates

Campbell, M. A., Loncar, S., Kotin, R. M. and Gifford, R. J. (2022) Comparative analysis reveals the long-term coevolutionary history of parvoviruses and vertebrates. PLoS Biology, 20(11), e3001867. (doi: 10.1371/journal.pbio.3001867) (PMID:36445931) (PMCID:PMC9707805)

[img] Text
286141.pdf - Published Version
Available under License Creative Commons Attribution.

4MB

Abstract

Parvoviruses (family Parvoviridae) are small DNA viruses that cause numerous diseases of medical, veterinary, and agricultural significance and have important applications in gene and anticancer therapy. DNA sequences derived from ancient parvoviruses are common in animal genomes and analysis of these endogenous parvoviral elements (EPVs) has demonstrated that the family, which includes twelve vertebrate-specific genera, arose in the distant evolutionary past. So far, however, such “paleovirological” analysis has only provided glimpses into the biology of ancient parvoviruses and their long-term evolutionary interactions with hosts. Here, we comprehensively map EPV diversity in 752 published vertebrate genomes, revealing defining aspects of ecology and evolution within individual parvovirus genera. We identify 364 distinct EPV sequences and show these represent approximately 200 unique germline incorporation events, involving at least five distinct parvovirus genera, which took place at points throughout the Cenozoic Era. We use the spatiotemporal and host range calibrations provided by these sequences to infer defining aspects of long-term evolution within individual parvovirus genera, including mammalian vicariance for genus Protoparvovirus, and interclass transmission for genus Dependoparvovirus. Moreover, our findings support a model of virus evolution in which the long-term cocirculation of multiple parvovirus genera in vertebrates reflects the adaptation of each viral genus to fill a distinct ecological niche. Our findings show that efforts to develop parvoviruses as therapeutic tools can be approached from a rational foundation based on comparative evolutionary analysis. To support this, we published our data in the form of an open, extensible, and cross-platform database designed to facilitate the wider utilisation of evolution-related domain knowledge in parvovirus research.

Item Type:Articles
Additional Information:This work was supported by funding from the Association Monégasque Contre les Myopathies (RK), and the Bill & Melinda Gates Foundation (OPP1202116 to RK).
Status:Published
Refereed:Yes
Glasgow Author(s) Enlighten ID:Gifford, Dr Robert
Creator Roles:
Gifford, R. J.Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Resources, Software, Validation, Visualization, Writing – original draft, Writing – review and editing
Authors: Campbell, M. A., Loncar, S., Kotin, R. M., and Gifford, R. J.
College/School:College of Medical Veterinary and Life Sciences > School of Infection & Immunity > Centre for Virus Research
Journal Name:PLoS Biology
Publisher:Public Library of Science
ISSN:1544-9173
ISSN (Online):1545-7885
Published Online:29 November 2022
Copyright Holders:Copyright © 2022 Campbell et al.
First Published:First published in PLoS Biology 20(10): e3001867
Publisher Policy:Reproduced under a Creative Commons License
Related URLs:
Data DOI:10.5281/zenodo.6968218

University Staff: Request a correction | Enlighten Editors: Update this record