“Frozen evolution” of an RNA virus suggests accidental release as a potential cause of arbovirus re-emergence

Pascall, D. J. et al. (2020) “Frozen evolution” of an RNA virus suggests accidental release as a potential cause of arbovirus re-emergence. PLOS Biology, 18(4), e3000673. (doi: 10.1371/journal.pbio.3000673)

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Abstract

The mechanisms underlying virus emergence are rarely well understood, making the appearance of outbreaks largely unpredictable. Bluetongue virus serotype 8 (BTV-8), an arthropod-borne virus of ruminants, emerged in livestock in northern Europe in 2006, spreading to most European countries by 2009 and causing losses of billions of euros. Although the outbreak was successfully controlled through vaccination by early 2010, puzzlingly, a closely related BTV-8 strain re-emerged in France in 2015, triggering a second outbreak that is still ongoing. The origin of this virus and the mechanisms underlying its re-emergence are unknown. Here, we performed phylogenetic analyses of 164 whole BTV-8 genomes sampled throughout the two outbreaks. We demonstrate consistent clock-like virus evolution during both epizootics but found negligible evolutionary change between them. We estimate that the ancestor of the second outbreak dates from the height of the first outbreak in 2008. This implies that the virus had not been replicating for multiple years prior to its re-emergence in 2015. Given the absence of any known natural mechanism that could explain BTV-8 persistence over this long period without replication, we hypothesise that the second outbreak could have been initiated by accidental exposure of livestock to frozen material contaminated with virus from approximately 2008. Our work highlights new targets for pathogen surveillance programmes in livestock and illustrates the power of genomic epidemiology to identify pathways of infectious disease emergence.

Item Type:Articles
Keywords:Short Reports, Biology and life sciences, Computer and information sciences, Medicine and health sciences, People and places
Status:Published
Refereed:Yes
Glasgow Author(s) Enlighten ID:Singer, Dr Josh and Palmarini, Professor Massimo and Biek, Dr Roman and Mertens, Professor Peter and Nomikou, Dr Kyriaki and Pascall, Dr David and Jacquot, Dr Maude
Creator Roles:
Mertens, P.Conceptualization, Funding acquisition, Resources, Supervision, Writing – review and editing
Biek, R.Conceptualization, Funding acquisition, Investigation, Methodology, Project administration, Supervision, Writing – original draft, ["credit_typename_" not defined]
Palmarini, M.Conceptualization, Funding acquisition, Project administration, Supervision, Writing – original draft, ["credit_typename_" not defined]
Pascall, D.Data curation, Formal analysis, Investigation, Methodology, Visualization, Writing – original draft, Writing – review and editing
Nomikou, K.Data curation, Formal analysis, Investigation, Methodology, Project administration, Writing – review and editing
Da Silva Costa, A.Investigation, Methodology, Writing – review and editing
Jacquot, M.Investigation, Methodology, Writing – review and editing
Singer, J.Software, Writing – review and editing
Authors: Pascall, D. J., Nomikou, K., Bréard, E., Zientara, S., Filipe, A. d. S., Hoffmann, B., Jacquot, M., Singer, J., De Clercq, K., Bøtner, A., Sailleau, C., Viarouge, C., Batten, C., Puggioni, G., Ligios, C., Savini, G., van Rijn, P. A., Mertens, P. P.C., Biek, R., and Palmarini, M.
College/School:College of Medical Veterinary and Life Sciences > Institute of Biodiversity Animal Health and Comparative Medicine
College of Medical Veterinary and Life Sciences > Institute of Infection Immunity and Inflammation
Journal Name:PLOS Biology
Publisher:Public Library of Science
ISSN:1545-7885
ISSN (Online):1545-7885
Copyright Holders:Copyright © 2020 Pascall et al.
First Published:First published in PLoS Biology 18(4): e3000673
Publisher Policy:Reproduced under a Creative Commons Licence

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Project CodeAward NoProject NamePrincipal InvestigatorFunder's NameFunder RefLead Dept
164053Phylogeography, transmission dynamics and pathogenesis of bluetongueMassimo PalmariniWellcome Trust (WELLCOTR)092806/Z/10/ZIII - Centre for Virus Research
301049Host determinants of disease outcomes in arboviral infectionsMassimo PalmariniWellcome Trust (WELLCOTR)206369/Z/17/ZIII - Centre for Virus Research