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

Type Article
Date 2020-04
Language English
Author(s) Pascall David J.1, Nomikou KyriakiORCID2, 3, Breard Emmanuel4, Zientara StephanORCID4, Filipe Ana Da Silva2, Hoffmann Bernd5, Jacquot MaudeORCID6, 7, Singer Joshua B.2, de Clercq KrisORCID8, Botner Anette9, 10, Sailleau Corinne4, Viarouge Cyril4, Batten Carrie11, Puggioni Giantonella12, Ligios CiriacoORCID12, Savini GiovanniORCID13, Van Rijn Piet A.ORCID14, 15, Mertens Peter P. C.3, 11, Biek RomanORCID1, Palmarini Massimo2
Affiliation(s) 1 : Univ Glasgow, Boyd Orr Ctr Populat & Ecosyst Hlth, Inst Biodivers Anim Hlth & Comparat Med, Glasgow, Lanark, Scotland.
2 : Univ Glasgow, MRC, Ctr Virus Res, Glasgow, Lanark, Scotland.
3 : Univ Nottingham, Sch Vet Med & Sci, Loughborough, Leics, England.
4 : Univ Paris Est, ANSES, Lab Sante Anim Alfort, UMR Virol,INRA,Ecole Natl Vet Alfort, Maisons Alfort, France.
5 : Friedrich Loeffler Inst, Inst Diagnost Virol, Greifswald, Germany.
6 : Univ Brussels, Spatial Epidemiol Lab SpELL, Brussels, Belgium.
7 : INRAE VetAgro Sup, UMR Epidemiol Anim & Zoonot Dis, St Genes Champanelle, France.
8 : Sciensano, Infect Dis Anim Exot & Particular Dis, Brussels, Belgium.
9 : Univ Copenhagen, Dept Vet & Anim Sci, Sect Vet Clin Microbiol, Copenhagen, Denmark.
10 : Statens Serum Inst, Dept Virus & Microbiol Special Diagnost, Copenhagen, Denmark.
11 : Pirbright Inst, Woking, Surrey, England.
12 : Ist Zooprofilatt Sperimentale Sardegna, Via Duca Abruzzi, Sassari, Italy.
13 : Ist Zooprofilatt Sperimentale Abruzzo & Molise IZ, Teramo, Italy.
14 : Wageningen Biovet Res WBVR, Dept Virol, Lelystad, Netherlands.
15 : North West Univ, Ctr Human Metabol, Dept Biochem, Potchefstroom, South Africa.
Source Plos Biology (1544-9173) (Public Library Science), 2020-04 , Vol. 18 , N. 4 , P. e3000673 (19p.)
DOI 10.1371/journal.pbio.3000673
WOS© Times Cited 11

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.

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Publisher's official version 19 1 MB Open access
S1 Data. Scripts for the analyses performed in the paper in a zipped folder. 16 KB Open access
S2 Data. BEAST 1.10 XMLs for the two Bayesian analyses in a zipped folder. 128 KB Open access
S3 Data. Data files used in the analyses in this paper in a zipped folder. 2 MB Open access
S1 Fig. Phylogenetic tree of 164 BTV-8 samples collected during the European outbreak between 2006 and 2018 with tip labels. 2 MB Open access
S2 Fig. Timescaled phylogenetic tree of BTV-8 samples collected during the European outbreaks between 2006 and 2018 with tip labels. 2 MB Open access
S1 Table. Table of all sample IDs and their associated metadata. 41 KB Open access
Preprint https://doi.org/10.1101/2019.12.11.872705 32 8 MB Open access
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Pascall David J., Nomikou Kyriaki, Breard Emmanuel, Zientara Stephan, Filipe Ana Da Silva, Hoffmann Bernd, Jacquot Maude, Singer Joshua B., de Clercq Kris, Botner Anette, Sailleau Corinne, Viarouge Cyril, Batten Carrie, Puggioni Giantonella, Ligios Ciriaco, Savini Giovanni, Van Rijn Piet A., Mertens Peter P. C., Biek Roman, Palmarini Massimo (2020). "Frozen evolution" of an RNA virus suggests accidental release as a potential cause of arbovirus re-emergence. Plos Biology, 18(4), e3000673 (19p.). Publisher's official version : https://doi.org/10.1371/journal.pbio.3000673 , Open Access version : https://archimer.ifremer.fr/doc/00667/77881/