publication . Article . 2019

Shared Common Ancestry of Rodent Alphacoronaviruses Sampled Globally

Tsoleridis, Theocharis; Chappell, Joseph; Onianwa, Okechukwu; Marston, Denise; Fooks, Anthony; Monchatre-Leroy, Elodie; Umhang, Gérald; Müller, Marcel; Drexler, Jan; Drosten, Christian; ...
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Open Access English
  • Published: 01 Feb 2019 Journal: Viruses, volume 11, issue 2 (eissn: 1999-4915, Copyright policy)
  • Publisher: MDPI
  • Country: France
Abstract
International audience; The recent discovery of novel alphacoronaviruses (alpha-CoVs) in European and Asian rodents revealed that rodent coronaviruses (CoVs) sampled worldwide formed a discrete phylogenetic group within this genus. To determine the evolutionary history of rodent CoVs in more detail, particularly the relative frequencies of virus-host co-divergence and cross-species transmission, we recovered longer fragments of CoV genomes from previously discovered European rodent alpha-CoVs using a combination of PCR and high-throughput sequencing. Accordingly, the full genome sequence was retrieved from the UK rat coronavirus, along with partial genome sequences from the UK field vole and Poland-resident bank vole CoVs, and a short conserved ORF1b fragment from the French rabbit CoV. Genome and phylogenetic analysis showed that despite their diverse geographic origins, all rodent alpha-CoVs formed a single monophyletic group and shared similar features, such as the same gene constellations, a recombinant beta-CoV spike gene, and similar core transcriptional regulatory sequences (TRS). These data suggest that all rodent alpha CoVs sampled so far originate from a single common ancestor, and that there has likely been a long-term association between alpha CoVs and rodents. Despite this likely antiquity, the phylogenetic pattern of the alpha-CoVs was also suggestive of relatively frequent host-jumping among the different rodent species.
Persistent Identifiers

doi: 10.3390/v11020125

pmc: PMC6409636

pmid: 30704076

Fields of Science and Technology classification (FOS)
03 medical and health sciences, 0301 basic medicine, 030304 developmental biology, 030306 microbiology
Subjects
Medical Subject Headings: virusesvirus diseasesrespiratory tract diseasesrespiratory systembiochemical phenomena, metabolism, and nutrition
free text keywords: Article, coronavirus, alphacoronavirus, rodents, ancestry, recombination, evolution, Virology, Infectious Diseases, [SDV]Life Sciences [q-bio], [SDV.MP.VIR]Life Sciences [q-bio]/Microbiology and Parasitology/Virology, [SDV.SPEE]Life Sciences [q-bio]/Santé publique et épidémiologie, COVID-19 ; alphacoronavirus ; rodents ; evolution ; recombination ; ancestry ; Coronavirus, Phylogenetic tree, Monophyly, Phylogenetic Pattern, Field vole, biology.organism_classification, biology, Bank vole, Alphacoronavirus, Genome, Whole genome sequencing, Evolutionary biology, lcsh:Microbiology, lcsh:QR1-502
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Funded by
EC| COMPARE
Project
COMPARE
COllaborative Management Platform for detection and Analyses of (Re-)emerging and foodborne outbreaks in Europe
  • Funder: European Commission (EC)
  • Project Code: 643476
  • Funding stream: H2020 | RIA
, UKRI| BB/J014508/1
Project
BB/J014508/1
  • Funder: UK Research and Innovation (UKRI)
  • Project Code: BB/J014508/1
  • Funding stream: BBSRC
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Article . 2019
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28 references, page 1 of 2

Hudson, C., Beaudette, F.R.. Infection of the cloaca with the virus of infectious bronchitis. Science. 1932; 76: 34 [OpenAIRE] [DOI]

Hamre, D., Procknow, J.J.. A new virus isolated from the human respiratory tract. Proc. Soc. Exp. Biol. Med.. 1966; 121: 190-193 [OpenAIRE] [PubMed] [DOI]

Weiss, S., Navas-Martin, S.. Coronavirus pathogenesis and the emerging pathogen severe acute respiratory syndrome coronavirus. Microbiol. Mol. Biol. Rev.. 2005; 69: 635-664 [OpenAIRE] [PubMed] [DOI]

Luis, A.D., Hayman, D.T., O’Shea, T.J., Cryan, P.M., Gilbert, A.T., Pulliam, J.R., Mills, J.N., Timonin, M.E., Willis, C.K., Cunningham, A.A.. A comparison of bats and rodents as reservoirs of zoonotic viruses: Are bats special?. Proc. Biol. Sci.. 2013; 280 [OpenAIRE] [DOI]

Huchon, D., Madsen, O., Sibbald, M.J., Ament, K., Stanhope, M.J., Catzeflis, F., de Jong, W.W., Douzery, E.J.. Rodent phylogeny and a timescale for the evolution of Glires: Evidence from an extensive taxon sampling using three nuclear genes. Mol. Biol. Evol.. 2002; 19: 1053-1065 [OpenAIRE] [PubMed] [DOI]

Phan, T.G., Kapusinszky, B., Wang, C., Rose, R.K., Lipton, H.L., Delwart, E.L.. The fecal viral flora of wild rodents. PLoS Pathog.. 2011; 7 [OpenAIRE] [PubMed] [DOI]

Cheever, F.S., Daniels, J.B., Pappenheimer, A.M., Bailey, O.T.. A murine virus (JHM) causing disseminated encephalomyelitis with extensive destruction of myelin. J. Exp. Med.. 1949; 90: 181-194 [OpenAIRE] [PubMed] [DOI]

Parker, J.C., Cross, S.S., Rowe, W.P.. Rat coronavirus (RCV): A prevalent, naturally occurring pneumotropic virus of rats. Arch. Gesamte Virusforsch.. 1970; 31: 293-302 [OpenAIRE] [PubMed] [DOI]

Tsoleridis, T., Onianwa, O., Horncastle, E., Dayman, E., Zhu, M., Danjittrong, T., Wachtl, M., Behnke, J.M., Chapman, S., Strong, V.. Discovery of Novel Alphacoronaviruses in European Rodents and Shrews. Viruses. 2016; 8 [OpenAIRE] [PubMed] [DOI]

Ge, X.Y., Yang, W.H., Zhou, J.H., Li, B., Zhang, W., Shi, Z.L., Zhang, Y.Z.. Detection of alpha- and betacoronaviruses in rodents from Yunnan, China. Virol. J.. 2017; 14: 98 [OpenAIRE] [PubMed] [DOI]

Hu, D., Zhu, C., Wang, Y., Ai, L., Yang, L., Ye, F., Ding, C., Chen, J., He, B., Zhu, J.. Virome analysis for identification of novel mammalian viruses in bats from Southeast China. Sci. Rep.. 2017; 7: 10917 [OpenAIRE] [PubMed] [DOI]

Monchatre-Leroy, E., Boué, F., Boucher, J.-M., Renault, C., Moutou, F., Ar Gouilh, M., Umhang, G.. Identification of Alpha and Beta Coronavirus in Wildlife Species in France: Bats, Rodents, Rabbits, and Hedgehogs. Viruses. 2017; 9 [OpenAIRE] [DOI]

Shi, M., Lin, X.D., Tian, J.H., Chen, L.J., Chen, X., Li, C.X., Qin, X.C., Li, J., Cao, J.P., Eden, J.S.. Redefining the invertebrate RNA virosphere. Nature. 2016 [OpenAIRE] [DOI]

Thompson, J.D., Higgins, D.G., Gibson, T.J.. CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res.. 1994; 22: 4673-4680 [OpenAIRE] [PubMed] [DOI]

Kumar, S., Stecher, G., Tamura, K.. MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Mol. Biol. Evol.. 2016; 33: 1870-1874 [OpenAIRE] [PubMed] [DOI]

28 references, page 1 of 2
6 research outcomes, page 1 of 1
Abstract
International audience; The recent discovery of novel alphacoronaviruses (alpha-CoVs) in European and Asian rodents revealed that rodent coronaviruses (CoVs) sampled worldwide formed a discrete phylogenetic group within this genus. To determine the evolutionary history of rodent CoVs in more detail, particularly the relative frequencies of virus-host co-divergence and cross-species transmission, we recovered longer fragments of CoV genomes from previously discovered European rodent alpha-CoVs using a combination of PCR and high-throughput sequencing. Accordingly, the full genome sequence was retrieved from the UK rat coronavirus, along with partial genome sequences from the UK field vole and Poland-resident bank vole CoVs, and a short conserved ORF1b fragment from the French rabbit CoV. Genome and phylogenetic analysis showed that despite their diverse geographic origins, all rodent alpha-CoVs formed a single monophyletic group and shared similar features, such as the same gene constellations, a recombinant beta-CoV spike gene, and similar core transcriptional regulatory sequences (TRS). These data suggest that all rodent alpha CoVs sampled so far originate from a single common ancestor, and that there has likely been a long-term association between alpha CoVs and rodents. Despite this likely antiquity, the phylogenetic pattern of the alpha-CoVs was also suggestive of relatively frequent host-jumping among the different rodent species.
Persistent Identifiers

doi: 10.3390/v11020125

pmc: PMC6409636

pmid: 30704076

Fields of Science and Technology classification (FOS)
03 medical and health sciences, 0301 basic medicine, 030304 developmental biology, 030306 microbiology
Subjects
Medical Subject Headings: virusesvirus diseasesrespiratory tract diseasesrespiratory systembiochemical phenomena, metabolism, and nutrition
free text keywords: Article, coronavirus, alphacoronavirus, rodents, ancestry, recombination, evolution, Virology, Infectious Diseases, [SDV]Life Sciences [q-bio], [SDV.MP.VIR]Life Sciences [q-bio]/Microbiology and Parasitology/Virology, [SDV.SPEE]Life Sciences [q-bio]/Santé publique et épidémiologie, COVID-19 ; alphacoronavirus ; rodents ; evolution ; recombination ; ancestry ; Coronavirus, Phylogenetic tree, Monophyly, Phylogenetic Pattern, Field vole, biology.organism_classification, biology, Bank vole, Alphacoronavirus, Genome, Whole genome sequencing, Evolutionary biology, lcsh:Microbiology, lcsh:QR1-502
Related Organizations
View more
Communities
Communities with gateway
OpenAIRE Connect image
Other Communities
  • COVID-19
Funded by
EC| COMPARE
Project
COMPARE
COllaborative Management Platform for detection and Analyses of (Re-)emerging and foodborne outbreaks in Europe
  • Funder: European Commission (EC)
  • Project Code: 643476
  • Funding stream: H2020 | RIA
, UKRI| BB/J014508/1
Project
BB/J014508/1
  • Funder: UK Research and Innovation (UKRI)
  • Project Code: BB/J014508/1
  • Funding stream: BBSRC
Download fromView all 9 versions
Open Access
Viruses
Article . 2019
Providers: PubMed Central
Open Access
Viruses
Article
Providers: UnpayWall
Open Access
Viruses
Article . 2019
Providers: DOAJ-Articles
Open Access
Fachrepositorium Lebenswissenschaften
Article . 2019
Providers: Fachrepositorium Lebenswissenschaften
View more
28 references, page 1 of 2

Hudson, C., Beaudette, F.R.. Infection of the cloaca with the virus of infectious bronchitis. Science. 1932; 76: 34 [OpenAIRE] [DOI]

Hamre, D., Procknow, J.J.. A new virus isolated from the human respiratory tract. Proc. Soc. Exp. Biol. Med.. 1966; 121: 190-193 [OpenAIRE] [PubMed] [DOI]

Weiss, S., Navas-Martin, S.. Coronavirus pathogenesis and the emerging pathogen severe acute respiratory syndrome coronavirus. Microbiol. Mol. Biol. Rev.. 2005; 69: 635-664 [OpenAIRE] [PubMed] [DOI]

Luis, A.D., Hayman, D.T., O’Shea, T.J., Cryan, P.M., Gilbert, A.T., Pulliam, J.R., Mills, J.N., Timonin, M.E., Willis, C.K., Cunningham, A.A.. A comparison of bats and rodents as reservoirs of zoonotic viruses: Are bats special?. Proc. Biol. Sci.. 2013; 280 [OpenAIRE] [DOI]

Huchon, D., Madsen, O., Sibbald, M.J., Ament, K., Stanhope, M.J., Catzeflis, F., de Jong, W.W., Douzery, E.J.. Rodent phylogeny and a timescale for the evolution of Glires: Evidence from an extensive taxon sampling using three nuclear genes. Mol. Biol. Evol.. 2002; 19: 1053-1065 [OpenAIRE] [PubMed] [DOI]

Phan, T.G., Kapusinszky, B., Wang, C., Rose, R.K., Lipton, H.L., Delwart, E.L.. The fecal viral flora of wild rodents. PLoS Pathog.. 2011; 7 [OpenAIRE] [PubMed] [DOI]

Cheever, F.S., Daniels, J.B., Pappenheimer, A.M., Bailey, O.T.. A murine virus (JHM) causing disseminated encephalomyelitis with extensive destruction of myelin. J. Exp. Med.. 1949; 90: 181-194 [OpenAIRE] [PubMed] [DOI]

Parker, J.C., Cross, S.S., Rowe, W.P.. Rat coronavirus (RCV): A prevalent, naturally occurring pneumotropic virus of rats. Arch. Gesamte Virusforsch.. 1970; 31: 293-302 [OpenAIRE] [PubMed] [DOI]

Tsoleridis, T., Onianwa, O., Horncastle, E., Dayman, E., Zhu, M., Danjittrong, T., Wachtl, M., Behnke, J.M., Chapman, S., Strong, V.. Discovery of Novel Alphacoronaviruses in European Rodents and Shrews. Viruses. 2016; 8 [OpenAIRE] [PubMed] [DOI]

Ge, X.Y., Yang, W.H., Zhou, J.H., Li, B., Zhang, W., Shi, Z.L., Zhang, Y.Z.. Detection of alpha- and betacoronaviruses in rodents from Yunnan, China. Virol. J.. 2017; 14: 98 [OpenAIRE] [PubMed] [DOI]

Hu, D., Zhu, C., Wang, Y., Ai, L., Yang, L., Ye, F., Ding, C., Chen, J., He, B., Zhu, J.. Virome analysis for identification of novel mammalian viruses in bats from Southeast China. Sci. Rep.. 2017; 7: 10917 [OpenAIRE] [PubMed] [DOI]

Monchatre-Leroy, E., Boué, F., Boucher, J.-M., Renault, C., Moutou, F., Ar Gouilh, M., Umhang, G.. Identification of Alpha and Beta Coronavirus in Wildlife Species in France: Bats, Rodents, Rabbits, and Hedgehogs. Viruses. 2017; 9 [OpenAIRE] [DOI]

Shi, M., Lin, X.D., Tian, J.H., Chen, L.J., Chen, X., Li, C.X., Qin, X.C., Li, J., Cao, J.P., Eden, J.S.. Redefining the invertebrate RNA virosphere. Nature. 2016 [OpenAIRE] [DOI]

Thompson, J.D., Higgins, D.G., Gibson, T.J.. CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res.. 1994; 22: 4673-4680 [OpenAIRE] [PubMed] [DOI]

Kumar, S., Stecher, G., Tamura, K.. MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Mol. Biol. Evol.. 2016; 33: 1870-1874 [OpenAIRE] [PubMed] [DOI]

28 references, page 1 of 2
6 research outcomes, page 1 of 1
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