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; ...
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
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
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
  • Funder: UK Research and Innovation (UKRI)
  • Project Code: BB/J014508/1
  • Funding stream: BBSRC
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
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
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
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
  • Funder: UK Research and Innovation (UKRI)
  • Project Code: BB/J014508/1
  • Funding stream: BBSRC
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
Any information missing or wrong?Report an Issue