SARS-CoV related Betacoronavirus and diverse Alphacoronavirus members found in western old-world

Meriadeg Ar Gouilh, Sébastien J Puechmaille, Laure Diancourt, Mathias Vandenbogaert, Jordi Serra-Cobo, Marc Lopez Roïg, Paul Brown, François Moutou, Valérie Caro, Astrid Vabret, Jean-Claude Manuguerra, EPICOREM consortium, Meriadeg Ar Gouilh, Sébastien J Puechmaille, Laure Diancourt, Mathias Vandenbogaert, Jordi Serra-Cobo, Marc Lopez Roïg, Paul Brown, François Moutou, Valérie Caro, Astrid Vabret, Jean-Claude Manuguerra, EPICOREM consortium

Abstract

The emergence of SARS-CoV and MERS-CoV, triggered the discovery of a high diversity of coronaviruses in bats. Studies from Europe have shown that coronaviruses circulate in bats in France but this reflects only a fraction of the whole diversity. In the current study the diversity of coronaviruses circulating in western Europe was extensively explored. Ten alphacoronaviruses in eleven bat species belonging to the Miniopteridae, Vespertilionidae and Rhinolophidae families and, a SARS-CoV-related Betacoronavirus in Rhinolophus ferrumequinum were identified. The diversity and prevalence of bat coronaviruses presently reported from western Europe is much higher than previously described and includes a SARS-CoV sister group. This diversity demonstrates the dynamic evolution and circulation of coronaviruses in this species. That said, the identified coronaviruses were consistently associated with a particular bat species or genus, and these relationships were maintained no matter the geographic location. The observed phylogenetic grouping of coronaviruses from the same species in Europe and Asia, emphasizes the role of host/pathogen coevolution in this group.

Keywords: Bats; Chiroptera; Coronavirus; Diversity; Emergence; Europe; Evolution; MERS-CoV; Phylogenetics; SARS-CoV.

Copyright © 2018 Elsevier Inc. All rights reserved.

Figures

Graphical abstract
Graphical abstract
Fig. 1
Fig. 1
Bayesian phylogeny of 127 genetic sequences representative of coronavirus strains detected in the study with sequences representing the world diversity of Coronavirinae. A) Nsp12 sequences were aligned using Mafft 7 (http://mafft.cbrc.jp). Statistical support (posterior probability) of nodes are depicted using a gradual color code of the tree, red indicating significant posterior probability values (>0.95). Strain names and main information is written in taxa labels. Viruses detected in this study are highlighted in purple.
Fig. 2
Fig. 2
Phylogenetic analysis and geo-localisation of coronaviruses detected in the Western Palearctic region. A) Bayesian phylogeny depicted in Fig. 1 (selected nodes collapsed for clarity reasons) showing clusters including a number of sequences ranging from 3 to 63 with a mean of 14 per clade. Statistical support (posterior probability) of nodes are depicted using a gradual color code of the tree, red indicating significant posterior probability values (>0.95). Labels of viruses detected in this study are bolded and coloured in blue. Corresponding host names are indicated in the right panel, in front of each taxa reported in the study. When significant mixing of species at the roost was observed, the name of the co-roosting coronavirus-negative species is added in brackets. Country of origin and identity score (ID) to the closest reference found in GenBank were also added for each coronavirus clade detected in this study. B) Map of the study region depicting the 39 investigated sites and highlighting in red those where bat samples were found positive for coronaviruses.
Fig. S2
Fig. S2
Detail of the alignment of several coronavirus phylogroups belonging to Betacoronavirus and Alphacoronavirus genera. Details of the alignment generated by MAFFT and used for phylogenetic reconstruction exhibiting regions with genetic differences between sequences (i.e. SNPs). GenBank identification numbers, strain partial names and partial sequences extracted from the alignment which shows variable positions affecting phylogroups Betacoronavirus EPI1 and Alphacoronavirus EPI4.

References

    1. Balboni A., Battilani M., Prosperi S. The SARS-like coronaviruses: the role of bats and evolutionary relationships with SARS coronavirus. New Microbiol. 2012;35:1–16.
    1. Barataud M., Aulagnier S. Pourquoi certaines espèces de chauves-souris s'associent-elles en essaims mixtes durant lamise-bas et l'élevage des jeunes? Exemple en Limousin. Arvicola. 2012;20:40–42.
    1. Bermingham A., Chand M.A., Brown C.S., Aarons E., Tong C., Langrish C. Severe respiratory illness caused by a novel coronavirus, in a patient transferred to the United Kingdom from the middle East, September 2012. Eur. Surveill. Bull. Eur. Sur Mal. Transm. Eur. Commun. Dis. Bull. 2012;17:20290.
    1. CBEM Reusken, Lina P.H.C., Pielaat A., de Vries A., Dam-Deisz C., Adema J. Circulation of group 2 coronaviruses in a bat species common to urban areas in Western Europe. Vector-Borne Zoonotic Dis. 2010;10:785–791. doi: 10.1089/vbz.2009.0173.
    1. Crucitti P. Caratteristiche della aggregazione Miniopterus schreibersi - Myotis capaccinii nel Lazio, Italia centrale (Chiroptera) Boll. Mus. Reg. Sci. Nat. 1993;11:407–422.
    1. Cui J., Han N., Streicker D., Li G., Tang X., Shi Z. Evolutionary relationships between bat coronaviruses and their hosts. Emerg. Infect. Dis. 2007;13:1526–1532.
    1. Darriba D., Taboada G.L., Doallo R., Posada D. jModelTest 2: more models, new heuristics and parallel computing. Nat. Methods. 2012;9 doi: 10.1038/nmeth.2109. (772–772)
    1. Dominguez S.R., Sims G.E., Wentworth D.E., Halpin R.A., Robinson C.C., Town C.D. Genomic analysis of 16 Colorado human NL63 coronaviruses identifies a new genotype, high sequence diversity in the N-terminal domain of the spike gene and evidence of recombination. J. Gen. Virol. 2012;93:2387–2398. doi: 10.1099/vir.0.044628-0.
    1. Drexler J.F., Gloza-Rausch F., Glende J., Corman V.M., Muth D., Goettsche M. Genomic characterization of severe acute respiratory syndrome-related coronavirus in european bats and classification of coronaviruses based on partial RNA-dependent RNA polymerase gene sequences. J. Virol. 2010;84:11336–11349. doi: 10.1128/JVI.00650-10.
    1. Drexler J.F., Corman V.M., Drosten C. Ecology, evolution and classification of bat coronaviruses in the aftermath of SARS. Antivir. Res. 2014;101:45–56. doi: 10.1016/j.antiviral.2013.10.013.
    1. Drosten C., Günther S., Preiser W., Werf S., van der, Brodt H.-R., Becker S. Identification of a novel coronavirus in patients with severe acute respiratory syndrome. N. Engl. J. Med. 2003;348:1967–1976. doi: 10.1056/NEJMoa030747.
    1. Drummond A.J., Rambaut A. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 2007;7 doi: 10.1186/1471-2148-7-214. (214–214)
    1. Drummond A.J., Ho S.Y.W., Phillips M.J., Rambaut A. Relaxed phylogenetics and dating with confidence. PLoS Biol. 2006;4:e88. doi: 10.1371/journal.pbio.0040088.
    1. Falcón A., Vázquez-Morón S., Casas I., Aznar C., Ruiz G., Pozo F. Detection of alpha and betacoronaviruses in multiple Iberian bat species. Arch. Virol. 2011;156:1883–1890. doi: 10.1007/s00705-011-1057-1.
    1. Fischer K., Zeus V., Kwasnitschka L., Kerth G., Haase M., Groschup M.H. Insectivorous bats carry host specific astroviruses and coronaviruses across different regions in Germany. Infect. Genet Evol. 2016;37:108–116. doi: 10.1016/j.meegid.2015.11.010.
    1. Foley N.M., Thong V.D., Soisook P., Goodman S.M., Armstrong K.N., Jacobs D.S. How and why overcome the impediments to resolution: lessons from rhinolophid and hipposiderid bats. Mol. Biol. Evol. 2015;32:313–333. doi: 10.1093/molbev/msu329.
    1. Ge X.-Y., Li J.-L., Yang X.-L., Chmura A.A., Zhu G., Epstein J.H. Isolation and characterization of a bat SARS-like coronavirus that uses the ACE2 receptor. Nature. 2013;503:535–538. doi: 10.1038/nature12711.
    1. Gloza-Rausch F., Ipsen A., Seebens A., Göttsche M., Panning M., Drexler J.F. Detection and prevalence patterns of group I coronaviruses in bats, northern Germany. Emerg. Infect. Dis. 2008;14(626):631.
    1. Goffard A., Demanche C., Arthur L., Pinçon C., Michaux J., Dubuisson J. Alphacoronaviruses detected in French bats are phylogeographically linked to coronaviruses of European bats. Viruses. 2015;7:6279–6290. doi: 10.3390/v7122937.
    1. Gouilh M.A., Puechmaille S.J., Gonzalez J.-P., Teeling E., Kittayapong P., Manuguerra J.-C. SARS-Coronavirus ancestor's foot-prints in South-East Asian bat colonies and the refuge theory. Infect. Genet Evol. 2011;11:1690–1702. doi: 10.1016/j.meegid.2011.06.021.
    1. Gouy M., Guindon S., Gascuel O. Seaview version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol. Biol. Evol. 2010;27:221–224. doi: 10.1093/molbev/msp259.
    1. Guindon S., Dufayard J.-F., Lefort V., Anisimova M., Hordijk W., Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 2010;59:307–321. doi: 10.1093/sysbio/syq010.
    1. Huynh J., Li S., Yount B., Smith A., Sturges L., Olsen J.C. Evidence supporting a zoonotic origin of human coronavirus strain NL63. J. Virol. 2012;86:12816–12825. doi: 10.1128/JVI.00906-12.
    1. Katoh K., Standley D.M. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 2013;30:772–780. doi: 10.1093/molbev/mst010.
    1. Kin N., Miszczak F., Lin W., Gouilh M.A., Vabret A., Consortium E. Genomic analysis of 15 human coronaviruses OC43 (HCoV-OC43s) circulating in France from 2001 to 2013 reveals a high intra-specific diversity with new recombinant genotypes. Viruses. 2015;7:2358–2377. doi: 10.3390/v7052358.
    1. Kin N., Miszczak F., Diancourt L., Caro V., Moutou F., Vabret A. Comparative molecular epidemiology of two closely related coronaviruses, bovine coronavirus (BCoV) and human coronavirus OC43 (HCoV-OC43), reveals a different evolutionary pattern. Infect. Genet Evol. J. Mol. Epidemiol. Evol. Genet Infect. Dis. 2016;40:186–191. doi: 10.1016/j.meegid.2016.03.006.
    1. Kingman J.F.C. The coalescent. Stoch. Process Appl. 1982;13:235–248. doi: 10.1016/0304-4149(82)90011-4.
    1. Kohl C., Kurth A. European bats as carriers of viruses with zoonotic potential. Viruses. 2014;6:3110–3128. doi: 10.3390/v6083110.
    1. Lau S.K.P., Woo P.C.Y., Li K.S.M., Huang Y., Wang M., Lam C.S.F. Complete genome sequence of bat coronavirus HKU2 from Chinese horseshoe bats revealed a much smaller spike gene with a different evolutionary lineage from the rest of the genome. Virology. 2007;367:428–439. doi: 10.1016/j.virol.2007.06.009.
    1. Lau S.K.P., Li K.S.M., Huang Y., Shek C.-T., Tse H., Wang M. Eco-epidemiology and complete genome comparison of SARS-related Rhinolophus bat coronavirus in China reveal bats as reservoir for acute, self-limiting infection that allows recombination events. J. Virol. 2010 doi: 10.1128/JVI.02219-09.
    1. Lelli D., Papetti A., Sabelli C., Rosti E., Moreno A., Boniotti M.B. Detection of coronaviruses in bats of various species in Italy. Viruses. 2013;5:2679–2689. doi: 10.3390/v5112679.
    1. Li W., Shi Z., Yu M., Ren W., Smith C., Epstein J.H. Bats are natural reservoirs of SARS-like coronaviruses. Science. 2005;310:676–679. (doi:1118391)
    1. Li Z., Hu Y., Zhan H., Yun X., Du Y., Ke X. An epidemiological investigation of bats carrying SARS-CoV in Guangzhou and its vicinity. Nan Fang. Yi Ke Xue Xue Bao. 2006;26:949–953.
    1. Puechmaille S.J., Mathy G., Petit E.J. Good DNA from bat droppings. Acta Chiropterologica. 2007;9:269–276. doi: 10.3161/1733-5329(2007)9[269:GDFBD];2.
    1. Pyrc K., Dijkman R., Deng L., Jebbink M.F., Ross H.A., Berkhout B. Mosaic structure of human coronavirus NL63, one thousand years of evolution. J. Mol. Biol. 2006;364(964):973. doi: 10.1016/j.jmb.2006.09.074.
    1. Quan P.-L., Firth C., Street C., Henriquez J.A., Petrosov A., Tashmukhamedova A. Identification of a severe acute respiratory syndrome coronavirus-like virus in a leaf-nosed bat in Nigeria. mBio. 2010;1 doi: 10.1128/mBio.00208-10. (e00208-10-e00208-18)
    1. Rihtarič D., Hostnik P., Steyer A., Grom J., Toplak I. Identification of SARS-like coronaviruses in horseshoe bats (Rhinolophus hipposideros) in Slovenia. Arch. Virol. 2010;155:507–514. doi: 10.1007/s00705-010-0612-5.
    1. Tang X.C., Zhang J.X., Zhang S.Y., Wang P., Fan X.H., Li L.F. Prevalence and Genetic Diversity of Coronaviruses in Bats from China. J. Virol. 2006;80:7481–7490. doi: 10.1128/JVI.00697-06.
    1. Tong S., Conrardy C., Ruone S., Kuzmin I.V., Guo X., Tao Y. Detection of novel SARS-like and other coronaviruses in bats from Kenya. Emerg. Infect. Dis. 2009;15:482–485. doi: 10.3201/eid1503.081013.
    1. Wacharapluesadee S., Duengkae P., Rodpan A., Kaewpom T., Maneeorn P., Kanchanasaka B. Diversity of coronavirus in bats from Eastern Thailand. Virol. J. 2015;12:57. doi: 10.1186/s12985-015-0289-1.
    1. Woo P.C.Y., Lau S.K.P., Li K.S.M., Poon R.W.S., Wong B.H.L., Tsoi H. Molecular diversity of coronaviruses in bats. Virology. 2006;351:180–187. doi: 10.1016/j.virol.2006.02.041.
    1. Yang Y., Du L., Liu C., Wang L., Ma C., Tang J. Receptor usage and cell entry of bat coronavirus HKU4 provide insight into bat-to-human transmission of MERS coronavirus. Proc. Natl. Acad. Sci. USA. 2014;111:12516–12521. doi: 10.1073/pnas.1405889111.

Source: PubMed

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