{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,11,4]],"date-time":"2025-11-04T10:55:58Z","timestamp":1762253758736,"version":"build-2065373602"},"reference-count":38,"publisher":"MDPI AG","issue":"4","license":[{"start":{"date-parts":[[2021,4,7]],"date-time":"2021-04-07T00:00:00Z","timestamp":1617753600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Friedrich-Loeffler-Institut","award":["Rie-0373"],"award-info":[{"award-number":["Rie-0373"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Viruses"],"abstract":"<jats:p>European bat lyssavirus type 1 (EBLV-1) is the causative agent for almost all reported rabies cases found in European bats. In recent years, increasing numbers of available EBLV-1 full genomes and their phylogenetic analyses helped to further elucidate the distribution and genetic characteristics of EBLV-1 and its two subtypes, namely EBLV-1a and EBLV-1b. Nonetheless, the absence of full-genome sequences from regions with known detections of EBLV-1 still limit the understanding of the phylogeographic relations between viruses from different European regions. In this study, a set of 21 archived Danish EBLV-1 samples from the years 1985 to 2009 was processed for the acquisition of full-genome sequences using a high-throughput sequencing approach. Subsequent phylogenetic analysis encompassing all available EBLV-1 full genomes from databases revealed the Danish sequences belong to the EBLV-1a subtype and further highlighted the distinct, close phylogenetic relationship of Danish, Dutch and German isolates in this region. In addition, the formation of five putative groups nearly exclusively formed by Danish isolates and the overall increased resolution of the EBLV-1a branch indicate a higher genetic diversity and spatial segregation for this sublineage than was previously known. These results emphasize the importance of phylogenetic analyses of full-genome sequences of lyssaviruses for genetic geography.<\/jats:p>","DOI":"10.3390\/v13040634","type":"journal-article","created":{"date-parts":[[2021,4,7]],"date-time":"2021-04-07T21:49:06Z","timestamp":1617832146000},"page":"634","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":8,"title":["Full-Genome Sequences and Phylogenetic Analysis of Archived Danish European Bat Lyssavirus 1 (EBLV-1) Emphasize a Higher Genetic Resolution and Spatial Segregation for Sublineage 1a"],"prefix":"10.3390","volume":"13","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-8511-9067","authenticated-orcid":false,"given":"Sten","family":"Calvelage","sequence":"first","affiliation":[{"name":"Institute of Diagnostic Virology, Friedrich-Loeffler-Institut (FLI), 17493 Greifswald-Insel Riems, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1076-398X","authenticated-orcid":false,"given":"Conrad M.","family":"Freuling","sequence":"additional","affiliation":[{"name":"Central Duties, Friedrich-Loeffler-Institut (FLI), 17493 Greifswald-Insel Riems, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3243-6154","authenticated-orcid":false,"given":"Anthony R.","family":"Fooks","sequence":"additional","affiliation":[{"name":"Animal &amp; Plant Health Agency, WHO Collaborating Centre for Rabies Surveillance and Research, OIE Reference Laboratory for Rabies, Weybridge KT15 3NB, Surrey, UK"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8408-2274","authenticated-orcid":false,"given":"Dirk","family":"H\u00f6per","sequence":"additional","affiliation":[{"name":"Institute of Diagnostic Virology, Friedrich-Loeffler-Institut (FLI), 17493 Greifswald-Insel Riems, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9215-088X","authenticated-orcid":false,"given":"Denise A.","family":"Marston","sequence":"additional","affiliation":[{"name":"Animal &amp; Plant Health Agency, WHO Collaborating Centre for Rabies Surveillance and Research, OIE Reference Laboratory for Rabies, Weybridge KT15 3NB, Surrey, UK"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6022-348X","authenticated-orcid":false,"given":"Lorraine","family":"McElhinney","sequence":"additional","affiliation":[{"name":"Animal &amp; Plant Health Agency, WHO Collaborating Centre for Rabies Surveillance and Research, OIE Reference Laboratory for Rabies, Weybridge KT15 3NB, Surrey, UK"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Thomas Bruun","family":"Rasmussen","sequence":"additional","affiliation":[{"name":"Virus &amp; Mikrobiologisk Specialdiagnostik, Statens Serum Institut, 2300 Copenhagen, Denmark"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8716-2341","authenticated-orcid":false,"given":"Stefan","family":"Finke","sequence":"additional","affiliation":[{"name":"Institute of Molecular Virology and Cell Biology, Friedrich-Loeffler-Institut (FLI), WHO Collaborating Centre for Rabies Surveillance and Research, OIE Reference Laboratory for Rabies, 17493 Greifswald-Insel Riems, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Martin","family":"Beer","sequence":"additional","affiliation":[{"name":"Institute of Diagnostic Virology, Friedrich-Loeffler-Institut (FLI), 17493 Greifswald-Insel Riems, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0959-3653","authenticated-orcid":false,"given":"Thomas","family":"M\u00fcller","sequence":"additional","affiliation":[{"name":"Institute of Molecular Virology and Cell Biology, Friedrich-Loeffler-Institut (FLI), WHO Collaborating Centre for Rabies Surveillance and Research, OIE Reference Laboratory for Rabies, 17493 Greifswald-Insel Riems, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2021,4,7]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Banyard, A.C., Davis, A., Gilbert, A.T., and Markotter, W. (2020). Bat Rabies: Rabies\u2014Scientific Basis of the Disease and Its Management, Elsevier Academic Press. [4th ed.].","DOI":"10.1016\/B978-0-12-818705-0.00007-8"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"3023","DOI":"10.1007\/s00705-020-04731-2","article-title":"2020 taxonomic update for phylum Negarnaviricota (Riboviria: Orthornavirae), including the large orders Bunyavirales and Mononegavirales","volume":"165","author":"Kuhn","year":"2020","journal-title":"Arch. Virol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"1967","DOI":"10.1007\/s00705-019-04247-4","article-title":"Taxonomy of the order Mononegavirales: Update 2019","volume":"164","author":"Amarasinghe","year":"2019","journal-title":"Arch. Virol."},{"key":"ref_4","unstructured":"International Committee on Taxonomy of Viruses (2021, April 06). ICTV Report on Virus Classification and Taxon Nomenclatur, Genus: Lyssavirus. Available online: https:\/\/talk.ictvonline.org\/ictv-reports\/ictv_online_report\/negative-sense-rna-viruses\/w\/rhabdoviridae\/795\/genus-lyssavirus."},{"key":"ref_5","unstructured":"WHO Expert Consultation on Rabies (2018). WHO Expert Consultation on Rabies: Third Report, Bangkok, Thailand on 26\u201328 April 2017, WHO."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"676","DOI":"10.1126\/science.1188836","article-title":"Host phylogeny constrains cross-species emergence and establishment of rabies virus in bats","volume":"329","author":"Streicker","year":"2010","journal-title":"Science"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"68","DOI":"10.1016\/j.coviro.2017.11.007","article-title":"The lyssavirus host-specificity conundrum-rabies virus-the exception not the rule","volume":"28","author":"Marston","year":"2018","journal-title":"Curr. Opin. Virol."},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Shipley, R., Wright, E., Selden, D., Wu, G., Aegerter, J., Fooks, A.R., and Banyard, A.C. (2019). Bats and Viruses: Emergence of Novel Lyssaviruses and Association of Bats with Viral Zoonoses in the EU. Trop. Med. Infect. Dis., 4.","DOI":"10.3390\/tropicalmed4010031"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"2419","DOI":"10.1128\/jcm.30.9.2419-2426.1992","article-title":"Antigenic and molecular characterization of bat rabies virus in Europe","volume":"30","author":"Bourhy","year":"1992","journal-title":"J. Clin. Microbiol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"273","DOI":"10.1007\/s00705-006-0853-5","article-title":"Epidemiology of bat rabies in Germany","volume":"152","author":"Johnson","year":"2007","journal-title":"Arch. Virol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1111\/j.1439-0450.2003.00725.x","article-title":"Spill-over of European bat lyssavirus type 1 into a stone marten (Martes foina) in Germany","volume":"51","author":"Cox","year":"2004","journal-title":"J. Vet. Med. B Infect. Dis. Vet. Public Health"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"190","DOI":"10.1016\/j.jcpa.2005.10.005","article-title":"Natural and experimental infection of sheep with European bat lyssavirus type-1 of Danish bat origin","volume":"134","author":"Fooks","year":"2006","journal-title":"J. Comp. Pathol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"280","DOI":"10.3201\/eid1502.080637","article-title":"European bat Lyssavirus transmission among cats, Europe","volume":"15","author":"Dacheux","year":"2009","journal-title":"Emerg. Infect. Dis."},{"key":"ref_14","first-page":"273","article-title":"Bat rabies surveillance in the former Soviet Union","volume":"125","author":"Kuzmin","year":"2006","journal-title":"Dev. Biol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"3202","DOI":"10.1093\/gbe\/evx236","article-title":"Host Genetic Variation Does Not Determine Spatio-Temporal Patterns of European Bat 1 Lyssavirus","volume":"9","author":"Troupin","year":"2017","journal-title":"Genome Biol. Evol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"10487","DOI":"10.1128\/JVI.79.16.10487-10497.2005","article-title":"Phylogeography, population dynamics, and molecular evolution of European bat lyssaviruses","volume":"79","author":"Davis","year":"2005","journal-title":"J. Virol."},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Eggerbauer, E., Pfaff, F., Finke, S., H\u00f6per, D., Beer, M., Mettenleiter, T.C., Nolden, T., Teifke, J.-P., M\u00fcller, T., and Freuling, C.M. (2017). Comparative analysis of European bat lyssavirus 1 pathogenicity in the mouse model. PLoS Negl. Trop. Dis., 11.","DOI":"10.1371\/journal.pntd.0005668"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1302","DOI":"10.1099\/vir.0.82692-0","article-title":"Comparative analysis of the full genome sequence of European bat lyssavirus type 1 and type 2 with other lyssaviruses and evidence for a conserved transcription termination and polyadenylation motif in the G-L 3\u2032 non-translated region","volume":"88","author":"Marston","year":"2007","journal-title":"J. Gen. Virol."},{"key":"ref_19","unstructured":"Conraths, F.J., Freuling, C.M., Hoffmann, B., Selhorst, T., Kliemt, J., Schatz, J., and M\u00fcller, T. (2012). New insights into the genetics of EBLV-1 from Germany. Berl. Munch. Tierarztl. Wochenschr., 259\u2013263."},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"V\u00e1zquez-Moron, S. (2011). Phylogeny of European Bat Lyssavirus 1 in Eptesicus isabellinus Bats, Spain. Emerg. Infect. Dis.","DOI":"10.3201\/eid1703100894"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"2319","DOI":"10.1099\/0022-1317-78-9-2319","article-title":"Evolution of European bat lyssaviruses","volume":"78","author":"Amengual","year":"1997","journal-title":"J. Gen. Virol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1111\/zph.12003","article-title":"Molecular Epidemiology of Bat Lyssaviruses in Europe","volume":"60","author":"McElhinney","year":"2013","journal-title":"Zoonoses Public Health"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"379","DOI":"10.1016\/S0140-6736(87)91746-6","article-title":"Bat rabies in Denmark","volume":"329","author":"Grauballe","year":"1987","journal-title":"Lancet"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"22","DOI":"10.1111\/zph.12002","article-title":"Bat rabies surveillance in Europe","volume":"60","author":"Schatz","year":"2013","journal-title":"Zoonoses Public Health"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"799","DOI":"10.20506\/rst.31.3.2152","article-title":"The WHO Rabies Bulletin Europe: A key source of information on rabies and a pivotal tool for surveillance and epidemiology","volume":"31","author":"Freuling","year":"2012","journal-title":"Rev. Off. Int. Epizoot."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"13108","DOI":"10.1038\/s41598-018-31496-1","article-title":"A Versatile Sample Processing Workflow for Metagenomic Pathogen Detection","volume":"8","author":"Wylezich","year":"2018","journal-title":"Sci. Rep."},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Delmas, O., Holmes, E.C., Talbi, C., Larrous, F., Dacheux, L., Bouchier, C., and Bourhy, H. (2008). Genomic diversity and evolution of the lyssaviruses. PLoS ONE, 3.","DOI":"10.1371\/journal.pone.0002057"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"3059","DOI":"10.1093\/nar\/gkf436","article-title":"MAFFT: A novel method for rapid multiple sequence alignment based on fast Fourier transform","volume":"30","author":"Katoh","year":"2002","journal-title":"Nucleic Acids Res."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"268","DOI":"10.1093\/molbev\/msu300","article-title":"IQ-TREE: A fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies","volume":"32","author":"Nguyen","year":"2015","journal-title":"Mol. Biol. Evol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"518","DOI":"10.1093\/molbev\/msx281","article-title":"UFBoot2: Improving the Ultrafast Bootstrap Approximation","volume":"35","author":"Hoang","year":"2018","journal-title":"Mol. Biol. Evol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"587","DOI":"10.1038\/nmeth.4285","article-title":"ModelFinder: Fast model selection for accurate phylogenetic estimates","volume":"14","author":"Kalyaanamoorthy","year":"2017","journal-title":"Nat. Methods"},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Marston, D.A., McElhinney, L.M., Ellis, R.J., Horton, D.L., Wise, E.L., Leech, S.L., David, D., Lamballerie, X., and de Fooks, A.R. (2013). Next generation sequencing of viral RNA genomes. BMC Genom., 14.","DOI":"10.1186\/1471-2164-14-444"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"413","DOI":"10.3201\/eid0804.010263","article-title":"European bat lyssavirus infection in Spanish bat populations","volume":"8","author":"Amengual","year":"2002","journal-title":"Emerg. Infect. Dis."},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Picard-Meyer, E., Robardet, E., Arthur, L., Larcher, G., Harbusch, C., Servat, A., and Cliquet, F. (2014). Bat rabies in France: A 24-year retrospective epidemiological study. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0098622"},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Schatz, J., Freuling, C.M., Auer, E., Goharriz, H., Harbusch, C., Johnson, N., Kaipf, I., Mettenleiter, T.C., M\u00fchldorfer, K., and M\u00fchle, R.-U. (2014). Enhanced passive bat rabies surveillance in indigenous bat species from Germany-a retrospective study. PLoS Negl. Trop. Dis., 8.","DOI":"10.1371\/journal.pntd.0002835"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"35","DOI":"10.3161\/150811013X667849","article-title":"Population Genetics and Bat Rabies: A Case Study of Eptesicus serotinus in Poland","volume":"15","author":"Bogdanowicz","year":"2013","journal-title":"Acta Chiropt."},{"key":"ref_37","unstructured":"Hutterer, R., Ivanova, T., Meyer-Cords, C.H., and Rodrigues, L. (2005). Bat Migration in Europe: A Review of Banding Data and Literature, Federal Agency for Nature Conservation."},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"McElhinney, L.M., Marston, D.A., Wise, E.L., Freuling, C.M., Bourhy, H., Zanoni, R., Moldal, T., Kooi, E.A., Neubauer-Juric, A., and Nokireki, T. (2018). Molecular Epidemiology and Evolution of European Bat Lyssavirus 2. Int. J. Mol. Sci., 19.","DOI":"10.3390\/ijms19010156"}],"container-title":["Viruses"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1999-4915\/13\/4\/634\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,13]],"date-time":"2025-10-13T14:12:00Z","timestamp":1760364720000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1999-4915\/13\/4\/634"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,4,7]]},"references-count":38,"journal-issue":{"issue":"4","published-online":{"date-parts":[[2021,4]]}},"alternative-id":["v13040634"],"URL":"https:\/\/doi.org\/10.3390\/v13040634","relation":{},"ISSN":["1999-4915"],"issn-type":[{"type":"electronic","value":"1999-4915"}],"subject":[],"published":{"date-parts":[[2021,4,7]]}}}