{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,29]],"date-time":"2026-06-29T22:40:59Z","timestamp":1782772859611,"version":"3.54.5"},"reference-count":49,"publisher":"Oxford University Press (OUP)","issue":"2","license":[{"start":{"date-parts":[[2023,7,28]],"date-time":"2023-07-28T00:00:00Z","timestamp":1690502400000},"content-version":"vor","delay-in-days":27,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"German Federal Ministry of Food and Agriculture","award":["01KI2111 2819114019"],"award-info":[{"award-number":["01KI2111 2819114019"]}]},{"name":"German Federal Ministry of Food and Agriculture","award":["01KI2111 2819114019"],"award-info":[{"award-number":["01KI2111 2819114019"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2023,9,20]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>Rustrela virus (RusV; species Rubivirus strelense, family Matonaviridae) was discovered in different zoo animal species affected by fatal encephalitis. Simultaneous RusV RNA detection in multiple yellow-necked field mice (Apodemus flavicollis) suggested this rodent as a reservoir of RusV. Here, we investigated 1,264 yellow-necked field mice and sympatric other small mammals from different regions in Germany for RusV RNA using an optimized reverse transcription-quantitative polymerase chain reaction (RT-qPCR) protocol and high-throughput sequencing. The investigation resulted in the detection of RusV RNA exclusively in 50 of 396 (12.6\u2009per cent) yellow-necked field mice but absence in other sympatric species. RT-qPCR-determined tissue distribution of RusV RNA revealed the highest viral loads in the central nervous system, with other tissues being only very rarely affected. The histopathological evaluation did not reveal any hints of encephalitis in the brains of infected animals despite the detection of viral RNA in neurons by in situ hybridization (ISH). The positive association between the body mass of yellow-necked field mice and RusV RNA detection suggests a persistent infection. Phylogenetic analysis of partial E1 and full-genome sequences showed a high diversification with at least four RusV lineages (1A\u20131D) in northeastern Germany. Moreover, phylogenetic and isolation-by-distance analyses indicated evolutionary processes of RusV mostly in local reservoir populations. A comparison of complete genome sequences from all detected RusV lineages demonstrated a high level of amino acid and nucleotide sequence variability within a part of the p150 peptide of the non-structural polyprotein and its coding sequence, respectively. The location of this region within the RusV genome and its genetic properties were comparable to the hypervariable region of the rubella virus. The broad range of detected RusV spillover hosts in combination with its geographical distribution in northeastern Germany requires the assessment of its zoonotic potential and further analysis of encephalitis cases in mammals. Future studies have to prove a putative co-evolution scenario for RusV in the yellow-necked field mouse reservoir.<\/jats:p>","DOI":"10.1093\/ve\/vead048","type":"journal-article","created":{"date-parts":[[2023,7,28]],"date-time":"2023-07-28T17:38:51Z","timestamp":1690565931000},"source":"Crossref","is-referenced-by-count":11,"title":["Continuous presence of\u00a0genetically diverse rustrela virus lineages in\u00a0yellow-necked field mouse reservoir populations in\u00a0northeastern Germany"],"prefix":"10.1093","volume":"9","author":[{"given":"Sina","family":"Nippert","sequence":"first","affiliation":[{"name":"Institute of Novel and Emerging Infectious Diseases, Friedrich-Loeffler-Institut, Federal Research Institute for Animal Health , S\u00fcdufer 10, Greifswald-Insel Riems 17493, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8209-6274","authenticated-orcid":false,"given":"Dennis","family":"Rubbenstroth","sequence":"additional","affiliation":[{"name":"Institute of Novel and Emerging Infectious Diseases, Friedrich-Loeffler-Institut, Federal Research Institute for Animal Health , S\u00fcdufer 10, Greifswald-Insel Riems 17493, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jessica Anna","family":"Geers","sequence":"additional","affiliation":[{"name":"Institute of Diagnostic Virology, Friedrich-Loeffler-Institut, Federal Research Institute for Animal Health , S\u00fcdufer 10, Greifswald-Insel Riems 17493, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8451-5719","authenticated-orcid":false,"given":"Arnt","family":"Ebinger","sequence":"additional","affiliation":[{"name":"Institute of Diagnostic Virology, Friedrich-Loeffler-Institut, Federal Research Institute for Animal Health , S\u00fcdufer 10, Greifswald-Insel Riems 17493, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4552-031X","authenticated-orcid":false,"given":"Donata","family":"Hoffmann","sequence":"additional","affiliation":[{"name":"Institute of Diagnostic Virology, Friedrich-Loeffler-Institut, Federal Research Institute for Animal Health , S\u00fcdufer 10, Greifswald-Insel Riems 17493, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6373-5923","authenticated-orcid":false,"given":"Angele","family":"Breithaupt","sequence":"additional","affiliation":[{"name":"Department of Experimental Animal Facilities and Biorisk Management, Friedrich-Loeffler-Institut, Federal Research Institute for Animal Health , S\u00fcdufer 10, Greifswald-Insel Riems 17493, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0436-4480","authenticated-orcid":false,"given":"Claudia","family":"Wylezich","sequence":"additional","affiliation":[{"name":"Institute of Diagnostic Virology, Friedrich-Loeffler-Institut, Federal Research Institute for Animal Health , S\u00fcdufer 10, Greifswald-Insel Riems 17493, Germany"},{"name":"Department of Experimental Animal Facilities and Biorisk Management, Friedrich-Loeffler-Institut, Federal Research Institute for Animal Health , S\u00fcdufer 10, Greifswald-Insel Riems 17493, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1258-8214","authenticated-orcid":false,"given":"Xuejing","family":"Wang","sequence":"additional","affiliation":[{"name":"Institute of Ecology and Evolution, University of Bern , Baltzerstra\u00dfe 6, Bern CH-3012, Switzerland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0007-7595-8239","authenticated-orcid":false,"given":"Viola C","family":"Haring","sequence":"additional","affiliation":[{"name":"Institute of Novel and Emerging Infectious Diseases, Friedrich-Loeffler-Institut, Federal Research Institute for Animal Health , S\u00fcdufer 10, Greifswald-Insel Riems 17493, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9882-8292","authenticated-orcid":false,"given":"Philip","family":"Starcky","sequence":"additional","affiliation":[{"name":"Institute of Diagnostic Virology, Friedrich-Loeffler-Institut, Federal Research Institute for Animal Health , S\u00fcdufer 10, Greifswald-Insel Riems 17493, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6946-8467","authenticated-orcid":false,"given":"Paola","family":"Fruci","sequence":"additional","affiliation":[{"name":"Institute of Diagnostic Virology, Friedrich-Loeffler-Institut, Federal Research Institute for Animal Health , S\u00fcdufer 10, Greifswald-Insel Riems 17493, Germany"},{"name":"Laboratory of Infectious Diseases, Faculty of Veterinary Medicine, University of Teramo , Via Renato Balzarini 1, Teramo 64100, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Christoph","family":"Langner","sequence":"additional","affiliation":[{"name":"Stralsund Zoological Garden , Gr\u00fcnhufer Bogen 2, Stralsund 18437, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Christin","family":"Trapp","sequence":"additional","affiliation":[{"name":"Tierpark Grimmen , Friedrichstra\u00dfe 20, Grimmen 18507, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Heiko","family":"Schulz","sequence":"additional","affiliation":[{"name":"Betriebsteil Forstplanung\/Versuchswesen\/Informationssysteme, Landesforst Mecklenburg-Vorpommern\u2014Anstalt des \u00f6ffentlichen Rechts , Zeppelinstra\u00dfe 3, Schwerin 19061, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wilko","family":"Stubbe","sequence":"additional","affiliation":[{"name":"Institut f\u00fcr Allgemeine und Systematische Zoologie, Universit\u00e4t Greifswald , Loitzer Stra\u00dfe 26, Greifswald 17489, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7504-9509","authenticated-orcid":false,"given":"Christian","family":"Imholt","sequence":"additional","affiliation":[{"name":"Rodent Research, Institute for Epidemiology and Pathogen Diagnostics, Julius K\u00fchn-Institute (JKI), Federal Research Centre for Cultivated Plants , Toppheideweg 88, M\u00fcnster 48161, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0162-323X","authenticated-orcid":false,"given":"Gerald","family":"Heckel","sequence":"additional","affiliation":[{"name":"Institute of Ecology and Evolution, University of Bern , Baltzerstra\u00dfe 6, Bern CH-3012, Switzerland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0598-5254","authenticated-orcid":false,"given":"Martin","family":"Beer","sequence":"additional","affiliation":[{"name":"Institute of Diagnostic Virology, Friedrich-Loeffler-Institut, Federal Research Institute for Animal Health , S\u00fcdufer 10, Greifswald-Insel Riems 17493, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0178-6183","authenticated-orcid":false,"given":"Florian","family":"Pfaff","sequence":"additional","affiliation":[{"name":"Institute of Diagnostic Virology, Friedrich-Loeffler-Institut, Federal Research Institute for Animal Health , S\u00fcdufer 10, Greifswald-Insel Riems 17493, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5620-1528","authenticated-orcid":false,"given":"Rainer G","family":"Ulrich","sequence":"additional","affiliation":[{"name":"Partner Site Hamburg-L\u00fcbeck-Borstel-Riems, German Center for Infection Research (DZIF) , Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2023,7,28]]},"reference":[{"key":"2023092216594231500_R1","doi-asserted-by":"crossref","DOI":"10.1186\/1743-422X-10-32","article-title":"Analysis of\u00a0Whole Genome Sequences of\u00a016 Strains of\u00a0Rubella Virus from the United States, 1961\u20132009","volume":"10","author":"Abernathy","year":"2013","journal-title":"Virology Journal"},{"key":"2023092216594231500_R2","doi-asserted-by":"crossref","first-page":"353","DOI":"10.4098\/AT.arch.73-23","article-title":"Growth, Variations and\u00a0Age Criteria in\u00a0Apodemus agrarius (Pallas, 1771)","volume":"18","author":"Adamczewska-Andrzejewska","year":"1973","journal-title":"Acta Theriologica"},{"key":"2023092216594231500_R3","doi-asserted-by":"crossref","first-page":"54","DOI":"10.1080\/13921657.2004.10512592","article-title":"Sex- and\u00a0Age Related Differences in\u00a0Tooth Row Length of\u00a0Small Mammals: Mice","volume":"14","author":"Bal\u010diauskien\u0117","year":"2004","journal-title":"Acta Zoologica Lituanica"},{"key":"2023092216594231500_R4","doi-asserted-by":"crossref","first-page":"455","DOI":"10.1089\/cmb.2012.0021","article-title":"SPAdes: A New Genome Assembly Algorithm and\u00a0Its Applications to Single-Cell Sequencing","volume":"19","author":"Bankevich","year":"2012","journal-title":"Journal of Computational Biology"},{"key":"2023092216594231500_R5","doi-asserted-by":"crossref","DOI":"10.1038\/s41586-020-2897-1","article-title":"Author Correction: Relatives of\u00a0Rubella Virus in\u00a0Diverse Mammals","volume":"588","author":"Bennett","year":"2020","journal-title":"Nature"},{"key":"2023092216594231500_R36","doi-asserted-by":"crossref","first-page":"424","DOI":"10.1038\/s41586-020-2812-9","article-title":"Relatives of\u00a0Rubella Virus in\u00a0Diverse Mammals","volume":"586","year":"2020","journal-title":"Nature"},{"key":"2023092216594231500_R6","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1038\/nmeth.3176","article-title":"Fast and\u00a0Sensitive Protein Alignment Using DIAMOND","volume":"12","author":"Buchfink","year":"2015","journal-title":"Nature Methods"},{"key":"2023092216594231500_R7","first-page":"1","volume-title":"Molecular and Cellular Endocrinology","author":"Carmichael","year":"1997"},{"key":"2023092216594231500_R8","article-title":"Create a New Family Matonaviridae to Include the Genus Rubivirus, Removed from the Family Togaviridae","author":"Chen","year":"2018"},{"key":"2023092216594231500_R9","doi-asserted-by":"crossref","first-page":"8171","DOI":"10.1002\/ece3.4291","article-title":"Regional and\u00a0Local Patterns of\u00a0Genetic Variation and\u00a0Structure in\u00a0Yellow-Necked Mice \u2013 The Roles of\u00a0Geographic Distance, Population Abundance, and\u00a0Winter Severity","volume":"8","author":"Czarnomska","year":"2018","journal-title":"Ecology and Evolution"},{"key":"2023092216594231500_R10","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1128\/JVI.02294-20","article-title":"The Enigmatic Capsid Protein of\u00a0an Encephalitic Rubivirus","volume":"95","author":"Das","year":"2021","journal-title":"Journal of Virology"},{"key":"2023092216594231500_R11","doi-asserted-by":"crossref","first-page":"1042","DOI":"10.3201\/eid2905.230172","article-title":"Rustrela Virus as Putative Cause of\u00a0Nonsuppurative Meningoencephalitis in\u00a0Lions","volume":"29","author":"de Le Roi","year":"2023","journal-title":"Emerging Infectious Diseases"},{"key":"2023092216594231500_R12","doi-asserted-by":"crossref","first-page":"83","DOI":"10.3201\/eid2301.160224","article-title":"Host-Associated Absence of\u00a0Human Puumala Virus Infections in\u00a0Northern and\u00a0Eastern Germany","volume":"23","author":"Drewes","year":"2017","journal-title":"Emerging Infectious Diseases"},{"key":"2023092216594231500_R13","doi-asserted-by":"crossref","DOI":"10.1186\/1471-2105-5-113","article-title":"MUSCLE: A Multiple Sequence Alignment Method with Reduced Time and\u00a0Space Complexity","volume":"5","author":"Edgar","year":"2004","journal-title":"BMC Bioinformatics"},{"key":"2023092216594231500_R14","article-title":"Virome Composition in\u00a0Marine Fish Revealed by Meta-Transcriptomics","volume":"7","author":"Geoghegan","year":"2021","journal-title":"Virus Evolution"},{"key":"2023092216594231500_R15","doi-asserted-by":"crossref","first-page":"109","DOI":"10.4098\/j.at.0001-7051.102.2009","article-title":"Landscape Pattern and\u00a0Genetic Structure of\u00a0a Yellow-Necked Mouse Apodemus flavicollis Population in\u00a0North-Eastern Poland","volume":"55","author":"Gortat","year":"2010","journal-title":"Acta Theriologica"},{"key":"2023092216594231500_R16","doi-asserted-by":"crossref","DOI":"10.3390\/v13040585","article-title":"A Novel Rubi-Like Virus in\u00a0the Pacific Electric Ray (Tetronarce californica) Reveals the Complex Evolutionary History of\u00a0the Matonaviridae","volume":"13","author":"Grimwood","year":"2021","journal-title":"Viruses"},{"key":"2023092216594231500_R17","doi-asserted-by":"crossref","first-page":"200","DOI":"10.1016\/j.jviromet.2006.05.020","article-title":"A Universal Heterologous Internal Control System for\u00a0Duplex Real-Time RT-PCR Assays Used in\u00a0a Detection System for\u00a0Pestiviruses","volume":"136","author":"Hoffmann","year":"2006","journal-title":"Journal of Virological Methods"},{"key":"2023092216594231500_R18","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1016\/S0168-1702(03)00180-1","article-title":"Phylogenetic Analysis of\u00a0Rubella Virus Including New Genotype I Isolates","volume":"96","author":"Hofmann","year":"2003","journal-title":"Virus Research"},{"key":"2023092216594231500_R19","doi-asserted-by":"crossref","DOI":"10.1017\/S0950268821000443","article-title":"Hantavirus\u2013Leptospira Coinfections in\u00a0Small Mammals from Central Germany","volume":"149","author":"Jeske","year":"2021","journal-title":"Epidemiology and Infection"},{"key":"2023092216594231500_R20","doi-asserted-by":"crossref","first-page":"772","DOI":"10.1093\/molbev\/mst010","article-title":"MAFFT Multiple Sequence Alignment Software Version 7: Improvements in\u00a0Performance and\u00a0Usability","volume":"30","author":"Katoh","year":"2013","journal-title":"Molecular Biology and Evolution"},{"key":"2023092216594231500_R21","volume-title":"Fields Virology: Rubella Virus","author":"Knipe","year":"2007","edition":"5th edn"},{"key":"2023092216594231500_R22","doi-asserted-by":"crossref","DOI":"10.1099\/jgv.0.001817","article-title":"ICTV Virus Taxonomy Profile: Matonaviridae 2022","volume":"103","author":"Mankertz","year":"2022","journal-title":"Journal of General Virology"},{"key":"2023092216594231500_R23","doi-asserted-by":"crossref","first-page":"W327","DOI":"10.1093\/nar\/gkh454","article-title":"CD-Search: Protein Domain Annotations on\u00a0the Fly","volume":"32","author":"Marchler-Bauer","year":"2004","journal-title":"Nucleic Acids Research"},{"key":"2023092216594231500_R24","doi-asserted-by":"crossref","DOI":"10.1093\/ve\/veaa087","article-title":"RDP5: A Computer Program for\u00a0Analyzing Recombination In, and\u00a0Removing Signals of\u00a0Recombination From, Nucleotide Sequence Datasets","volume":"7","author":"Martin","year":"2021","journal-title":"Virus Evolution"},{"key":"2023092216594231500_R25","doi-asserted-by":"crossref","DOI":"10.1038\/s41467-023-36204-w","article-title":"Mystery of\u00a0Fatal \u2018Staggering Disease\u2019 Unravelled: Novel Rustrela Virus Causes Severe Meningoencephalomyelitis in\u00a0Domestic Cats","volume":"14","author":"Matiasek","year":"2023","journal-title":"Nature Communications"},{"key":"2023092216594231500_R26","doi-asserted-by":"crossref","first-page":"788","DOI":"10.1016\/j.ympev.2004.02.018","article-title":"Phylogeographic History of\u00a0the Yellow-Necked Fieldmouse (Apodemus flavicollis) in\u00a0Europe and\u00a0in the near and\u00a0Middle East","volume":"32","author":"Michaux","year":"2004","journal-title":"Molecular Phylogenetics and Evolution"},{"key":"2023092216594231500_R27","doi-asserted-by":"crossref","first-page":"1188","DOI":"10.1093\/molbev\/mst024","article-title":"Ultrafast Approximation for\u00a0Phylogenetic Bootstrap","volume":"30","author":"Minh","year":"2013","journal-title":"Molecular Biology and Evolution"},{"key":"2023092216594231500_R28","article-title":"Studies on\u00a0the Ecology of\u00a0Two Sympatric Species of\u00a0Apodemus (Rodentia: Muridae)","author":"Montgomery","year":"1977"},{"key":"2023092216594231500_R29","doi-asserted-by":"crossref","first-page":"268","DOI":"10.1093\/molbev\/msu300","article-title":"IQ-TREE: A Fast and\u00a0Effective Stochastic Algorithm for\u00a0Estimating Maximum-Likelihood Phylogenies","volume":"32","author":"Nguyen","year":"2015","journal-title":"Molecular Biology and Evolution"},{"key":"2023092216594231500_R30","doi-asserted-by":"crossref","first-page":"354","DOI":"10.1128\/jvi.51.2.354-358.1984","article-title":"The Gene Order for\u00a0Rubella Virus Structural Proteins Is NH2-C-E2-E1-COOH","volume":"51","author":"Oker-Blom","year":"1984","journal-title":"Journal of Virology"},{"key":"2023092216594231500_R31","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1128\/jvi.49.2.403-408.1984","article-title":"Rubella Virus 40S Genome RNA Specifies a 24S Subgenomic mRNA that Codes for\u00a0a Precursor to Structural Proteins","volume":"49","author":"Oker-Blom","year":"1984","journal-title":"Journal of Virology"},{"key":"2023092216594231500_R32","doi-asserted-by":"crossref","first-page":"3047","DOI":"10.1099\/0022-1317-71-12-3047","article-title":"Translocation and\u00a0Cleavage of\u00a0Rubella Virus Envelope Glycoproteins: Identification and\u00a0Role of\u00a0the E2 Signal Sequence","volume":"71","author":"Oker-Blom","year":"1990","journal-title":"Journal of General Virology"},{"key":"2023092216594231500_R33","doi-asserted-by":"crossref","DOI":"10.1128\/spectrum.00103-22","article-title":"Revisiting Rustrela Virus: New Cases of\u00a0Encephalitis and\u00a0a Solution to the Capsid 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