Evolutionary Relationships of Ljungan Virus Variants Circulating in Multi-Host Systems across Europe

The picornavirus named 'Ljungan virus' (LV, species Parechovirus B) has been detected in a dozen small mammal species from across Europe, but detailed information on its genetic diversity and host specificity is lacking. Here, we analyze the evolutionary relationships of LV variants circul...

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Published in:Viruses
Main Authors: Rossi, Chiara, Zadra, Nicola, Fevola, Cristina, Ecke, Frauke, Hornfeldt, Birger, Kallies, Rene, Kazimirova, Maria, Magnusson, Magnus, Olsson, Gert E., Ulrich, Rainer G., Jaaskelainen, Anne J., Henttonen, Heikki, Hauffe, Heidi C.
Other Authors: Department of Virology, Faculty of Medicine, University of Helsinki
Format: Article in Journal/Newspaper
Language:English
Published: MDPI 2021
Subjects:
Picornaviridae
Parechovirus B
Ljungan virus isolates
small mammals
rodent-borne virus
zoonosis
bank vole
VOLES MYODES-GLAREOLUS
HUMAN PARECHOVIRUSES
LYMPHOCYTIC CHORIOMENINGITIS
MOLECULAR CHARACTERIZATION
MAXIMUM-LIKELIHOOD
SEROLOGICAL SURVEY
MITOCHONDRIAL-DNA
CLINICAL-SAMPLES
PUUMALA VIRUSES
PUBLIC-HEALTH
3111 Biomedicine
11832 Microbiology and virology
Microtus arvalis
Online Access:http://hdl.handle.net/10138/334316
id ftunivhelsihelda:oai:helda.helsinki.fi:10138/334316
record_format openpolar
institution Open Polar
collection HELDA – University of Helsinki Open Repository
op_collection_id ftunivhelsihelda
language English
topic Picornaviridae
Parechovirus B
Ljungan virus isolates
small mammals
rodent-borne virus
zoonosis
bank vole
VOLES MYODES-GLAREOLUS
HUMAN PARECHOVIRUSES
LYMPHOCYTIC CHORIOMENINGITIS
MOLECULAR CHARACTERIZATION
MAXIMUM-LIKELIHOOD
SEROLOGICAL SURVEY
MITOCHONDRIAL-DNA
CLINICAL-SAMPLES
PUUMALA VIRUSES
PUBLIC-HEALTH
3111 Biomedicine
11832 Microbiology and virology
spellingShingle Picornaviridae
Parechovirus B
Ljungan virus isolates
small mammals
rodent-borne virus
zoonosis
bank vole
VOLES MYODES-GLAREOLUS
HUMAN PARECHOVIRUSES
LYMPHOCYTIC CHORIOMENINGITIS
MOLECULAR CHARACTERIZATION
MAXIMUM-LIKELIHOOD
SEROLOGICAL SURVEY
MITOCHONDRIAL-DNA
CLINICAL-SAMPLES
PUUMALA VIRUSES
PUBLIC-HEALTH
3111 Biomedicine
11832 Microbiology and virology
Rossi, Chiara
Zadra, Nicola
Fevola, Cristina
Ecke, Frauke
Hornfeldt, Birger
Kallies, Rene
Kazimirova, Maria
Magnusson, Magnus
Olsson, Gert E.
Ulrich, Rainer G.
Jaaskelainen, Anne J.
Henttonen, Heikki
Hauffe, Heidi C.
Evolutionary Relationships of Ljungan Virus Variants Circulating in Multi-Host Systems across Europe
topic_facet Picornaviridae
Parechovirus B
Ljungan virus isolates
small mammals
rodent-borne virus
zoonosis
bank vole
VOLES MYODES-GLAREOLUS
HUMAN PARECHOVIRUSES
LYMPHOCYTIC CHORIOMENINGITIS
MOLECULAR CHARACTERIZATION
MAXIMUM-LIKELIHOOD
SEROLOGICAL SURVEY
MITOCHONDRIAL-DNA
CLINICAL-SAMPLES
PUUMALA VIRUSES
PUBLIC-HEALTH
3111 Biomedicine
11832 Microbiology and virology
description The picornavirus named 'Ljungan virus' (LV, species Parechovirus B) has been detected in a dozen small mammal species from across Europe, but detailed information on its genetic diversity and host specificity is lacking. Here, we analyze the evolutionary relationships of LV variants circulating in free-living mammal populations by comparing the phylogenetics of the VP1 region (encoding the capsid protein and associated with LV serotype) and the 3D(pol) region (encoding the RNA polymerase) from 24 LV RNA-positive animals and a fragment of the 5 ' untranslated region (UTR) sequence (used for defining strains) in sympatric small mammals. We define three new VP1 genotypes: two in bank voles (Myodes glareolus) (genotype 8 from Finland, Sweden, France, and Italy, and genotype 9 from France and Italy) and one in field voles (Microtus arvalis) (genotype 7 from Finland). There are several other indications that LV variants are host-specific, at least in parts of their range. Our results suggest that LV evolution is rapid, ongoing and affected by genetic drift, purifying selection, spillover and host evolutionary history. Although recent studies suggest that LV does not have zoonotic potential, its widespread geographical and host distribution in natural populations of well-characterized small mammals could make it useful as a model for studying RNA virus evolution and transmission. Peer reviewed
author2 Department of Virology
Faculty of Medicine
University of Helsinki
format Article in Journal/Newspaper
author Rossi, Chiara
Zadra, Nicola
Fevola, Cristina
Ecke, Frauke
Hornfeldt, Birger
Kallies, Rene
Kazimirova, Maria
Magnusson, Magnus
Olsson, Gert E.
Ulrich, Rainer G.
Jaaskelainen, Anne J.
Henttonen, Heikki
Hauffe, Heidi C.
author_facet Rossi, Chiara
Zadra, Nicola
Fevola, Cristina
Ecke, Frauke
Hornfeldt, Birger
Kallies, Rene
Kazimirova, Maria
Magnusson, Magnus
Olsson, Gert E.
Ulrich, Rainer G.
Jaaskelainen, Anne J.
Henttonen, Heikki
Hauffe, Heidi C.
author_sort Rossi, Chiara
title Evolutionary Relationships of Ljungan Virus Variants Circulating in Multi-Host Systems across Europe
title_short Evolutionary Relationships of Ljungan Virus Variants Circulating in Multi-Host Systems across Europe
title_full Evolutionary Relationships of Ljungan Virus Variants Circulating in Multi-Host Systems across Europe
title_fullStr Evolutionary Relationships of Ljungan Virus Variants Circulating in Multi-Host Systems across Europe
title_full_unstemmed Evolutionary Relationships of Ljungan Virus Variants Circulating in Multi-Host Systems across Europe
title_sort evolutionary relationships of ljungan virus variants circulating in multi-host systems across europe
publisher MDPI
publishDate 2021
url http://hdl.handle.net/10138/334316
genre Microtus arvalis
genre_facet Microtus arvalis
op_relation 10.3390/v13071317
Laboratory work was funded by the European Union grant FP7?261504 EDENext?Biology and control of vector-borne infections in Europe to A.R., H.H., R.G.U., and H.C.H., by Sigrid Jus?lius Foundation to C.F., and the Fondazione E. Mach to C.R., C.F., H.C.H. Sample collection in Sweden was financed by grants from the Swedish Environmental Protection Agency (by the National Environmental Monitoring Programme for small rodents and Alvins fond) to B.H.; the Stiftelsen Oscar och Lili Lamms minne to B.H. and F.E.; VINNOVA?Swedish Governmental Agency .? for Innovation Systems (Verket Fo Innovations system) (P32060?1) to F.E.; the Swedish Research Council Formas (221-2012-1562) to F.E., B.H., and G.E.O.; the National Environmental and Wildlife Monitoring and Assessment program (FoMA, www.slu.se/en/environment) to G.E.O.; and the Helge Ax:son Johnsons Stiftelse to M.M. The collection of rodents in Germany was commissioned and funded by the Federal Environment Agency (UBA) within the Environment Research Plan of the German Federal Ministry for the Environment, Nature Conservation and Nuclear Safety (BMU). Acknowledgments: We thank Elena Buzan, Nathalie Charbonnel, Nicola Ferrari, Miriam Maas, Jaroslav Pi?lek, Claudia Romeo and Michal Stanko for providing samples. We also thank Roberto Celva for help with the Figure 1.
Rossi , C , Zadra , N , Fevola , C , Ecke , F , Hornfeldt , B , Kallies , R , Kazimirova , M , Magnusson , M , Olsson , G E , Ulrich , R G , Jaaskelainen , A J , Henttonen , H & Hauffe , H C 2021 , ' Evolutionary Relationships of Ljungan Virus Variants Circulating in Multi-Host Systems across Europe ' , Viruses (Basel) , vol. 13 , no. 7 , 1317 . https://doi.org/10.3390/v13071317
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http://hdl.handle.net/10138/334316
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container_title Viruses
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spelling ftunivhelsihelda:oai:helda.helsinki.fi:10138/334316 2024-01-07T09:44:49+01:00 Evolutionary Relationships of Ljungan Virus Variants Circulating in Multi-Host Systems across Europe Rossi, Chiara Zadra, Nicola Fevola, Cristina Ecke, Frauke Hornfeldt, Birger Kallies, Rene Kazimirova, Maria Magnusson, Magnus Olsson, Gert E. Ulrich, Rainer G. Jaaskelainen, Anne J. Henttonen, Heikki Hauffe, Heidi C. Department of Virology Faculty of Medicine University of Helsinki 2021-09-13T12:05:01Z 18 application/pdf http://hdl.handle.net/10138/334316 eng eng MDPI 10.3390/v13071317 Laboratory work was funded by the European Union grant FP7?261504 EDENext?Biology and control of vector-borne infections in Europe to A.R., H.H., R.G.U., and H.C.H., by Sigrid Jus?lius Foundation to C.F., and the Fondazione E. Mach to C.R., C.F., H.C.H. Sample collection in Sweden was financed by grants from the Swedish Environmental Protection Agency (by the National Environmental Monitoring Programme for small rodents and Alvins fond) to B.H.; the Stiftelsen Oscar och Lili Lamms minne to B.H. and F.E.; VINNOVA?Swedish Governmental Agency .? for Innovation Systems (Verket Fo Innovations system) (P32060?1) to F.E.; the Swedish Research Council Formas (221-2012-1562) to F.E., B.H., and G.E.O.; the National Environmental and Wildlife Monitoring and Assessment program (FoMA, www.slu.se/en/environment) to G.E.O.; and the Helge Ax:son Johnsons Stiftelse to M.M. The collection of rodents in Germany was commissioned and funded by the Federal Environment Agency (UBA) within the Environment Research Plan of the German Federal Ministry for the Environment, Nature Conservation and Nuclear Safety (BMU). Acknowledgments: We thank Elena Buzan, Nathalie Charbonnel, Nicola Ferrari, Miriam Maas, Jaroslav Pi?lek, Claudia Romeo and Michal Stanko for providing samples. We also thank Roberto Celva for help with the Figure 1. Rossi , C , Zadra , N , Fevola , C , Ecke , F , Hornfeldt , B , Kallies , R , Kazimirova , M , Magnusson , M , Olsson , G E , Ulrich , R G , Jaaskelainen , A J , Henttonen , H & Hauffe , H C 2021 , ' Evolutionary Relationships of Ljungan Virus Variants Circulating in Multi-Host Systems across Europe ' , Viruses (Basel) , vol. 13 , no. 7 , 1317 . https://doi.org/10.3390/v13071317 2a717831-e77a-4632-8940-0abace487298 http://hdl.handle.net/10138/334316 000677027800001 cc_by openAccess info:eu-repo/semantics/openAccess Picornaviridae Parechovirus B Ljungan virus isolates small mammals rodent-borne virus zoonosis bank vole VOLES MYODES-GLAREOLUS HUMAN PARECHOVIRUSES LYMPHOCYTIC CHORIOMENINGITIS MOLECULAR CHARACTERIZATION MAXIMUM-LIKELIHOOD SEROLOGICAL SURVEY MITOCHONDRIAL-DNA CLINICAL-SAMPLES PUUMALA VIRUSES PUBLIC-HEALTH 3111 Biomedicine 11832 Microbiology and virology Article publishedVersion 2021 ftunivhelsihelda 2023-12-14T00:06:20Z The picornavirus named 'Ljungan virus' (LV, species Parechovirus B) has been detected in a dozen small mammal species from across Europe, but detailed information on its genetic diversity and host specificity is lacking. Here, we analyze the evolutionary relationships of LV variants circulating in free-living mammal populations by comparing the phylogenetics of the VP1 region (encoding the capsid protein and associated with LV serotype) and the 3D(pol) region (encoding the RNA polymerase) from 24 LV RNA-positive animals and a fragment of the 5 ' untranslated region (UTR) sequence (used for defining strains) in sympatric small mammals. We define three new VP1 genotypes: two in bank voles (Myodes glareolus) (genotype 8 from Finland, Sweden, France, and Italy, and genotype 9 from France and Italy) and one in field voles (Microtus arvalis) (genotype 7 from Finland). There are several other indications that LV variants are host-specific, at least in parts of their range. Our results suggest that LV evolution is rapid, ongoing and affected by genetic drift, purifying selection, spillover and host evolutionary history. Although recent studies suggest that LV does not have zoonotic potential, its widespread geographical and host distribution in natural populations of well-characterized small mammals could make it useful as a model for studying RNA virus evolution and transmission. Peer reviewed Article in Journal/Newspaper Microtus arvalis HELDA – University of Helsinki Open Repository Viruses 13 7 1317

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