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

Overview

Journal Viruses

Publisher MDPI

Specialty Microbiology

Date 2021 Aug 10

PMID 34372523

Citations 2

Authors

Chiara Rossi

Nicola Zadra

Cristina Fevola

Frauke Ecke

Birger Hornfeldt

Rene Kallies

Maria Kazimirova

Magnus Magnusson

Gert E Olsson

Rainer G Ulrich

Anne J Jaaskelainen

Heikki Henttonen

Heidi C Hauffe

Affiliations

Soon will be listed here.

Abstract

The picornavirus named 'Ljungan virus' (LV, species ) 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 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 () (genotype 8 from Finland, Sweden, France, and Italy, and genotype 9 from France and Italy) and one in field voles () (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.

Citing Articles

MYADM binds human parechovirus 1 and is essential for viral entry.

Qiao W, Richards C, Kim Y, Zengel J, Ding S, Greenberg H Nat Commun. 2024; 15(1):3469.

PMID: 38658526 PMC: 11043367. DOI: 10.1038/s41467-024-47825-0.

Picornavirus May Be Linked to Parkinson's Disease through Viral Antigen in Dopamine-Containing Neurons of Substantia Nigra.

Niklasson B, Lindquist L, Klitz W, Fredrikson S, Morgell R, Mohammadi R Microorganisms. 2022; 10(3).

PMID: 35336174 PMC: 8953350. DOI: 10.3390/microorganisms10030599.

References

Mills J, Fulhorst C . Small mammal-associated zoonoses. Vector Borne Zoonotic Dis. 2010; 10(6):547. DOI: 10.1089/vbz.2010.1503. View

Plyusnin A, Vapalahti O, Lehvaslaiho H, Apekina N, Mikhailova T, Gavrilovskaya I . Genetic variation of wild Puumala viruses within the serotype, local rodent populations and individual animal. Virus Res. 1995; 38(1):25-41. DOI: 10.1016/0168-1702(95)00038-r. View

Johansson E, Niklasson B, Tesh R, Shafren D, Travassos da Rosa A, Lindberg A . Molecular characterization of M1146, an American isolate of Ljungan virus (LV) reveals the presence of a new LV genotype. J Gen Virol. 2003; 84(Pt 4):837-844. DOI: 10.1099/vir.0.18792-0. View

Lundstig A, McDonald S, Maziarz M, Weldon W, Vaziri-Sani F, Lernmark A . Neutralizing Ljungan virus antibodies in children with newly diagnosed type 1 diabetes. J Gen Virol. 2021; 102(5). PMC: 8969827. DOI: 10.1099/jgv.0.001602. View

Benschop K, de Vries M, Minnaar R, Stanway G, van der Hoek L, Wolthers K . Comprehensive full-length sequence analyses of human parechoviruses: diversity and recombination. J Gen Virol. 2009; 91(Pt 1):145-54. DOI: 10.1099/vir.0.014670-0. View

Krous H, Langlois N . Ljungan virus: a commentary on its association with fetal and infant morbidity and mortality in animals and humans. Birth Defects Res A Clin Mol Teratol. 2010; 88(11):947-52. DOI: 10.1002/bdra.20728. View

Niklasson B, Nyholm E, Feinstein R, Samsioe A, Hornfeldt B . Diabetes and myocarditis in voles and lemmings at cyclic peak densities--induced by Ljungan virus?. Oecologia. 2006; 150(1):1-7. DOI: 10.1007/s00442-006-0493-1. View

Fevola C, Rossi C, Rosa R, Nordstrom A, Ecke F, Magnusson M . DISTRIBUTION AND SEASONAL VARIATION OF LJUNGAN VIRUS IN BANK VOLES (MYODES GLAREOLUS) IN FENNOSCANDIA. J Wildl Dis. 2017; 53(3):552-560. DOI: 10.7589/2016-06-145. View

Calvert J, Chieochansin T, Benschop K, McWilliam Leitch E, Drexler J, Grywna K . Recombination dynamics of human parechoviruses: investigation of type-specific differences in frequency and epidemiological correlates. J Gen Virol. 2010; 91(Pt 5):1229-38. DOI: 10.1099/vir.0.018747-0. View

10.

Nii-Trebi N . Emerging and Neglected Infectious Diseases: Insights, Advances, and Challenges. Biomed Res Int. 2017; 2017:5245021. PMC: 5327784. DOI: 10.1155/2017/5245021. View

11.

Salisbury A, Begon M, Dove W, Niklasson B, Stewart J . Ljungan virus is endemic in rodents in the UK. Arch Virol. 2013; 159(3):547-51. DOI: 10.1007/s00705-013-1731-6. View

12.

Mitake H, Fujii Y, Nagai M, Ito N, Okadera K, Okada K . Isolation of a sp. nov. Ljungan virus from wild birds in Japan. J Gen Virol. 2016; 97(8):1818-1822. DOI: 10.1099/jgv.0.000508. View

13.

Olijve L, Jennings L, Walls T . Human Parechovirus: an Increasingly Recognized Cause of Sepsis-Like Illness in Young Infants. Clin Microbiol Rev. 2017; 31(1). PMC: 5740974. DOI: 10.1128/CMR.00047-17. View

14.

Tapparel C, Junier T, Gerlach D, Van-Belle S, Turin L, Cordey S . New respiratory enterovirus and recombinant rhinoviruses among circulating picornaviruses. Emerg Infect Dis. 2009; 15(5):719-26. PMC: 2687021. DOI: 10.3201/eid1505.081286. View

15.

Darriba D, Taboada G, Doallo R, Posada D . jModelTest 2: more models, new heuristics and parallel computing. Nat Methods. 2012; 9(8):772. PMC: 4594756. DOI: 10.1038/nmeth.2109. View

16.

Benschop K, Molenkamp R, van der Ham A, Wolthers K, Beld M . Rapid detection of human parechoviruses in clinical samples by real-time PCR. J Clin Virol. 2008; 41(2):69-74. DOI: 10.1016/j.jcv.2007.10.004. View

17.

Fevola C, Kuivanen S, Smura T, Vaheri A, Kallio-Kokko H, Hauffe H . Seroprevalence of lymphocytic choriomeningitis virus and Ljungan virus in Finnish patients with suspected neurological infections. J Med Virol. 2017; 90(3):429-435. DOI: 10.1002/jmv.24966. View

18.

Han B, Schmidt J, Bowden S, Drake J . Rodent reservoirs of future zoonotic diseases. Proc Natl Acad Sci U S A. 2015; 112(22):7039-44. PMC: 4460448. DOI: 10.1073/pnas.1501598112. View

19.

Samsioe A, Feinstein R, Saade G, Sjoholm A, Hornfeldt B, Fundele R . Intrauterine death, fetal malformation, and delayed pregnancy in Ljungan virus-infected mice. Birth Defects Res B Dev Reprod Toxicol. 2006; 77(4):251-6. DOI: 10.1002/bdrb.20083. View

20.

Niklasson B, Heller K, Schonecker B, Bildsoe M, Daniels T, Hampe C . Development of type 1 diabetes in wild bank voles associated with islet autoantibodies and the novel ljungan virus. Int J Exp Diabesity Res. 2003; 4(1):35-44. PMC: 2480497. DOI: 10.1080/15438600303733. View