Phylogenetic Analysis of Puumala Virus Strains from Central Europe Highlights the Need for a Full-genome Perspective on Hantavirus Evolution

Overview

Journal Virus Genes

Specialties Microbiology
Molecular Biology

Date 2017 Jul 1

PMID 28664467

Citations 7

Authors

Robert Szabo

Lukas Radosa

Martina Lickova

Monika Slavikova

Marta Heroldova

Michal Stanko

Milan Pejcoch

Anja Osterberg

Lies Laenen

Susanne Schex

Rainer G Ulrich

Sandra Essbauer

Piet Maes

Boris Klempa

Affiliations

Soon will be listed here.

Abstract

Puumala virus (PUUV), carried by bank voles (Myodes glareolus), is the medically most important hantavirus in Central and Western Europe. In this study, a total of 523 bank voles (408 from Germany, 72 from Slovakia, and 43 from Czech Republic) collected between the years 2007-2012 were analyzed for the presence of hantavirus RNA. Partial PUUV genome segment sequences were obtained from 51 voles. Phylogenetic analyses of all three genome segments showed that the newfound strains cluster with other Central and Western European PUUV strains. The new sequences from Šumava (Bohemian Forest), Czech Republic, are most closely related to the strains from the neighboring Bavarian Forest, a known hantavirus disease outbreak region. Interestingly, the Slovak strains clustered with the sequences from Bohemian and Bavarian Forests only in the M but not S segment analyses. This well-supported topological incongruence suggests a segment reassortment event or, as we analyzed only partial sequences, homologous recombination. Our data highlight the necessity of sequencing all three hantavirus genome segments and of a broader bank vole screening not only in recognized endemic foci but also in regions with no reported human hantavirus disease cases.

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References

Yang Z . Maximum-likelihood estimation of phylogeny from DNA sequences when substitution rates differ over sites. Mol Biol Evol. 1993; 10(6):1396-401. DOI: 10.1093/oxfordjournals.molbev.a040082. View

Nikolic V, Stajkovic N, Stamenkovic G, cekanac R, Marusic P, Siljic M . Evidence of recombination in Tula virus strains from Serbia. Infect Genet Evol. 2013; 21:472-8. DOI: 10.1016/j.meegid.2013.08.020. View

Filipi K, Markova S, Searle J, Kotlik P . Mitogenomic phylogenetics of the bank vole Clethrionomys glareolus, a model system for studying end-glacial colonization of Europe. Mol Phylogenet Evol. 2014; 82 Pt A:245-57. DOI: 10.1016/j.ympev.2014.10.016. View

Ronquist F, Teslenko M, van der Mark P, Ayres D, Darling A, Hohna S . MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol. 2012; 61(3):539-42. PMC: 3329765. DOI: 10.1093/sysbio/sys029. View

Kruger D, Figueiredo L, Song J, Klempa B . Hantaviruses--globally emerging pathogens. J Clin Virol. 2014; 64:128-36. DOI: 10.1016/j.jcv.2014.08.033. View

Kirsanovs S, Klempa B, Franke R, Lee M, Schonrich G, Rang A . Genetic reassortment between high-virulent and low-virulent Dobrava-Belgrade virus strains. Virus Genes. 2010; 41(3):319-28. DOI: 10.1007/s11262-010-0523-2. View

Biek R, Pybus O, Lloyd-Smith J, Didelot X . Measurably evolving pathogens in the genomic era. Trends Ecol Evol. 2015; 30(6):306-13. PMC: 4457702. DOI: 10.1016/j.tree.2015.03.009. View

Essbauer S, Schmidt-Chanasit J, Madeja E, Wegener W, Friedrich R, Petraityte R . Nephropathia epidemica in metropolitan area, Germany. Emerg Infect Dis. 2007; 13(8):1271-3. PMC: 2828076. DOI: 10.3201/eid1308.061425. View

Rizvanov A, Khaiboullina S, St Jeor S . Development of reassortant viruses between pathogenic hantavirus strains. Virology. 2004; 327(2):225-32. DOI: 10.1016/j.virol.2004.07.012. View

10.

Mertens M, Kindler E, Emmerich P, Esser J, Wagner-Wiening C, Wolfel R . Phylogenetic analysis of Puumala virus subtype Bavaria, characterization and diagnostic use of its recombinant nucleocapsid protein. Virus Genes. 2011; 43(2):177-91. DOI: 10.1007/s11262-011-0620-x. View

11.

Hasegawa M, Kishino H, Yano T . Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol. 1985; 22(2):160-74. DOI: 10.1007/BF02101694. View

12.

Thoma B, Muller J, Bassler C, Georgi E, Osterberg A, Schex S . Identification of factors influencing the Puumala virus seroprevalence within its reservoir in aMontane Forest Environment. Viruses. 2014; 6(10):3944-67. PMC: 4213572. DOI: 10.3390/v6103944. View

13.

Razzauti M, Plyusnina A, Sironen T, Henttonen H, Plyusnin A . Analysis of Puumala hantavirus in a bank vole population in northern Finland: evidence for co-circulation of two genetic lineages and frequent reassortment between strains. J Gen Virol. 2009; 90(Pt 8):1923-1931. DOI: 10.1099/vir.0.011304-0. View

14.

Heyman P, Thoma B, Marie J, Cochez C, Essbauer S . In Search for Factors that Drive Hantavirus Epidemics. Front Physiol. 2012; 3:237. PMC: 3429022. DOI: 10.3389/fphys.2012.00237. View

15.

Edgar R . MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004; 32(5):1792-7. PMC: 390337. DOI: 10.1093/nar/gkh340. View

16.

Henderson W, Monroe M, St Jeor S, Thayer W, Rowe J, Peters C . Naturally occurring Sin Nombre virus genetic reassortants. Virology. 1995; 214(2):602-10. DOI: 10.1006/viro.1995.0071. View

17.

Essbauer S, Schmidt J, Conraths F, Friedrich R, Koch J, Hautmann W . A new Puumala hantavirus subtype in rodents associated with an outbreak of Nephropathia epidemica in South-East Germany in 2004. Epidemiol Infect. 2006; 134(6):1333-44. PMC: 2870504. DOI: 10.1017/S0950268806006170. View

18.

Hofmann J, Meisel H, Klempa B, Vesenbeckh S, Beck R, Michel D . Hantavirus outbreak, Germany, 2007. Emerg Infect Dis. 2008; 14(5):850-2. PMC: 2600236. DOI: 10.3201/eid1405.071533. View

19.

Handke W, Oelschlegel R, Franke R, Wiedemann L, Kruger D, Rang A . Generation and characterization of genetic reassortants between Puumala and Prospect Hill hantavirus in vitro. J Gen Virol. 2010; 91(Pt 9):2351-9. DOI: 10.1099/vir.0.021139-0. View

20.

Klempa B, Schmidt H, Ulrich R, Kaluz S, Labuda M, Meisel H . Genetic interaction between distinct Dobrava hantavirus subtypes in Apodemus agrarius and A. flavicollis in nature. J Virol. 2002; 77(1):804-9. PMC: 140611. DOI: 10.1128/jvi.77.1.804-809.2003. View