Genetic similarity of Puumala viruses found in Finland and western Siberia and of the mitochondrial DNA of their rodent hosts suggests a common evolutionary origin

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Abstract

A total of 678 small mammals representing eight species were trapped in western Siberia in 1999–2000 and assayed for the presence of hantaviruses. Eighteen animals, all Clethrionomys species, were antigen positive by enzyme-linked immunosorbent assay (ELISA). Small and medium genome segments were recovered by RT-PCR from six samples from Clethrionomys glareolus and three from Clethrionomys rufocanus. Sequence comparison and phylogenetic analysis revealed that these hantaviruses were Puumala virus and were similar to hantavirus strains from Finland. To confirm these data, partial nucleotide sequences of the rodent hosts’ cytochrome b genes were obtained, as well as several sequences from genes from rodents trapped at different localities of European Russia and western Siberia. The cytochrome b sequences of Siberian bank voles were similar to sequences of C. glareolus, trapped in Finland. These data suggest that the Puumala hantaviruses, as well as their rodent hosts, share a common evolutionary history. We propose that these rodents and viruses may be descendents of a population of bank voles that expanded northward from southern refugia during one of the interglacial periods.

Introduction

The Hantavirus genus (family Bunyaviridae) includes viruses that cause hemorrhagic fever with renal syndrome (HFRS). The hantavirus genome consists of a tripartite, single-strand, negative-sense RNA surrounded by a lipid membrane with two surface glycoproteins, G1 and G2. The large (L), medium (M) and small (S) genomic segments encode the viral polymerase, the glycoprotein precursor and the nucleocapsid protein, respectively (Schmaljohn et al., 1986, Schmaljohn et al., 1987, Schmaljohn, 1990).

There are four serologically distinct groups of hantaviruses causing HFRS, represented by Hantaan (HTN), Dobrava (DOB), Seoul (SEO) and Puumala (PUU) viruses (Avsic-Zupank et al., 1992, Lee et al., 1985, Schmaljohn et al., 1985, Sugiyama et al., 1987). They are isolated from the striped field mouse (Apodemus agrarius), yellow-necked field mouse (Apodemus flavicollis), rats (Rattus norvegicus and R. rattus) and bank voles (Clethrionomys glareolus), respectively.

HTN, DOB, SEO and PUU viruses cause the various clinical forms of HFRS characterized by fever, renal failure and, in severe cases, hemorrhagic manifestations. The mortality of HFRS varies from 0.2 to 10%, depending largely upon which hantavirus caused the infection (Schmaljohn and Hjelle, 1997).

In 1993 in the United States, the existence of another hantavirus-associated human disease, called hantavirus pulmonary syndrome (HPS), was reported. The predominant rodent host of the first HPS-causing virus identified, Sin Nombre virus (SN), is the deer mouse (Peromyscus maniculatus) (Childs et al., 1994). Since the discovery of SNV, numerous other hantaviruses able to cause HPS have been identified in North and South America (Enria et al., 2001, Rhodes et al., 2000) and hantaviruses not known to cause either HFRS or HPS have been found worldwide (Parrington and Kang, 1990, Plyusnin et al., 1994).

HFRS is endemic in Russia where approximately four cases per 100,000 people occur annually. However, the level of morbidity differs greatly in various parts of Russia. Thus, only a few cases of HFRS were detected in western Siberia over 20 years, although Clethrionomys species, the main carriers of PUU virus, are abundant in this territory, and findings of hantaviral antigens in rodents were reported repeatedly (Miasnikov et al., 1987, Miasnikov et al., 1992). In contrast, Bashkortostan, which is close to the western Siberian part of central Russia, has the highest rate of HFRS morbidity in Russia (58.3 per 100,000 of population) (Tkachenko et al., 1998). The goal of this study was to determine the type of hantavirus circulating in western Siberia. This study also suggests new information with regard to the evolutionary history of hantaviruses and their carriers.

Section snippets

Trapping and processing of rodents

Samples were obtained from rodents trapped in four locations of the Omsk region in a conifer forest (southern taiga). In addition, several samples from bank voles, C. glareolus, grey red-backed voles, Clethrionomys rufocanus and northern red-backed voles, C. rutilus from several other regions of Russia: Nizhniy Novgorod, Samara, Novosibirsk regions, Bashkortostan, Polar Ural and far east (Khabarovsk region) were used (Fig. 1). Animals were live-trapped (5–10 m between traps), humanely killed,

Detection of viral RNA in rodent samples

A total of 678 rodents representing eight species were trapped. They included (total/ELISA-positive/PCR-positive): C. glareolus—161 (23.7%)/9/6, C. rufocanus—109 (16.1%)/6/3, C. rutilus—306 (45.1%)/3/0, A. agrarius—26 (3.8%), Microtus arvalis—2 (0.3%), M. agrestis—43 (6.3%), M. oeconomus—30 (4.4%) and Micromys minutus—1 (0.1%).

Nine of the lung suspensions from the Omsk samples (CG144, CG315, CG463, CG168, CG215, CG222, CRF308, CRF366 and CRF161) were found to have viral RNA when M-segment

Discussion

Until recently, the diversity of hantaviruses to the east of the Ural mountains in Russia was unknown. Even their presence in Siberia was questioned, as there were no confirmed cases of human disease associated with hantaviruses in this area for over 20 years. A study (Vapalahti et al., 1999) of Siberian lemmings in the arctic tundra (Yamal peninsula, western Siberia) established the existence of a novel hantavirus, Topografov virus. However, because the lemmings’ habitat is generally limited

Acknowledgements

This work was performed while the author (A.D.) held a National Research Council Research Associateship Award at the Laboratory of Molecular Virology, United States Army Medical Research Institute of Infectious Diseases (USAMRIID). We are indebted to the University of Alaska Museum Mammal Collection for providing materials for this study. The authors thank Dr. L.I. Ivanov, Khabarovsk Anti-plague Station, for providing the sample of rodent’s lung tissue. We are grateful to Tricia Lewis for help

References (48)

  • P Sunnucks

    Efficient genetic markers for population biology

    Trends Ecol. E

    (2000)
  • R Adkins et al.

    Molecular phylogeny and divergence time estimates for major rodent groups: evidence from multiple genes

    Mol. Biol. E

    (2001)
  • K Asikainen et al.

    Molecular evolution of Puumala hantavirus in Fennoscandia: phylogenetic analysis of strains from two recolonization routes, Karelia and Denmark

    J. Gen. Virol.

    (2000)
  • T Avsic-Zupank et al.

    Characterization of Dobrava virus: a Hantavirus from Slovenia, Yugoslavia

    J. Med. Virol.

    (1992)
  • P Beerli et al.

    Maximum likelihood estimation of a migration matrix and effective population sizes in n subpopulations by using a coalescent approach

    Proc. Natl. Acad. Sci. U.S.A.

    (2001)
  • J Childs et al.

    Serologic and genetic identification of Peromyscus maniculatus as the primary rodent reservoir for a new hantavirus in the southwestern United States

    J. Infect. Dis.

    (1994)
  • J Dallas et al.

    Population subdivision and gene flow in Danish house mice

    Mol. Ecol.

    (1995)
  • D Enria et al.

    Clinical manifestations of new world hantaviruses

    Curr. Top. Microbiol. Immunol.

    (2001)
  • G Hewitt

    The genetic legacy of the quaternary ice ages

    Nature

    (2000)
  • J Hörling et al.

    Khabarovsk, a phylogenetically and serologically distinct hantavirus isolated from Microtus fortis trapped in far east Russia

    J. Gen. Virol.

    (1996)
  • A Ivanov et al.

    Outbreak of hemorrhagic fever with renal syndrome in Egor’evsk district of Moscow region

    Voprosy Virusologii

    (2000)
  • G.C Johns et al.

    A comparative summary of genetic distances in the vertebrates from the mitochondrial cytochrome b gene

    Mol. Biol. Evol.

    (1998)
  • Kumar, S., Tamura, K., Jakobsen, I., Nei, M., 2000. MEGA: Molecular Evolutionary Genetics Analysis, Version 2β....
  • P Lee et al.

    Serotypic classification of hantaviruses by indirect immunofluorescent antibody and plaque reduction neutralization tests

    J. Clin. Microbiol.

    (1985)
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