Genetic features of the Puumala virus (Hantaviridae: Orthohantavirus) identified in the Moscow region

Cover Page

Cite item

Full Text

Abstract

Introduction. Puumala virus (family Hantaviridae, genus Orthohantavirus) is distributed in most regions of the European part of Russia. However, information about its genetic variants circulating on the territory of the Central Federal District is extremely scarce.

Materials and methods. Rodents’ tissue samples were tested after reverse transcription by PCR for the presence of hantaviral RNA. The amplified fragments of the L segment were sequenced by the Sanger method. For two samples, sequences of all three segments were obtained using the NGS method. Phylogenetic trees were built in the MEGA-X software.

Results. Puumala virus was found in six samples. Based on the phylogenetic analysis of sequences of three segments, the obtained genetic variants belong to the sublineage previously designated as W-RUS.

Conclusion. A genetic variant of the Puumala virus, belonging to the subline W-RUS, circulates on the territory of the Volokolamsk district of Moscow region.

About the authors

Ekaterina A. Blinova

Central Research Institute for Epidemiology of the Federal Service for Surveillance on Consumer Rights Protection and Human Wellbeing; Federal Scientific Center for Research and Development of Immune-and-Biological Products of Russian Academy of Sciences (Institute of poliomyelitis)

Author for correspondence.
Email: blinova.e@cmd.su
ORCID iD: 0000-0002-0735-5627

research associate; PhD student

Russian Federation, 111123, Moskow; 108819, Moscow

Marat T. Makenov

Central Research Institute for Epidemiology of the Federal Service for Surveillance on Consumer Rights Protection and Human Wellbeing

Email: makenov@cmd.su
ORCID iD: 0000-0002-6835-4572

PhD, research associate

Russian Federation, 111123, Moskow

Evgeny S. Morozkin

Central Research Institute for Epidemiology of the Federal Service for Surveillance on Consumer Rights Protection and Human Wellbeing

Email: morozkin@cmd.su
ORCID iD: 0000-0001-8407-2623

PhD, research associate

Russian Federation, 111123, Moskow

Ivan S. Kholodilov

Federal Scientific Center for Research and Development of Immune-and-Biological Products of Russian Academy of Sciences (Institute of poliomyelitis)

Email: ivan-kholodilov@bk.ru
ORCID iD: 0000-0002-3764-7081

PhD, research associate

Russian Federation, 108819, Moscow

Marina V. Fedorova

Central Research Institute for Epidemiology of the Federal Service for Surveillance on Consumer Rights Protection and Human Wellbeing

Email: culicidae@mail.ru
ORCID iD: 0000-0002-1232-1624

PhD, research associate

Russian Federation, 111123, Moskow

Olga B. Zhurenkova

Central Research Institute for Epidemiology of the Federal Service for Surveillance on Consumer Rights Protection and Human Wellbeing

Email: Zhurenkova@cmd.su
ORCID iD: 0000-0003-1571-4826

research associate

Russian Federation, 111123, Moskow

German V. Roev

Central Research Institute for Epidemiology of the Federal Service for Surveillance on Consumer Rights Protection and Human Wellbeing; Moscow Institute of Physics and Technology (National Research University)

Email: roev@cmd.su
ORCID iD: 0000-0002-2353-5222

research associate; Student

Russian Federation, 111123, Moskow; 141701, Moscow

Kamil F. Khafizov

Central Research Institute for Epidemiology of the Federal Service for Surveillance on Consumer Rights Protection and Human Wellbeing

Email: khafizov@cmd.su
ORCID iD: 0000-0001-5524-0296

PhD, Head of the Laboratory

Russian Federation, 111123, Moskow

Ludmila S. Karan

Central Research Institute for Epidemiology of the Federal Service for Surveillance on Consumer Rights Protection and Human Wellbeing

Email: karan@cmd.su
ORCID iD: 0000-0002-5927-460X

Group Leader

Russian Federation, 111123, Moskow

References

  1. Bernshteyn A.D., Gavrilovskaya I.N., Apekina N.S., Dzagurova T.K., Tkachenko E.A. Features of the natural focality of hantavirus zoonoses. Epidemiologiya i vaktsinoprofilaktika. 2010; (2): 5–13. https://www.elibrary.ru/micwyl (in Russian)
  2. Kuhn J.H., Schmaljohn C.S. A brief history of bunyaviral family hantaviridae. Diseases. 2023; 11(1): 38. https://doi.org/10.3390/diseases11010038
  3. Lee G.Y., Kim W.K., Park K., Lee S.H., Hwang J., No J.S., et al. Phylogeographic diversity and hybrid zone of Hantaan orthohantavirus collected in Gangwon Province, Republic of Korea. PLoS Negl. Trop. Dis. 2020; 14(10): e0008714. https://doi.org/10.1371/journal.pntd.0008714
  4. Vetter P., L’Huillier A.G., Montalbano M.F., Pigny F., Eckerle I., Torriani G., et al. Puumala virus infection in family, Switzerland. Emerg. Infect. Dis. 2021; 27(2): 658–60. https://doi.org/10.3201/eid2702.203770
  5. Tkachenko E.A., Ishmukhametov A.A., Dzagurova T.K., Bernshtein A.D., Morozov V.G., Siniugina A.A., et al. Hemorrhagic fever with renal syndrome, Russia. Emerg. Infect. Dis. 2019; 25(12): 2325–8. https://doi.org/10.3201/eid2512.181649
  6. Szabó R., Radosa L., Ličková M., Sláviková M., Heroldová M., Stanko M., et al. Phylogenetic analysis of Puumala virus strains from Central Europe highlights the need for a full-genome perspective on hantavirus evolution. Virus Genes. 2017; 53(6): 913–7. https://doi.org/10.1007/s11262-017-1484-5
  7. Garanina S.B., Platonov A.E., Zhuravlev V.I., Murashkina A.N., Yakimenko V.V., Korneev A.G., et al. Genetic diversity and geographic distribution of hantaviruses in Russia. Zoonoses Public Health. 2009; 56(6-7): 297–309. https://doi.org/10.1111/j.1863-2378.2008.01210.x
  8. Kabwe E., Davidyuk Y., Shamsutdinov A., Garanina E., Martynova E., Kitaeva K., et al. Orthohantaviruses, emerging zoonotic pathogens. Pathogens. 2020; 9(9): 775. https://doi.org/10.3390/pathogens9090775
  9. Klempa B. Reassortment events in the evolution of hantaviruses. Virus Genes. 2018; 54(5): 638–46. https://doi.org/10.1007/s11262-018-1590-z
  10. Castel G., Chevenet F., Razzauti M., Murri S., Marianneau P., Cosson J.F., et al. Phylogeography of Puumala orthohantavirus in Europe. Viruses. 2019; 11(8): 679. https://doi.org/10.3390/v11080679
  11. Dekonenko A., Yakimenko V., Ivanov A., Morozov V., Nikitin P., Khasanova S., et al. 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. Infect. Genet. Evol. 2003; 3(4): 245–57. https://doi.org/10.1016/s1567-1348(03)00088-1
  12. Sironen T., Vaheri A., Plyusnin A. Molecular evolution of Puumala hantavirus. J. Virol. 2001; 75(23): 11803–10. https://doi.org/10.1128/JVI.75.23.11803-11810.2001
  13. Blinova E., Deviatkin A., Kurashova S., Balovneva M., Volgina I., Valdokhina A., et al. A fatal case of haemorrhagic fever with renal syndrome in Kursk Region, Russia, caused by a novel Puumala virus clade. Infect. Genet. Evol. 2022; 102: 105295. https://doi.org/10.1016/j.meegid.2022.105295
  14. Yashina L.N., Tregubchak T.V., Malyshev B.S., Smetannikova N.A., Grishchenko I.V., Dol’skiy A.A., et al. Study of the exosomal microrna-126 and microrna-218 expression profiles in patients with hemorrhagic fever with renal syndrome (hfrs). Problemy osobo opasnykh infektsiy. 2021; (4): 150–6. https://doi.org/10.21055/0370-1069-2021-4-150-156 https://elibrary.ru/dxxsey (in Russian)
  15. Kabwe E., Al Sheikh W., Shamsutdinov A.F., Ismagilova R.K., Martynova E.V., Ohlopkova O.V., et al. Analysis of Puumala orthohantavirus genome variants identified in the territories of Volga federal district. Trop. Med. Infect. Dis. 2022; 7(3): 46. https://doi.org/10.3390/tropicalmed7030046
  16. Davidyuk Y., Shamsutdinov A., Kabwe E., Ismagilova R., Martynova E., Belyaev A., et al. Prevalence of the Puumala orthohantavirus strains in the Pre-Kama area of the Republic of Tatarstan, Russia. Pathogens. 2020; 9(7): 540. https://doi.org/10.3390/pathogens9070540
  17. Davidyuk Y.N., Kabwe E., Shamsutdinov A.F., Knyazeva A.V., Martynova E.V., Ismagilova R.K., et al. The Distribution of Puumala orthohantavirus genome variants correlates with the regional landscapes in the Trans-Kama area of the Republic of Tatarstan. Pathogens. 2021; 10(9): 1169. https://doi.org/10.3390/pathogens10091169
  18. Martynova E., Davidyuk Y., Kabwe E., Garanina E.E., Shakirova V., Pavelkina V., et al. Cytokine, chemokine, and metalloprotease activation in the serum of patients with nephropathia epidemica from the Republic of Tatarstan and the Republic of Mordovia, Russia. Pathogens. 2021; 10(5): 527. https://doi.org/10.3390/pathogens10050527
  19. Savitskaya T.A., Ivanova A.V., Isaeva G.Sh., Reshetnikova I.D., Trifonov V.A., Ziatdinov V.B., et al. Assessment of epidemiological situation on hemorhhagic fever with renal syndrome around the world and in Russia, forecast for 2020. Problemy osobo opasnykh infektsiy. 2020; (2): 62–70. https://doi.org/10.21055/0370-1069-2020-2-62-70 https://elibrary.ru/oqmbzo (in Russian)
  20. Shchipanov N.A. Universal live-trap for small mammals. Zoologicheskiy zhurnal. 1987; 66(5): 759–61. (in Russian)
  21. Mills J., Childs J., Ksiazek T., Peters C., Velleca W. Methods for trapping and sampling small mammals for virologic testing; 1995. Available at: https://stacks.cdc.gov/view/cdc/11507
  22. Klempa B., Fichet-Calvet E., Lecompte E., Auste B., Aniskin V., Meisel H., et al. Hantavirus in African wood mouse, Guinea. Emerg. Infect. Dis. 2006; 12(5): 838–40. https://doi.org/10.3201/eid1205.051487
  23. Bolger A.M., Lohse M., Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014; 30(15): 2114–20. https://doi.org/10.1093/bioinformatics/btu170
  24. Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.journal. 2011; 17(1): 10. https://doi.org/10.14806/ej.17.1.200
  25. Langmead B., Salzberg S.L. Fast gapped-read alignment with Bowtie 2. Nat. Methods. 2012; 9(4): 357–9. https://doi.org/10.1038/nmeth.1923
  26. Wilm A., Aw P.P., Bertrand D., Yeo G.H., Ong S.H., Wong C.H., et al. LoFreq: a sequence-quality aware, ultra-sensitive variant caller for uncovering cell-population heterogeneity from high-throughput sequencing datasets. Nucleic. Acids. Res. 2012; 40(22): 11189–201. https://doi.org/10.1093/nar/gks918
  27. Danecek P., Bonfield J.K., Liddle J., Marshall J., Ohan V., Pollard M.O., et al. Twelve years of SAMtools and BCFtools. Gigascience. 2021; 10(2): giab008. https://doi.org/10.1093/gigascience/giab008
  28. Van der Auwera G.A., O’Connor B.D. Genomics in the Cloud: Using Docker, GATK, and WDL in Terra. O’Reilly Media; 2020.
  29. Kumar S., Stecher G., Li M., Knyaz C., Tamura K. MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Mol. Biol. Evol. 2018; 35(6): 1547–9. https://doi.org/10.1093/molbev/msy096
  30. Ivanov A.P., Dekonenko A.E., Dzagurova T.K., Malkin A.E., Shervarli I.V., Baranovskiy P.M., et al. Analysis of an outbreak of hemorrhagic fever with the renal syndrome in the Egoryevsk district of the Moscow region. Voprosy virusologii. 2000; 45(4): 33–6. (in Russian)
  31. Garanina S.B., Platonov A.E., Zhuravlev V.I., Murashkina A.N., Yakimenko V.V., Korneev A.G., et al. Genetic diversity and geographic distribution of hantaviruses in Russia. Zoonoses Public Health. 2009; 56(6-7): 297–309. https://doi.org/10.1111/j.1863-2378.2008.01210.x
  32. Razzauti M., Plyusnina A., Niemimaa J., Henttonen H., Plyusnin A. Co-circulation of two Puumala hantavirus lineages in Latvia: a Russian lineage described previously and a novel Latvian lineage. J. Med. Virol. 2012; 84(2): 314–8. https://doi.org/10.1002/jmv.22263
  33. Kabwe E., Shamsutdinov A.F., Suleimanova S., Martynova E.V., Ismagilova R.K., Shakirova V.G., et al. Puumala orthohantavirus reassortant genome variants likely emerging in the watershed forests. Int. J. Mol. Sci. 2023; 24(2): 1018. https://doi.org/10.3390/ijms24021018

Supplementary files

Supplementary Files
Action
1. JATS XML
Download
2. Figure. Phylogenetic trees constructed on the basis of alignments: a ‒ 1302 nucleotides of the S segment corresponding to the complete reading frame of the nucleocapsid protein; b – 3050 nucleotides of the M segment (partial open reading frame, ORF); c – 5960 nucleotides of the L segment (partial ORF). The sequences obtained in this study are marked. Phylogenetic trees were constructed using the Maximum Likelihood method using the General Time Reversible (G+I) model using the MEGA X program [29].

Download (684KB)
Indexing metadata

Copyright (c) 2023 Blinova E.A., Makenov M.T., Morozkin E.S., Kholodilov I.S., Fedorova M.V., Zhurenkova O.B., Roev G.V., Khafizov K.F., Karan L.S.

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.

This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies