Dissemination of Yersinia pestis of Medieval Biovar in Northern, North-Western Caspian Sea Region and Fore-Caucasus in the second Half of the Twentieth Century

Objective of the study was to determine the origin of Y. pestis strains that widely disseminated in natural plague foci of Northern, North-Western Caspian Sea region and Fore-Caucasus in the second half of the XX century. Materials and methods. We have carried out the investigation of properties and whole genome sequencing of 22 Y. pestis strains, isolated between 1923 and 2003 in five natural foci of the souslik type, situated in Northern and North-Western Caspian Sea region and Fore-Caucasus. Phylogenetic analysis was conducted using the data of whole genome SNP-typing, based on 1348 identified SNPs. The search of SNPs in the core genome was performed with the help of Wombac 2.0 software. Phylogenetic relations were analyzed using Maximum Likelihood dendrogram, GTR model. Results and discussion. All the studied strains from the foci of Northern, North-Western Caspian Sea region and Fore-Caucasus fall into phylogenetic branch 2. MED1of medieval biovar. On the basis of whole genome SNP-analysis, existence of two groups of closely related strains, comprising the strains dated 1923-1945 and 1962-2003, has been revealed. The predecessors of the 1962-2003 strains from the Northern, North-Western Caspian Sea region and Fore-Caucasus on the phylogenetic tree are the strains from Northern Aral Sea region that go back to 1945. It testifies to the fact that synchronized activation of a group of natural foci in Caspian Sea lowland and Fore-Caucasus in 1975-1979, after prolonged 20-37 year long breaks, could be caused by the dissemination of the strains from the Northern Aral Sea region. The data of epizootic observations indicate that activation of Volga-Ural sandy plague focus in 1960s preceded the start of registration of plague epizooties in the territory of natural foci of souslik type in Northern, North-Western Caspian sea region and Fore-Caucasus.

1. Kutyrev V.V., Popova A.Yu., editors. [Cadastre of Epidemic and Epizootic Plague Manifestations in the Territory of the Russian Federation and Neighboring Countries (between 1876 and 2016)]. Saratov: “Amirit” LLC; 2016. 248 p.

2. Onishchenko G.G., Kutyrev V.V., editors. [Natural Plague Foci in the Territory of Caucasus, Caspian Sea Region, Central Asia, and Siberia]. M.: “Meditsina”; 2004. 191 p.

3. Bocharnikov O.N., Karpuzidi K.S., Klimchenko I.V, Ter-Vartanov V.N., Tinker I.S., Shishkin A.K., Shiryaev D.T. [Experience in eradication of plague in the focus of North-Western Caspian Sea region]. In: [Natural Focality and Epidemiology of Particularly Dangerous Infectious Diseases]. Saratov; 1959. P. 235-46.

4. Jones S D., Atshabar B., Schmid B.V., Zuka M., Amramina A., Stenseth N.C. Living with plague: Lessons from the Soviet Union’s antiplague system. Proc. Natl. Acad. Sci. USA. 2019; 116(19):9155-63.

5. Zolotokrylin A.N. [Climatic Desertification]. M.: “Nauka”; 2003. 245 p.

6. Sizemskaya M.L. [Modern Natural-Anthropogenic Transformation of Semi-Desert Soils of Northern Caspian Sea Region]. M.; 2013. 276 p.

7. Kolchin E.A., Barmin A.N., Kryzhinovskaya G.V., Valov M.V [Peculiarities of climate changes of arid territories of the Russian Federation]. Geologiya, Geografiya i Global’naya Energiya. [Geology, Geography, and Global Energy]. 2017; 4:113-22.

8. Titkova T.B. [Climate changes in semi-desert areas of Caspian Sea region and Turgai in the XX century]. RAS Bulletin. Geography series. 2003; 1:106-12.

9. Zolotokrylin A.N., Titkova T.B., Cherenkova E.A., Vinogradova V.V [Trends in hydration and biophysical parameters of arid lands in the European part of Russia over the period of 2000-2014]. Sovremennye Problemy Distantsionnogo Zondirovaniya Zemli iz Kosmosa. [Current Problems of Earth Remote Probing from Space]. 2015; 12(2):155-61.

10. Nesterov E.S., editor. [Water Balance and Fluctuations in the Level of the Caspian Sea. Modeling and Forecasting]. M.: “Triada”; 2016. 370 p.

11. Popov N.V, Udovikov A.I., Eroshenko G.A., Karavaeva T.B., Yakovlev S.A., Porshakov A.M., Zenkevich E.S., Kutyrev V.V. [Effect of Caspian Sea level fluctuations on epizootic activity of Pre-Caspian sandy natural plague focus]. MeditsinskayaParazitologiya i Parazitarnye Bolezni [Medical Parasitology and Parasitic Diseases]. 2016; 1:12-7.

12. Tanitovsky V.A., Maikanov N.S. [Alleged causes of de-crease in epizootic activity of plague foci in the Northern Caspian Sea region]. Karantinnye i Zoonoznye Infektsii v Kazakhstane. [Quarantine and Zoonotic Infections in Kazakhstan]. Almaty. 2019; 1(38):127-31.

13. Khasnis AA, Nettleman MD. Global warming and infec¬tious diseases. Arch. Med. Res. 2005; 36:689-96.

14. Stenseth N.C., Samia N.I., Viljugrein H., Kausrud K.L., Begon M., Davis S., Leirs H., Dubyanskiy V.M., Esper J., Ageyev V.S., Klassovskiy N.L., Pole S.B., Chan K.-S. Plague dynamics are driven by climate variation. Proc. Natl. Acad. Sci. USA. 2006; 103(35):13110-15. DOI: 10.1073/pnas.0602447103.

15. Kausrud K.L., Viljugrein H., Frigessi A., Begon M., Davis S., Leirs H., Dubyandkiy V, Stenseth N.C. Climatically driven syn-chrony of gerbil populations allows large-scale plague outbreaks. Proc. Natl. Acad. Sci. USA. 2007; 274(1621):1963-9. DOI: 10.1098/rspb.2007.0568.

16. Nakazawa Y, Williams R., Peterson A.T., Mead P., Staples E., Gage K.L. Climate change effects on plague and tularemia in the United States. Vector Borne Zoonotic Dis. 2007; 7(4):529-40. DOI: 10.1089/vbz.2007.0125.

17. Snall T., O’Hara R.B., Ray C., Collinge S.K. Climate-driven spatial dynamics of plague among prairie dog colonies. Am. Nat. 2008; 171(2):238-48. DOI: 10.1086/525051.

18. Ben Ari T., Neerinckx S., Gage K.L., Kreppel K., Laudisoit A., Leirs H.,. Stenseth N.C. Plague andClimate: Scales Matter. PLoS Pathog. 2011; 7(9):e1002160. DOI: 10.1371/journal.ppat.1002160.

19. Kutyrev V.V., Eroshenko G.A., Motin V.L., Nosov N.Y, Krasnov J.M., Kukleva L.M., Nikiforov K.A., Al’hova J.V., Oglodin E.G., Guseva N.P. Phylogeny and classification of Yersinia pestis through the lens of strains from the plague foci of Commonwealth of Independent States. Front. Microbiol. 2018; 9:1106. DOI: 10.3389/fmicb.2018.01106.

20. Eroshenko G.A., Popov N.V., Alkhova Zh.V., Balykova A.N., Kukleva L.M., Chervyakova N.S., Maykanov N.S., Sarmuldina A. Kh., Kutyrev V.V. [Circulation of Yersinia pestis in the Volga-Ural sandy focus: spatiotemporal analysis]. Problemy Osobo Opasnykh Infektsii [Problems of Particularly Dangerous Infections]. 2019; 3:51-7. DOI: 10.21055/0370-1069-2019-3-51-57.

21. Eroshenko G.A., Popov N.V., Alkhova Zh.V., Balykova A.N., Kukleva L.M., Kutyrev V.V. [Phylogenetic analysis of Yersinia pestis strains of Medieval biovar, isolated in Precaspian North-Western steppe plague focus in the XX century]. Problemy Osobo Opasnykh Infektsii [Problems of Particularly Dangerous Infections]. 2019; 2:55-61. DOi: 10.21055/0370-1069-2019-2-55-61.

22. Onishchenko G.G., Kutyrev V.V., editors. [Laboratory Diagnostics of Particularly Dangerous Infectious Diseases. Practice Guidelines]. M.: CJSC «Shiko»; 2013: 560 p.

23. Cui Y., Yu C., Yan Y, Li D., Li Y, Jombart T., Lucy A Weinert, Wang Z., Guo Z., Xu L., Zhang Y, Zheng H., Qin N., Xiao X., Wu M., Wang X., Zhou D., Qi Z., Du Z., Wu H., Yang X., Cao H., Wang H., Wang J., Yao S., Rakin A., Li Y, Falush D., Balloux F., Achtman M., Song Y., Wang J., Yang R.. Historical variations in mu-tation rate in an epidemic pathogen, Yersinia pestis. Proc. Natl. Acad. Sci. USA. 2013; 110(2):577-82. DOI: 10.1073/pnas.1205750110.