Complex Characteristics of Yersinia pestis Strains Isolated in the Sarydzhaz and Upper-Naryn High-Mountain Foci in 2019–2020
https://doi.org/10.21055/0370-1069-2021-2-114-122
Abstract
The aim of the study was a comprehensive analysis of the phenotypic and genetic properties of Yersinia pestis strains isolated in the Sarydzhaz and Upper-Naryn high-mountain foci of the Tien Shan in 2019–2020; determination of the present-day population structure and areal of these highly virulent strains of the plague pathogen.
Materials and methods. Studies of biochemical properties (fermentation of carbohydrates, nutritional requirements), virulence (in vitro and in laboratory animals), molecular-genetic analysis and whole genome sequencing of Y. pestis strains isolated in the Sarydzhaz and Upper-Naryn high-mountain foci in 2019–2020 have been carried out. We used Y. pestis strains from the foci of the Tien Shan and Pamir-Alai dated 1928–2016 for the comparison. Whole genome sequencing was performed using the Ion S5 XL System. Phylogenetic analysis was performed on the basis of 1443 identified core SNPs in 36 Y. pestis strains of various phylogenetic lines included in the analysis. The construction of dendrograms was carried out using the Maximum Likelihood algorithm, PHYML program, HKY85 model.
Results and discussion. It is established that all Y. pestis strains isolated in the Sarydzhaz and Upper-Naryn high-mountain foci in 2019–2020 belong to the 0.ANT5 phylogenetic branch of the ancient biovar of the main subspecies. Genome-wide sequencing revealed the presence of two 0.ANT5 clones, the first of which consists of strains from the basin of the river Kooylu in the Sarydzhaz focus, dated 2020. The second powerful clone includes the strains of 2012–2020 isolated in the Sarydzhaz and Upper-Naryn foci. The high virulence of the isolated strains has been shown. It was concluded that further study of the territories of the highmountain foci of the Tien Shan and Pamir-Alai is necessary to establish the current boundaries of the 0.ANT5 areal, as well as to identify the circulation areas of Y. pestis of other phylogenetic lineages.
About the Authors
L. M. KuklevaRussian Federation
46, Universitetskaya St., Saratov, 410005
A. K. Dzhaparova
Kyrgyzstan
92, Skryabina St., Bishkek
E. G. Oglodin
Russian Federation
46, Universitetskaya St., Saratov, 410005
E. A. Naryshkina
Russian Federation
46, Universitetskaya St., Saratov, 410005
Ya. M. Krasnov
Russian Federation
46, Universitetskaya St., Saratov, 410005
A. A. Kuznetsov
Russian Federation
46, Universitetskaya St., Saratov, 410005
A. V. Fadeeva
Russian Federation
46, Universitetskaya St., Saratov, 410005
G. A. Eroshenko
Russian Federation
46, Universitetskaya St., Saratov, 410005
S. K. Berdiev
Kyrgyzstan
92, Skryabina St., Bishkek
V. V. Kutyrev
Russian Federation
46, Universitetskaya St., Saratov, 410005
References
1. Onishchenko G.G., Kutyrev V.V., editors. [Natural Plague Foci in the Territory of Caucasus, Caspian Sea Region, Central Asia and Siberia]. Moscow: “Meditsina”; 2004.191 p.
2. Kutyrev V.V., Popova A.Yu., editors. [Cadastre of Epidemic and Epizootic Manifestations of Plague in the Territory of the Russian Federation and Former Soviet Union (1876–2016)]. Saratov: LLC “Amirit”; 2016. 248 p.
3. Sariyeva G., Bazarkanova G., Maimulov R., Abdikarimov S., Kurmanov B., Abdirassilova A., Shabunin A., Sagiyev Z., Dzhaparova A., Abdel Z., Mussagaliyeva R., Morand S., Motin V., Kosoy M. Marmots and Yersinia pestis strains in two plague endemic areas of Tien Shan mountains. Front. Vet. Sci. 2019; 6:207. DOI: 10.3389/fvets.2019.00207.
4. Abdikarimov S.T., Ibragimov E.S., Egembergenov C.E. [Current Epizootic Condition of Natural Plague Foci in Kyrgyz Republic and Measures Aimed at Provision of Epidemiological Welfare as regards Plague]. Problemy Osobo Opasnykh Infektsii [Problems of Particularly Dangerous Infections]. 2018; (2):45-8. DOI: 10.21055/0370-1069-2018-2-45-48.
5. Eroshenko G.A., Dzhaparova A.K., Oglodin E.G., Al’khova Z.V., Kukleva L.M., Kuznetsov A.A., Krasnov Y.M., Abdikarimov S.T., Kutyrev V.V. [Phylogeny of Yersinia pestis Strains Belonging to 0.ANT Branch, Isolated in Tien-Shan and Pamir-Alay in XX– XXI Centuries]. Problemy Osobo Opasnykh Infektsii [Problems of Particularly Dangerous Infections]. 2020; 1:76–84. DOI: 10.21055/0370-1069-2020-1-76-84.
6. Eroshenko G.A., Nosov N.Y., Krasnov Y.M., Oglodin Y.G., Kukleva L.M., Guseva N.P., Kuznetsov A.A., Abdikarimov S.T., Dzhaparova A.K., Kutyrev V.V. Yersinia pestis strains of ancient phylogenetic branch 0.ANT are widely spread in the high-mountain plague foci of Kyrgyzstan. PLoS One. 2017; 12(10):e0187230. DOI: 10.1371/journal.pone.0187230.
7. 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.
8. Harbeck M., Seifert L., Hänsch S., Wagner D.M., Birdsell D., Parise K.L., Wiechmann I., Grupe G., Thomas A., Keim P., Zöller L., Bramanti B., Riehm J.M., Scholz H.C. Yersinia pestis DNA from skeletal remains from the 6(th) century AD reveals insights into Justinianic plague. PLoS Pathog. 2013; 9(5):e1003349. DOI: 10.1371/journal.ppat.1003349.
9. Wagner D.M., Klunk J., Harbeck M., Devault A., Waglechner N., Sahl J.W., Enk J., Birdsell D.N., Kuch M., Lumibao C., Poinar D., Pearson T., Fourment M., Golding B., Riehm J.M., Earn D.J., Dewitte S., Rouillard J.M., Grupe G., Wiechmann I., Bliska J.B., Keim P.S., Scholz H.C., Holmes E.C., Poinar H. Yersinia pestis and the plague of Justinian 541–543 AD: a genomic analysis. Lancet Infect. Dis. 2014; 14(4):319–26. DOI: 10.1016/S1473-3099(13)70323-2.
10. Feldman M., Harbeck M., Keller M., Spyrou M.A., Rott A., Trautmann B., Scholz H.C., Päffgen B., Peters J., McCormick M., Bos K., Herbig A., Krause J. A high-coverage Yersinia pestis genome from a sixth-century Justinianic Plague victim. Mol. Biol. Evol. 2016; 33(11):2911–23. DOI: 10.1093/molbev/msw170.
11. Keller M., Spyrou M.A., Scheib C.L., Neumann G.U., Kröpelin A., Haas-Gebhard B., Päffgen B., Haberstroh J., Ribera I Lacomba A., Raynaud C., Cessford C., Durand R., Stadler P., Nägele K., Bates J.S., Trautmann B., Inskip S.A., Peters J., Robb J.E., Kivisild T., Castex D., McCormick M., Bos K.I., Harbeck M., Herbig A., Krause J. Ancient Yersinia pestis genomes from across Western Europe reveal early diversification during the first pandemic (541–750). Proc. Natl. Acad. Sci. USA. 2019; 116(25):12363–72. DOI: 10.1073/pnas.1820447116.
12. Guelli M., Kersten O., Namouchi A., Luciani S., Marota I., Arcini C.A., Iregren E., Lindemann R.A., Warfvinge G. Bakanidze L., Bitadze L., Rubini M., Zaio P., Zaio M., Neri D., Stenseth N.C., Bramanti B. A genomic and historical synthesis of plague in 18th century Eurasia. Proc. Natl Acad. Sci. USA. 2020; 117(45):28328– 35. DOI: 10.1073/pnas.2009677117.
13. Onishchenko G.G., Kutyrev V.V., editors. [Laboratory Diagnostics of Particularly Dangerous Infectious Diseases]. Practice guidelines. Moscow: CJSC “Shiko”; 2013. 560 p.
14. Kado C.I., Liu S.-T. Rapid procedure for detection and isolation of large and small plasmids. J. Bacteriol. 1981; 145(3):1365– 73. DOI: 10.1128/JB.145.3.1365-1373.1981.
15. Odinokov G.N., Eroshenko G.A., Kukleva L.M., Shavina N.Yu., Krasnov Ya.M., Kutyrev V.V. [Determination of the genetic basis of auxotrophy in Yersinia pestis strains of subspecies caucasica]. Genetika [Genetics]. 2012; 48(4):457–64.
16. Plokhinsky N.A. [Biometrics]. Moscow: Publishing house of Moscow State University; 1970. 367 p.
17. Le Flèche P., Hauck Y., Onteniente L., Prieur A., Denoeud F., Ramisse V., Sylvestre P., Benson G., Ramisse F., Vergnaud G. A tandem repeats database for bacterial genomes: application to the genotyping of Yersinia pestis and Bacillus anthracis. BMC Microbiol. 2001; 1:2. DOI: 10.1186/1471-2180-1-2.
18. Rasmussen S., Allentoft M.E., Nielsen K., Orlando L., Sikora M., Sjögren K.G., Pedersen A.G., Schubert M., Van Dam A., Kapel C.M., Nielsen H.B., Brunak S., Avetisyan P., Epimakhov A., Khalyapin M.V., Gnuni A., Kriiska A., Lasak I., Metspalu M., Moiseyev V., Gromov A., Pokutta D., Saag L., Varul L., Yepiskoposyan L., Sicheritz-Pontén T., Foley R.A., Lahr M.M.., Nielsen R., Kristiansen K., Willerslev E. Early divergent strains of Yersinia pestis in Eurasia 5,000 years ago. Cell. 2015; 163(3):571– 82. DOI: 10.1016/j.cell.2015.10.009.
19. Andrades Valtueña A., Mittnik A., Key F.M., Haak W., Allmäe R., Belinskij A., Daubaras M., Feldman M., Jankauskas R., Janković I., Massy K., Novak M., Pfrengle S., Reinhold S., Šlaus M., Spyrou M.A., Szécsényi-Nagy A., Tõrv M., Hansen S., Bos K.I., Stockhammer P.W., Herbig A., Krause J. The Stone Age plague and its persistence in Eurasia. Curr. Biol. 2017; 27(23):3683–3691.e8. DOI: 10.1016/j.cub.2017.10.025.
20. Rascovan N., Sjögren K.G., Kristiansen K., Nielsen R., Willerslev E., Desnues C., Rasmussen S. Emergence and spread of basal lineages of Yersinia pestis during the neolithic decline. Cell. 2019; 176(1–2):295–305.e10. DOI: 10.1016/j.cell.2018.11.005.
21. Spyrou M.A. Tukhbatova R.I., Wang C.C., Valtueña A.A., Lankapalli A.K., Kondrashin V.V., Tsybin V.A., Khokhlov A., Kühnert D., Herbig A., Bos K.I., Krause J. Analysis of 3800-year-old Yersinia pestis genomes suggests Bronze Age origin for bubonic plague. Nat. Commun. 2018; 9(1):2234. DOI: 10.1038/s41467-018-04550-9.
22. Keller M., Spyrou M.A., McCormick M., Bos K.I., Herbig A., Krause J. Ancient Yersinia pestis genomes provide no evidence for the origins or spread of the Justinianic Plague. bioRxiv. 2019. DOI: 10.1101/819698.
23. de Barros Damgaard P., Marchi N., Rasmussen S., Peyrot M., Renaud G., Korneliussen T., Moreno-Mayar J.V., Pedersen M.W., Goldberg A., Usmanova E., Baimukhanov N., Loman V., Hedeager L., Pedersen A.G., Nielsen K., Afanasiev G., Akmatov K., Aldashev A., Alpaslan A., Baimbetov G., Bazaliiskii V.I., Beisenov A., Boldbaatar B., Boldgiv B., Dorzhu C., Ellingvag S., Erdenebaatar D., Dajani R., Dmitriev E., Evdokimov V., Frei K.M., Gromov A., Goryachev A., Hakonarson H., Hegay T., Khachatryan Z., Khaskhanov R., Kitov E., Kolbina A., Kubatbek T., Kukushkin A., Kukushkin I., Lau N., Margaryan A., Merkyte I., Mertz I.V., Mertz V.K., Mijiddorj E., Moiyesev V., Mukhtarova G., Nurmukhanbetov B., Orozbekova Z., Panyushkina I., Pieta K., Smrčka V., Shevnina I., Logvin A., Sjögren K.-G., Štolcová T., Taravella A.M., Tashbaeva K., Tkachev A., Tulegenov T., Voyakin D, Yepiskoposyan L., Undrakhbold S., Varfolomeev V., Weber A., Wilson Sayres M.A., Kradin N., Allentoft M.E., Orlando L., Nielsen R., Sikora M., Heyer E., Kristiansen K., Willerslev E. 137 ancient human genomes from across the Eurasian steppes. Nature. 2018; 557:369–74. DOI: 10.1038/s41586-018-0094-2.
Review
For citations:
Kukleva L.M., Dzhaparova A.K., Oglodin E.G., Naryshkina E.A., Krasnov Ya.M., Kuznetsov A.A., Fadeeva A.V., Eroshenko G.A., Berdiev S.K., Kutyrev V.V. Complex Characteristics of Yersinia pestis Strains Isolated in the Sarydzhaz and Upper-Naryn High-Mountain Foci in 2019–2020. Problems of Particularly Dangerous Infections. 2021;(2):114-122. (In Russ.) https://doi.org/10.21055/0370-1069-2021-2-114-122