Phylogenetic Analysis of Yersinia pestis Strains of Medieval Biovar, Isolated in Precaspian North-Western Steppe Plague Focus in the XX Century
https://doi.org/10.21055/0370-1069-2019-2-55-61
Abstract
Objective of the study – comparative phylogenetic analysis of Yersinia pestis strains, isolated in Precaspian North-Western steppe focus in 1924–1926, 1972, and 1986–1990 to understand the causes of focal reactivation during different time periods of the XX century.
Materials and methods. The work included 30 strains of Yersinia pestis from Precaspian North-Western steppe natural focus and adjacent plague foci. Whole genome sequencing of eight Y. pestis strains from the former was carried out. Also whole-genome sequences of 16 strains from neighboring natural foci were used. Whole-genome sequencing of Y. pestis strains was conducted in Ion PGM system (Life technologies). SNPs search across the core genome was performed using software package Wombac 2.0. Tree diagram Maximum Likelihood, HKU85 model, was constructed to analyze phylogenetic relations.
Results and discussion. It is established that in early XX century (1924–1926), strains of phylogenetic branches 2.MED4 and 2.MED1, belonging to medieval biovar, main subspecies, circulated on Ergenin Upland in the Precaspian North-Western steppe natural focus. Later on they became extinct in the territory. It is shown that the strains, isolated on Ergenin Upland in 1972, constituted a common subcluster on the dendrogram with the strains from low-mountain and piedmont plague foci of Caucasus and Transcaucasia, dated the same time period. It was inferred that epizootic manifestations on Ergenin upland in 1972, after a long recess since 1938, were caused by importation of Y. pestis strains from low-mountain natural plague foci of Caucasus and Transcaucasia. It was noted that expansion of Caucasian strains was of short-term character, and plague infected animals have not been found on Ergenin Upland since 1974 (including modern period). It is established that Y. pestis strains isolated in the eastern part of Precaspian North-Western steppe focus between 1986 and 1990, do not have close genetic relation to the strains that circulated on Ergenin Upland in 1924–1926 and 1972. It is determined that each epizootic period (1913–1938 and 1972–1973) in Precaspian North-Western steppe natural focus culminated in the elimination of the circulating Y. pestis strains and rehabilitation of the focal territory.
About the Authors
G. A. EroshenkoRussian Federation
46, Universitetskaya St., Saratov, 410005
N. V. Popov
Russian Federation
46, Universitetskaya St., Saratov, 410005
Zh. V. Al’khova
Russian Federation
46, Universitetskaya St., Saratov, 410005
A. N. Balykova
Russian Federation
46, Universitetskaya St., Saratov, 410005
L. M. Kukleva
Russian Federation
46, Universitetskaya St., Saratov, 410005
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]. M.: “Meditsina”; 2004. 192 p.
2. Popov N.V. [Discreteness – main spatial-temporal feature of plague manifestations in the foci of souslik type]. Saratov: Saratov State University Publishing House; 2002. 189 p.
3. Gage K.L., Kosoy M.Y. Natural history of plague: perspective from more than a century of research. Annu. Rev. Entomol. 2005; 50:505–28. DOI: 10.1146/annurev.ento.50.071803.130337
4. Bocharnikov O.N., Karpuzidi K.S., Klimchenko I.Z., TerVartanov V.N., Tinker I,S., Shishkin A.K., Shiryaev D.T. [Experience in eradication of plague epizooty in the Precaspian North-Western Focus]. In: [Natural Focality and Epidemiology of Particularly Dangerous Infectious Diseases]. Saratov; 1959. P. 235–46.
5. Kalabukhov N.I. [Phenomenon of long-term recesses in epizootic activity of natural plague foci and its possible causes]. Zoologichesky Zhurnal [Zoological Journal]. 1969; 48: 165–175.
6. Lavrovsky A.A., Varshavsky S.N., Gerasimova N.G., et all. [Plague epizooties among the little souslik in natural Precaspian North-Western Focus in 1972–1973]. Problemy Osobo Opasnykh Infektsii [Problems of Particularly Dangerous Infections]. 1974; 3:5–17.
7. Devignat R. Variétés de l’espèce Pasteurella pestis. Nouvelle hypothèse. Bull. World Health Organ. 1951; 4(2):241–63. PMCID: PMC2554099. PMID: 14859080.
8. Achtman M., Zurth K., Morelli G., Torrea G., Guiyoule A., Carniel E. Yersinia pestis, the cause of plague, is a recently emerged clone of Yersinia pseudotuberculosis. Proc. Natl. Acad. Sci. USA. 1999; 96(24):14043–8. DOI: 10.1073/pnas.96.24.14043.
9. Li Y., Cui Y., Hauck Y., Platonov M.E., Dai E., Song Y., Guo Z., Pourcel C., Dentovskaya S.V., Anisimov A.P., Yang R., Vergnaud G.. Genotyping and phylogenetic analysis of Yersinia pestis by MLVA: Insights into the worldwide expansion of Central Asia plague foci. PloS ONE. 2009; 4(6):e6000. DOI: 10.1371/journal.pone.0006000.
10. Morelli G., Song Y., Mazzoni C.J., Eppinger M., Roumagnac P., Wagner D.M., Feldkamp M., Kusecek B., Vogler A.J., Li Y., Cui Y., Thomson N.R., Jombart T., Leblois R., Lichtner P., Rahalison L., Petersen J.M., Balloux F., Keim P., Wirth T., Ravel J., Yang R., Carniel E., Achtman M. Yersinia pestis genome sequencing identifies patterns of global phylogenetic diversity. Nat. Genet. 2010; 42(12):1140–3. DOI: 10.1038/ng.705.
11. Cui Y., Yu C., Yan Y., Li D., Li Y., JombartT., Weinert L.A., 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 mutation rate in an epidemic pathogen, Yersinia pestis. Proc. Natl. Acad. Sci. USA. 2013; 110(2):577–82. DOI: 10.1073/pnas.1205750110.
12. 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.
13. Demeure C.E., Dussurget O., Fiol G.M., Le Guern A.-S., Savin C., Pizarro-Cerdá J. Yersinia pestis and plague: an updated view on evolution, virulence determinants, immune subversion, vaccination, and diagnostics. Genes Immun. 20(5):357–70. DOI: 10.1038/s41435-019-0065-0.
14. Spyrou M. A., Tukhbatova, R. I., Feldman, M., Drath, J., Kacki, S., Beltrán de Heredia J., Arnold S., Sitdikov A.G., Castex D., Wahl J., Gazimzyanov I.R., Nurgaliev D.K., Herbig A., Bos K.I., Krause J. Historical Y. pestis genomes reveal the European Black Death as the source of ancient and modern plague pandemics. Cell Host Microbe. 2016; 19(6):874–81. DOI: 10.1016/j. chom.2016.05.012.
15. Seifert L., Wiechmann I., Harbeck M., Thomas A., Grupe G., Projahn M., Scholz H.C., Riehm J.M. Genotyping Yersinia pestis in historical plague: evidence for long-term persistence of Y. pestis in Europe from the 14th to the 17th century. PloS ONE. 2016; 11(1):e0145194. DOI: 10.1371/journal.pone.0145194.
16. Bos K.I., Herbig A., Sahl J., Waglechner N., Fourment M., Forrest S.A., Klunk J., Schuenemann V.J., Poinar D., Kuch M., Golding G.B., Dutour O., Keim P., Wagner D.M., Holmes E.C., Krause J., Poinar H.N. Eighteenth century Yersinia pestis genomes reveal the long-term persistence of an historical plague focus. Elife. 2016; 5:e12994. DOI: 10.7554/eLife.12994.
17. Zharinova N.V., Bryukhanova G.D., Eremenko E.I., Bryukhanov A.F., Beyer A.P., Tsareva N.S., Zaitsev A.A. [ Properties of plague microbe strains, circulating in Central-Caucasian highmountain natural plague focus]. In: [Relevant Issues of Epidemiology and Prophylaxis of Infectious Diseases]. Samara; 2004. Vol. 2. P. 14.
18. Onishchenko G.G., Kutyrev V.V., editors. [Laboratory Diagnostics of Particularly Dangerous Infectious Diseases]. M.: “Shiko”; 2013. 560 p.
19. Darriba D., Taboada G.L., Doallo R., Posada D. jModelTest 2: more models, new heuristics and parallel computing. Nature Methods. 2012; 9(8):772. DOI: 10.1038/nmeth.2109.
Review
For citations:
Eroshenko G.A., Popov N.V., Al’khova 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. Problems of Particularly Dangerous Infections. 2019;(2):55-61. (In Russ.) https://doi.org/10.21055/0370-1069-2019-2-55-61