microbeПроблемы особо опасных инфекцийProblems of Particularly Dangerous Infections0370-10692658-719XRussian Research Anti-Plague Institute “Microbe”10.21055/0370-1069-2023-2-13-28microbe-1817Research ArticleОБЗОРЫREVIEWSПалеогеномика возбудителя чумы и перспективы палеогеномных исследований на территории РоссииPaleogenomics of the Plague Agent and Prospects for Paleogenomic Studies in Russiahttps://orcid.org/0000-0001-5403-989XЕрошенкоГ. А.EroshenkoG. A.

410005, Саратов, ул. Университетская, 46.

46, Universitetskaya St., Saratov, 410005

rusrapi@microbe.ruhttps://orcid.org/0000-0002-5703-117XБатиеваЕ. Ф.BatievaE. F.

346780, Азов, Ростовская область, ул.Московская, 38/40

38/40, Moskovskaya St., Azov, Rostov region, 346780

azovmuzey-reserve@mail.ruhttps://orcid.org/0000-0003-3788-3452КутыревВ. В.KutyrevV. V.

410005, Саратов, ул. Университетская, 46.

46, Universitetskaya St., Saratov, 410005

rusrapi@microbe.ruФКУН «Российский научно-исследовательский противочумный институт «Микроб»РоссияRussian Research Anti-Plague Institute “Microbe”Russian FederationГБУК РО «Азовский историко-археологический и палеонтологический музей-заповедник имени А.А. Горбенко»РоссияAzov Historical-Archaeological and Paleontological Museum-Reserve named after A.A. GorbenkoRussian Federation202311072023021328Copyright © Ерошенко Г.А., Батиева Е.Ф., Кутырев В.В., 20232023Ерошенко Г.А., Батиева Е.Ф., Кутырев В.В.Eroshenko G.A., Batieva E.F., Kutyrev V.V.Данная работа распространяется под лицензией Creative Commons Attribution 4.0.This work is licensed under a Creative Commons Attribution 4.0 License.https://journal.microbe.ru/jour/article/view/1817

В обзоре собрана информация по палеогеномным исследованиям возбудителя чумы Yersinia pestis, охватывающим доисторическую эпоху, периоды первой и второй пандемий чумы, эпидемий и вспышек чумы конца XIX – XX в. Обобщены данные по реконструкции древних геномов Y. pestis периода позднего неолита, бронзового и железного веков, эпидемии «Юстинианова чума» первой пандемии чумы, эпидемии «Черная смерть» и последующих эпидемий второй пандемии чумы XIV–XVIII вв., а также по реконструкции путей распространения волн чумы в Евразии и направлений эволюции возбудителя чумы с формированием трансмиссивного пути передачи инфекции с помощью артропод. Приводятся результаты собственных исследований геномов Y. pestis из ключевых мест формирования этиологических агентов первой и второй пандемий чумы в горах Тянь-Шаня, исторических вспышек в Северном и Северо-Западном Прикаспии и других регионах России и сопредельных государств в конце XIX – XX в. Обсуждаются перспективные для проведения отечественных палеогеномных исследований чумы области Кавказа, Крыма, Северного Прикаспия, Сибири, Тянь-Шаня на территории России и сопредельных государств. 

The review contains information on paleogenomic studies of the plague pathogen, Yersinia pestis, covering the prehistoric epoch, the periods of the first and second plague pandemics, epidemics and outbreaks of plague of the late XIX–XX centuries. We have summarized the data on the reconstruction of ancient Y. pestis genomes of the Late Neolithic, Bronze and Iron Ages, the Justinian Plague epidemic of the first plague pandemic, the Black Death epidemic and the subsequent epidemics of the second plague pandemic of the XIV–XVIII centuries, as well as on tracing the pathways of plague propagation waves in Eurasia and the course of plague agent evolution with the formation of a vector-borne transmission route with the help of arthropods. We present the results of our own research of Y. pestis genomes from the key sites of formation of etiological agents of the first and second plague pandemics in the Tien Shan Mountains, historical outbreaks in the Northern and North-Western Caspian sea region and other regions of Russia and adjoining countries in the late XIX–XX centuries. The paper discusses the areas of the Caucasus, Crimea, Northern Caspian, Siberia, and Tien Shan in the territory of Russia and neighboring states that are promising for national paleogenomic studies of plague.

чумапалеогеномикагеномыреконструкцияplaguepaleogenomicsgenomesreconstructionReferencesBos K.I., Kühnert D., Herbig A., Esquivel-Gomez L.R., Andrades Valtueña A., Barquera R., Giffin K., Kumar Lankapalli A., Nelson E.A., Sabin S., Spyrou M.A., Krause J. Paleomicrobiology: diagnosis and evolution of ancient pathogens. Annu. Rev. Microbiol. 2019; 73:639–66. DOI: 10.1146/annurev-micro-090817-062436.Bos K.I., Kühnert D., Herbig A., Esquivel-Gomez L.R., Andrades Valtueña A., Barquera R., Giffin K., Kumar Lankapalli A., Nelson E.A., Sabin S., Spyrou M.A., Krause J. Paleomicrobiology: diagnosis and evolution of ancient pathogens. Annu. Rev. Microbiol. 2019; 73:639–66. DOI: 10.1146/annurev-micro-090817-062436.Rasmussen S., Allentoft M.E., Nielsen K., Orlando L., Sikora M., Sjögren K.-G., Pedersen A.G., Schubert S., 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.Rasmussen S., Allentoft M.E., Nielsen K., Orlando L., Sikora M., Sjögren K.-G., Pedersen A.G., Schubert S., 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.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.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.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):295–305e10. DOI: 10.1016/j.cell.2018.11.0054.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):295–305e10. DOI: 10.1016/j.cell.2018.11.0054.Mordechai L., Eisenberg M., Newfield T.P., Izdebski A., Kay J.E., Poinar H. The Justinianic Plague: An inconsequential pandemic? Proc. Natl Acad. Sci. USA. 2019; 116(51):25546–54. DOI: 10.1073/pnas.1903797116.Mordechai L., Eisenberg M., Newfield T.P., Izdebski A., Kay J.E., Poinar H. The Justinianic Plague: An inconsequential pandemic? Proc. Natl Acad. Sci. USA. 2019; 116(51):25546–54. DOI: 10.1073/pnas.1903797116.Stenseth N.C., Atshabar B.B., Begon M., Belmain S.R., Bertherat E., Carniel E., Gage K.L., Leirs H., Rahalison L. Plague: past, present, and future. PLoS Med. 2008; 5(1):e3. DOI: 10.1371/journal.pmed.0050003.Stenseth N.C., Atshabar B.B., Begon M., Belmain S.R., Bertherat E., Carniel E., Gage K.L., Leirs H., Rahalison L. Plague: past, present, and future. PLoS Med. 2008; 5(1):e3. DOI: 10.1371/journal.pmed.0050003.Bos K.I., Schuenemann V.J., Golding G.B., Burbano H.A., Waglechner N., Coombes B.K., McPhee J.B., DeWitte S.N., Meyer M., Schmedes S., Wood J., Earn D.J., Herring D.A., Bauer P., Poinar H.N., Krause J. A draft genome of Yersinia pestis from victims of the Black Death. Nature. 2011; 478(7370):506–10. DOI: 10.1038/nature10549.Bos K.I., Schuenemann V.J., Golding G.B., Burbano H.A., Waglechner N., Coombes B.K., McPhee J.B., DeWitte S.N., Meyer M., Schmedes S., Wood J., Earn D.J., Herring D.A., Bauer P., Poinar H.N., Krause J. A draft genome of Yersinia pestis from victims of the Black Death. Nature. 2011; 478(7370):506–10. DOI: 10.1038/nature10549.Andrades Valtueña A., Neumann G.U., Spyrou M.A., Musralina L., Aron F., Beisenov A., Belinskiy A.B., Bos K.I., Buzhilova A., Conrad M., Djansugurova L.B., Dobeš M., Ernée M., Fernández-Eraso J., Frohlich B., Furmanek M, Hałuszko A, Hansen S., Harney É., Hiss A.N., Hübner A., Key F.M., Khussainova E., Kitov E., Kitova A.O., Knipper C., Kühnert D., Lalueza-Fox C., Littleton J., Massy K., Mittnik A., Mujika-Alustiza J.A., Olalde I., Papac L., Penske S., Peška J., Pinhasi R., Reich D., Reinhold S., Stahl R., Stäuble H., Tukhbatova R.I., Vasilyev S., Veselovskaya E., Warinner C., Stockhammer P.W., Haak W., Krause J., Herbig A. Stone Age Yersinia pestis genomes shed light on the early evolution, diversity, and ecology of plague. Proc. Natl Acad. Sci. USA. 2022; 119(17):e2116722119. DOI: 10.1073/pnas.2116722119.Andrades Valtueña A., Neumann G.U., Spyrou M.A., Musralina L., Aron F., Beisenov A., Belinskiy A.B., Bos K.I., Buzhilova A., Conrad M., Djansugurova L.B., Dobeš M., Ernée M., Fernández-Eraso J., Frohlich B., Furmanek M, Hałuszko A, Hansen S., Harney É., Hiss A.N., Hübner A., Key F.M., Khussainova E., Kitov E., Kitova A.O., Knipper C., Kühnert D., Lalueza-Fox C., Littleton J., Massy K., Mittnik A., Mujika-Alustiza J.A., Olalde I., Papac L., Penske S., Peška J., Pinhasi R., Reich D., Reinhold S., Stahl R., Stäuble H., Tukhbatova R.I., Vasilyev S., Veselovskaya E., Warinner C., Stockhammer P.W., Haak W., Krause J., Herbig A. Stone Age Yersinia pestis genomes shed light on the early evolution, diversity, and ecology of plague. Proc. Natl Acad. Sci. USA. 2022; 119(17):e2116722119. DOI: 10.1073/pnas.2116722119.Eisen R.J., Bearden S.W., Wilder A.P., Montenieri J.A., Antolin M.F., Gage K.L. Early-phase transmission of Yersinia pestis by unblocked fleas as a mechanism explaining rapidly spreading plague epizootics. Proc. Natl Acad. Sci. USA. 2006; 103(42):15380–5. DOI: 10.1073/pnas.0606831103.Eisen R.J., Bearden S.W., Wilder A.P., Montenieri J.A., Antolin M.F., Gage K.L. Early-phase transmission of Yersinia pestis by unblocked fleas as a mechanism explaining rapidly spreading plague epizootics. Proc. Natl Acad. Sci. USA. 2006; 103(42):15380–5. DOI: 10.1073/pnas.0606831103.Bland D.M., Miarinjara A., Bosio C.F., Calarco J., Hinnebusch B.J. Acquisition of yersinia murine toxin enabled Yersinia pestis to expand the range of mammalian hosts that sustain flea-borne plague. PLoS Pathog. 2021; 17(10):e1009995. DOI: 10.1371/journal.ppat.1009995.Bland D.M., Miarinjara A., Bosio C.F., Calarco J., Hinnebusch B.J. Acquisition of yersinia murine toxin enabled Yersinia pestis to expand the range of mammalian hosts that sustain flea-borne plague. PLoS Pathog. 2021; 17(10):e1009995. DOI: 10.1371/journal.ppat.1009995.Slavin P., Sebbane F. Emergence and spread of ancestral Yersinia pestis in Late-Neolithic and Bronze-Age Eurasia, ca. 5,000 to 2,500 y B.P. Proc. Natl Acad. Sci. USA. 2022; 119(21):e2204044119.Slavin P., Sebbane F. Emergence and spread of ancestral Yersinia pestis in Late-Neolithic and Bronze-Age Eurasia, ca. 5,000 to 2,500 y B.P. Proc. Natl Acad. Sci. USA. 2022; 119(21):e2204044119.Dai R., Wei B., Xiong H., Yang X., Peng Y., He J., Jin J., Wang Y., Zha X., Zhang Z., Liang Y., Zhang Q., Xu J., Wang Z., Li W. Human plague associated with Tibetan sheep originates in marmots. PLoS Negl. Trop. Dis. 2018; 12(8):e0006635. DOI: 10.1371/journal.pntd.0006635.Dai R., Wei B., Xiong H., Yang X., Peng Y., He J., Jin J., Wang Y., Zha X., Zhang Z., Liang Y., Zhang Q., Xu J., Wang Z., Li W. Human plague associated with Tibetan sheep originates in marmots. PLoS Negl. Trop. Dis. 2018; 12(8):e0006635. DOI: 10.1371/journal.pntd.0006635.Susat J., Lübke H., Immel A., Brinker U., Macāne A., Meadows J., Steer B., Tholey A., Zagorska I., Gerhards G., Schmölcke U., Kalniņš M., Franke A., Pētersone-Gordina E., Teßman B., Tõrv M., Schreiber S., Andree C., Bērziņš V., Nebel A., Krause-Kyora B. A 5,000-year-old hunter-gatherer already plagued by Yersinia pestis. Cell Rep. 2021; 35(13):109278. DOI: 10.1016/j. celrep.2021.109278.Susat J., Lübke H., Immel A., Brinker U., Macāne A., Meadows J., Steer B., Tholey A., Zagorska I., Gerhards G., Schmölcke U., Kalniņš M., Franke A., Pētersone-Gordina E., Teßman B., Tõrv M., Schreiber S., Andree C., Bērziņš V., Nebel A., Krause-Kyora B. A 5,000-year-old hunter-gatherer already plagued by Yersinia pestis. Cell Rep. 2021; 35(13):109278. DOI: 10.1016/j. celrep.2021.109278.Yu H., Spyrou M.A., Karapetian M., Shnaider S., Radzevičiūtė R., Nägele K., Neumann G.U., Penske S., Zech J., Lucas M., LeRoux P., Roberts P., Pavlenok G., Buzhilova A., Posth C., Jeong C., Krause J. Paleolithic to Bronze Age Siberians reveal connections with first Americans and across Eurasia. Cell. 2020; 181(6):1232–1245.e20. DOI: 10.1016/j.cell.2020.04.037.Yu H., Spyrou M.A., Karapetian M., Shnaider S., Radzevičiūtė R., Nägele K., Neumann G.U., Penske S., Zech J., Lucas M., LeRoux P., Roberts P., Pavlenok G., Buzhilova A., Posth C., Jeong C., Krause J. Paleolithic to Bronze Age Siberians reveal connections with first Americans and across Eurasia. Cell. 2020; 181(6):1232–1245.e20. DOI: 10.1016/j.cell.2020.04.037.Zimbler D.L., Schroeder J.A., Eddy J.L., Lathem W.W. Early emergence of Yersinia pestis as a severe respiratory pathogen. Nat. Commun. 2015; 6:7487. DOI: 10.1038/ncomms8487.Zimbler D.L., Schroeder J.A., Eddy J.L., Lathem W.W. Early emergence of Yersinia pestis as a severe respiratory pathogen. Nat. Commun. 2015; 6:7487. DOI: 10.1038/ncomms8487.Kılınç G.M., Kashuba N., Koptekin D., Bergfeldt N., Dönertaş H.M., Rodríguez-Varela R., Shergin D., Ivanov G., Kichigin D., Pestereva K., Volkov D., Mandryka P., Kharinskii A., Tishkin A., Ineshin E., Kovychev E., Stepanov A., Dalén L., Günther T., Kırdök E., Jakobsson M., Somel M., Krzewińska M., Storå J., Götherström A. Human population dynamics and Yersinia pestis in ancient northeast Asia. Sci. Adv. 2021; 7(2):eabc4587. DOI: 10.1126/sciadv.abc4587.Kılınç G.M., Kashuba N., Koptekin D., Bergfeldt N., Dönertaş H.M., Rodríguez-Varela R., Shergin D., Ivanov G., Kichigin D., Pestereva K., Volkov D., Mandryka P., Kharinskii A., Tishkin A., Ineshin E., Kovychev E., Stepanov A., Dalén L., Günther T., Kırdök E., Jakobsson M., Somel M., Krzewińska M., Storå J., Götherström A. Human population dynamics and Yersinia pestis in ancient northeast Asia. Sci. Adv. 2021; 7(2):eabc4587. DOI: 10.1126/sciadv.abc4587.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.J., Krause J. Analysis of 3800-yearold Yersinia pestis genomes suggests Bronze Age origin for bubonic plague. Nat. Commun. 2018; 9(1):2234. DOI: 10.1038/s41467-018-04550-9.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.J., Krause J. Analysis of 3800-yearold Yersinia pestis genomes suggests Bronze Age origin for bubonic plague. Nat. Commun. 2018; 9(1):2234. DOI: 10.1038/s41467-018-04550-9.Chouikha I., Hinnebusch B.J. Silencing urease: a key evolutionary step that facilitated the adaptation of Yersinia pestis to the flea-borne transmission route. Proc. Natl Acad. Sci. USA. 2014; 111(52):18709–14. DOI: 10.1073/pnas.1413209111.Chouikha I., Hinnebusch B.J. Silencing urease: a key evolutionary step that facilitated the adaptation of Yersinia pestis to the flea-borne transmission route. Proc. Natl Acad. Sci. USA. 2014; 111(52):18709–14. DOI: 10.1073/pnas.1413209111.Sun Y.-C., Jarrett C.O., Bosio C.F., Hinnebusch B.J. Retracing the evolutionary path that led to flea-borne transmission of Yersinia pestis. Cell Host Microbe. 2014; 15(5):578–86. DOI: 10.1016/j.chom.2014.04.003.20.Sun Y.-C., Jarrett C.O., Bosio C.F., Hinnebusch B.J. Retracing the evolutionary path that led to flea-borne transmission of Yersinia pestis. Cell Host Microbe. 2014; 15(5):578–86. DOI: 10.1016/j.chom.2014.04.003.20.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.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.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.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.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-сoverage Yersinia pestis genome from a sixth-century Justinianic Plague victim. Mol. Biol. Evol. 2016; 33(11):2911–23. DOI: 10.1093/molbev/msw170.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-сoverage Yersinia pestis genome from a sixth-century Justinianic Plague victim. Mol. Biol. Evol. 2016; 33(11):2911–23. DOI: 10.1093/molbev/msw170.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.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.Damgaard P.B., 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(7705):369–74. DOI: 10.1038/s41586-018-0094-2.Damgaard P.B., 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(7705):369–74. DOI: 10.1038/s41586-018-0094-2.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.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.Spyrou M.A., Musralina L., Gnecchi Ruscone G.A., Kocher A., Borbone P.G., Khartanovich V.I., Buzhilova A., Djansugurova L., Bos K.I., Kühnert D., Haak W., Slavin P., Krause J. The source of the Black Death in fourteenth-century central Eurasia. Nature. 2022; 606(7915):718–24. DOI: 10.1038/s41586-022-04800-3.Spyrou M.A., Musralina L., Gnecchi Ruscone G.A., Kocher A., Borbone P.G., Khartanovich V.I., Buzhilova A., Djansugurova L., Bos K.I., Kühnert D., Haak W., Slavin P., Krause J. The source of the Black Death in fourteenth-century central Eurasia. Nature. 2022; 606(7915):718–24. DOI: 10.1038/s41586-022-04800-3.Хвольсон Д. Несторианские надписи из Семиречья. В кн.: Записки Восточного отделения Императорского Русского Археологического общества. Т. I. 1886. СПб.: Тип. Имп. Академии Наук; 1887. С. 217–21.Khvol’son D. Nestorian inscriptions from Semirechye. In: [Notes of the Eastern Branch of the Imperial Russian Archaeological Society]. Vol. I. 1886. St. Petersburg: Publiching House of the Imperial Academy of Sciences; 1887. P. 217–21.Пенской В.В., Липич В.В., Реутов Н.Н., Артюх А.В. «Бысть мор зол…»: «Черная смерть» XIV века на Руси. Проблемы социальной гигиены, здравоохранения и истории медицины. 2021; 29(4):1017–24. DOI: 10.32687/0869-866X-2020-29-4-1017-1024.Penskoy V.V., Lipich V.V., Reutov N.N., Artyukh A.V. “Be the pestilence...”: “Black Death” of the XIV century in Rus. Problemy Sotsial’noy Gigiyeny, Zdravookhraneniya i Istorii Meditsiny [Problems of Social Hygiene, Public Health and the History of Medicine]. 2021; 29(4):1017–24. DOI: 10.32687/0869-866X-2020-29-4-1017-1024.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.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.Schmid B.V., Büntgen U., Easterday W.R., Ginzler C., Walløe L., Bramanti B., Stenseth N.C. Climate-driven introduction of the Black Death and successive plague reintroductions into Europe. Proc. Natl Acad. Sci. USA. 2015; 112(10):3020–5. DOI: 10.1073/pnas.1412887112 35.Schmid B.V., Büntgen U., Easterday W.R., Ginzler C., Walløe L., Bramanti B., Stenseth N.C. Climate-driven introduction of the Black Death and successive plague reintroductions into Europe. Proc. Natl Acad. Sci. USA. 2015; 112(10):3020–5. DOI: 10.1073/pnas.1412887112 35.Namouchi A., Guellil M., Kersten O., Hänsch S., Ottoni C., Schmid B.V., Pacciani E., Quaglia L., Vermunt M., Egil L. Bauer E.L., Derrick M., Jensend A.Ø., Kacki S., Cohn S.K. Jr, Stenseth N.C., Bramanti B. Integrative approach using Yersinia pestis geno­ mes to revisit the historical landscape of plague during the Medieval Period. Proc. Natl Acad. Sci. USA. 2018; 115(50):E11790-E11797. DOI: 10.1073/pnas.1812865115.Namouchi A., Guellil M., Kersten O., Hänsch S., Ottoni C., Schmid B.V., Pacciani E., Quaglia L., Vermunt M., Egil L. Bauer E.L., Derrick M., Jensend A.Ø., Kacki S., Cohn S.K. Jr, Stenseth N.C., Bramanti B. Integrative approach using Yersinia pestis geno­ mes to revisit the historical landscape of plague during the Medieval Period. Proc. Natl Acad. Sci. USA. 2018; 115(50):E11790-E11797. DOI: 10.1073/pnas.1812865115.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.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.Guellil 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.Guellil 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.Spyrou M.A., Keller M., Tukhbatova R.I., Scheib C.L., Nelson E.A., Andrades Valtueña A., Neumann G.U., Walker D., Alterauge A., Carty N., Cessford C., Fetz H., Gourvennec M., Hartle R., Henderson M., von Heyking K., Inskip S.A., Kacki S., Key F.M., Knox E.L., Later C., Maheshwari-Aplin P., Peters J., Robb J.E., Schreiber J., Ki-visild T., Castex D., Lösch S., Harbeck M., Herbig A., Bos K.I., Krause J. Phylogeography of the second plague pandemic revealed through analysis of historical Yersinia pestis genomes. Nat. Commun. 2019; 10(1):4470. DOI: 10.1038/s41467-019-12154-0.Spyrou M.A., Keller M., Tukhbatova R.I., Scheib C.L., Nelson E.A., Andrades Valtueña A., Neumann G.U., Walker D., Alterauge A., Carty N., Cessford C., Fetz H., Gourvennec M., Hartle R., Henderson M., von Heyking K., Inskip S.A., Kacki S., Key F.M., Knox E.L., Later C., Maheshwari-Aplin P., Peters J., Robb J.E., Schreiber J., Ki-visild T., Castex D., Lösch S., Harbeck M., Herbig A., Bos K.I., Krause J. Phylogeography of the second plague pandemic revealed through analysis of historical Yersinia pestis genomes. Nat. Commun. 2019; 10(1):4470. DOI: 10.1038/s41467-019-12154-0.Попова А.Ю., Кутырев В.В., редакторы. Атлас природных очагов чумы России и зарубежных государств. Калининград: РА Полиграфычъ; 2022. 348 с.Popova A.Yu., Kutyrev V.V., editors. [Atlas of Natural Foci of Plague in Russia and Foreign Countries]. Kaliningrad: “Poligrafych”; 2022. 348 p.Ефременко В.И., Таран И.Ф., Антоненко А.Д. Черная смерть и ее укротители: (Очерки истории чумы на Кавказе). Ставрополь; 2000.Efremenko V.I., Taran I.F., Antonenko A.D. [Black Death and Its Tamers: (Essays on the history of plague in the Caucasus)]. Stavropol; 2000.Супотницкий М.В., Супотницкая Н.С. Очерки истории чумы: в 2 кн. М.: Вузовская книга; 2006. 1119 с.Supotnitsky M.V., Supotnitskaya N.S. [Essays on the History of Plague: in 2 books]. M.: “University book”; 2006. 1119 p.Палеев Ф.Н., Оноприенко Г.А., Молочков А.В. Эпидемия чумы XVIII века и развитие здравоохранения в Москве. Альманах клинической медицины. 2015; 37:6–9.Paleev F.N., Onoprienko G.A., Molochkov A.V. [Plague epidemic of the 18th century and the development of health care in Moscow]. Al’manakh Klinicheskoy Meditsiny [Almanac of Clinical Medicine]. 2015; (37):6–9.Morozova I., Kasianov A., Bruskin S., Neukamm J., Molak M., Batieva E., Pudło A., Rühli F.J. Schuenemann V.J. New ancient Eastern European Yersinia pestis genomes illuminate the dispersal of plague in Europe. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2020; 375(1812):20190569. DOI: 10.1098/rstb.2019.0569.Morozova I., Kasianov A., Bruskin S., Neukamm J., Molak M., Batieva E., Pudło A., Rühli F.J. Schuenemann V.J. New ancient Eastern European Yersinia pestis genomes illuminate the dispersal of plague in Europe. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2020; 375(1812):20190569. DOI: 10.1098/rstb.2019.0569.Хайдаров Т.Ф. Латинские и арабские источники об эпидемии чумы в Крыму в 1346–1347 гг. Ученые записки Крымского федерального университета им. В.И. Вернадского. Серия «Исторические науки». 2016; 2(4):128–32.Khaidarov T.F. [Latin and Arabic sources on the plague epidemic in the Crimea in 1346–1347]. Scientific notes of the Crimean Federal University named after V.I. Vernadsky. Historical Sciences Series. 2016; 2(4):128–32.Wheelis M. Biological warfare at the 1346 siege of Caffa. Emerg. Infect. Dis. 2002; 8(9):971–5. DOI: 10.3201/eid0809.010536.Wheelis M. Biological warfare at the 1346 siege of Caffa. Emerg. Infect. Dis. 2002; 8(9):971–5. DOI: 10.3201/eid0809.010536.Попова А.Ю., Кутырев В.В., редакторы. Кадастр эпидемиологических и эпизоотических проявлений чумы на территории Российской Федерации и стран ближнего зарубежья (с 1876 по 2016 год). Саратов: ООО «Амирит»; 2016. 248 с.Popova A.Yu., Kutyrev V.V., editors. [Cadastre of Epidemiological and Epizootic Manifestations of Plague in the Territory of the Russian Federation and Former Soviet Union (1876–2016)]. Saratov: “Amirit” LLC; 2016. 248 p.Hashemi Shahraki A., Carniel E., Mostafavi E. Plague in Iran: its history and current status. Epidemiol. Health. 2016; 38:e2016033. DOI: 10.4178/epih.e2016033.Hashemi Shahraki A., Carniel E., Mostafavi E. Plague in Iran: its history and current status. Epidemiol. Health. 2016; 38:e2016033. DOI: 10.4178/epih.e2016033.Eroshenko G.A., Popov N.V., Al’khova Z.V., Kukleva L.M., Balykova A.N., Chervyakova N.S., Naryshkina E.A., Kutyrev V.V. Evolution and circulation of Yersinia pestis in the Northern Caspian and Northern Aral Sea regions in the 20th-21st centuries. PLoS One. 2021; 16(2):e0244615. DOI: 10.1371/journal.pone.0244615.Eroshenko G.A., Popov N.V., Al’khova Z.V., Kukleva L.M., Balykova A.N., Chervyakova N.S., Naryshkina E.A., Kutyrev V.V. Evolution and circulation of Yersinia pestis in the Northern Caspian and Northern Aral Sea regions in the 20th-21st centuries. PLoS One. 2021; 16(2):e0244615. DOI: 10.1371/journal.pone.0244615.Balykova A.N., Kukleva L.M., Naryshkina E.A., Eroshenko G.A., Kutyrev V.V. Five draft genome sequences of historical Yersinia pestis strains of phylogroups 2.MED4 and 2.MED1 of the medieval biovar. Microbiol. Resour. Announc. 2022; 1(5):e0004422. DOI: 10.1128/mra.00044-22.Balykova A.N., Kukleva L.M., Naryshkina E.A., Eroshenko G.A., Kutyrev V.V. Five draft genome sequences of historical Yersinia pestis strains of phylogroups 2.MED4 and 2.MED1 of the medieval biovar. Microbiol. Resour. Announc. 2022; 1(5):e0004422. DOI: 10.1128/mra.00044-22.

The authors declare that there are no conflicts of interest present.