Ecological scenario of the plague microbe Yersinia pestis speciation underlying adequate molecular evolutionary model

Cover Page

Cite item

Full Text

Abstract

It is known that the psychrophilic pseudotuberculosis microbe serotype 1 (Y. pseudotuberculosis 0:1b) causing Far East scarlet-like fever (FESLF) — an intestinal infection found in a wide range of invertebrates and vertebrates inhabiting cold regions in the Northern and Central Asia as well as Far East is direct ancestor of the plague causative agent Yersinia pestis. However, the mechanism of Y. pestis speciation remains poorly elucidated. Numerous Y. pestis phylogenies created by using molecular genetic (MG) technologies are largely contradictory, being not in line with reliable data obtained by natural science approaches (e.g., ecology, epizootology, biogeography, and paleontology), which disagree with current evolutionary doctrine (synthetic theory of evolution). The MG approach provides no definitive answer to the questions of where, when, how, and under what circumstances the species Y. pestis arose. One of the reasons for such situation might be due to inadequacy of using the molecular evolutionary model for Y. pestis phylogenetics. Knowledge of the life cycles for the ancestral pseudotuberculosis and derivative plague microbes as well as related unique environmental features allows to create a reliable ecological model for the plague microbe evolution to be further used for assessing patterns of molecular variability and building proper molecular model that might be accepted for MG-reconstruction of plague microbe history. According to the ecological model, the species Y. pestis was formed in a tritopic manner (almost) simultaneously from FESLF clones (populations) in the three geographical populations of the Mongolian marmot-tarbagan (Marmota sibirica) and the flea Oropsylla silantiewi parasitizing on it. The inducer of speciation was coupled to the last maximum (Sartan) cooling in Central Asia occurred 22–15 thousand years ago. Soil cooling and deep freezing resulted in altered behavior of the marmot flea larvae with emergence of facultative hematophagy, which, in turn, led to a unique traumatic (compared to routine alimentary) infection route of sleeping marmots with FESLF and, as a result, a unique way of Y. pestis speciation. The molecular model should predict a Y. pestis peripatric tritope speciation, existing numerous parallelisms in intraspecific variability associated with tritope speciation, and the quantum principle of speciation in the highly variable heterothermic (heteroimmune) stressful marmot-flea (Marmota sibirica — Oropsylla silantiewi) host-vector environment involving stress-induced mutagenesis. Such molecular model of evolution may be useful for improving molecular methodology of phylogenetic constructions for a wide range of parasitic microorganisms.

About the authors

V. V. Suntsov

A.N. Severtsov Institute of Problems of Ecology and Evolution of Russian Academy of Science

Author for correspondence.
Email: vvsuntsov@rambler.ru

PhD, MD (Biology), Leading Researcher, Laboratory of Population Ecology

Russian Federation, Moscow

References

  1. Балахонов С.В., Ярыгина М.Б., Гладких А.С., Миронова Л.В., Феранчук С.И., Бочалгин Н.О., Рождественский Е.Н., Витязева С.А., Нацагдорж Б., Цэрэнноров Д., Цогбадрах Н., Косилко С.А., Корзун В.М. Молекулярно-генетическая характеристика штаммов Yersinia pestis, выделенных на монгольской территории трансграничного Сайлюгемского природного очага чумы // Проблемы особо опасных инфекций. 2019. № 3. С. 34–42. [Balakhonov S.V., Yarygina M.B., Gladkikh A.S., Mironova L.V., Feranchuk S.I., Bochalgin N.O., Rozhdestvensky E.N., Vityazeva S.A., Natsagdorzh B., Tserennorov D., Tsogbadrakh N., Kosilko S.A., Korzun V.M. Molecular-genetic characteristics of Yersinia pestis strains isolated in the mongolian territory of transboundary Sailyugem natural plague focus. Problemy osobo opasnykh infektsii = Problems of Particularly Dangerous Infections, 2019, no. 3, pp. 34–42. (In Russ.)] doi: 10.21055/0370-1069-2019-3-34-42
  2. Банников А.Г. Млекопитающие Монгольской Народной Республики. М.: Изд-во АН СССР, 1954. 670 с. [Bannikov A.G. Mammals of Mongol People Republic. Moscow: Acad. Sci. USSR, 1954. 670 p. (In Russ.)]
  3. Ерошенко Г.А., Попов Н.В., Краснов Я.М., Никифоров К.А., Кузнецов А.А., Матросов А.Н., Кутырев В.В. Природный мегаочаг основного подвида Yersinia pestis античного биовара филогенетической ветви 4.ANT в Горном Алтае // Проблемы особо опасных инфекций. 2018. № 2. С. 49–56. [Eroshenko G.A., Popov N.V., Krasnov Y.M., Nikiforov K.A., Kuznetsov A.A., Matrosov A.N., Kutyrev V.V. Natural mega-focus of Yersinia pestis main subspecies, antique biovar, phylogenetic line 4.ANT in Gorny Altai. Problemy osobo opasnykh infektsii = Problems of Particularly Dangerous Infections, 2018, no. 2, pp. 49–56. (In Russ.)] doi: 10.21055/0370-1069-2018-2-49-56
  4. Куклева Л.М., Шавина Н.Ю., Одиноков Г.Н., Оглодин Е.Г., Носов Н.Ю., Виноградова Н.А., Гусева Г.А., Ерошенко Г.А., Кутырев В.В. Анализ разнообразия и определение геновариантов штаммов возбудителя чумы из очагов Монголии // Генетика. 2015. Т. 51, № 3. С. 298–305. [Kukleva L.M., Shavina N.Yu., Odinokov G.N., Oglodin E.G., Nosov N.Yu., Vinogradova N.A., Guseva N.P., Eroshenko G.A., Kutyrev V.V. Analysis of diversity and identification of the genovariants of plague agent strains from mongolian foci. Genetika = Genetics, 2015, vol. 51, no. 3, pp. 298–305. (In Russ.)]
  5. Кучерук В.В. Вопросы палеогенезиса природных очагов чумы в связи с историей фауны грызунов // Фауна и экология грызунов. 1965. № 7. С. 5–86. [Kucheruk V.V. Issues of paleogenesis of natural foci of plague in connection with the history of the rodent fauna. Fauna i ekologiya gryzunov = Fauna and Ecology of Rodents, 1965, no. 7, pp. 5–86. (In Russ.)]
  6. Павлова А.И., Ерошенко Г.А., Одиноков Г.Н., Куклева Л.М., Шавина Н.Ю., Краснов Я.М., Кутырев В.В. Анализ генетической изменчивости штаммов Yersinia pestis средневекового биовара из природных очагов чумы России и Монголии // Проблемы особо опасных инфекций. 2012. № 114. С. 49–53. [Pavlova A.I., Eroshenko G.A., Odinokov G.N., Koukleva L.M., Shavina N.Yu., Krasnov Ya.M., Kutyrev V.V. Analysis of genetic variability of Yersinia pestis strains (medieval biovar) isolated in natural plague foci of the Russian Federation and Mongolia. Problemy osobo opasnykh infektsii = Problems of Particularly Dangerous Infections, 2012, no. 114, pp. 49–53. (In Russ.)]
  7. Ралль Ю.М. Природная очаговость и эпизоотология чумы. М.: Медицина, 1965. 363 с. [Rall’ Yu.M. Natural focility and epizootologe of plague. Moscow: Medicina, 1965. 363 p. (In Russ.)]
  8. Сомов Г.П. Дальневосточная скарлатиноподобная лихорадка. М.: Медицина, 1979. 184 с. [Somov G.P. Far Eastern scarlet-like fever. Moscow: Medicina, 1979. 184 p. (In Russ.)]
  9. Сунцов В.В. Исключительная роль специфической блохи сурков Oropsylla silantiewi (Ceratophyllidae: Siphonaptera) в видообразовании микроба чумы Yersinia pestis // Паразитология. 2018. Т. 52, № 1. С. 3–18. [Suntsov V.V. The exceptional role of the specific marmot flea Oropsylla silantiewi (Ceratophyllidae: Siphonaptera) in the speciation of the plague microbe Yersinia pestis. Parazitologiya = Parazitologiya, 2018, vol. 1, pp. 3–18. (In Russ.)]
  10. Сунцов В.В. Политопное видообразование микроба чумы Yersinia pestis как причина филогенетической трихотомии в географических популяциях монгольского сурка-тарбагана (Marmota sibirica) // Журнал общей биологии. 2021. Т. 82, № 6. С. 431–444. [Suntsov V.V. Polytopic speciation of the plague microbe Yersinia pestis as a cause of phylogenetic trichotomy in geographical populations of the Mongolian marmot-tarbagan (Marmota sibirica). Zhurnal obshchei biologii = Biology Bulletin Reviews, 2021, vol. 82, no. 6, pp. 431–444. (In Russ.)] doi: 10.31857/S0044459621060075
  11. Сунцов В.В., Сунцова Н.И. Чума. Происхождение и эволюция эпизоотической системы (экологические, географические и социальные аспекты). М.: КМК, 2006. 247 с. [Suntsov V.V., Suntsova N.I. The plague. Origin and evolution of epizootic system (ecological, geographical and social aspects). Moscow: KMK, 2006. 247 p. (In Russ.)]
  12. Achtman M., Morelli G., Zhu P.,Wirth T., Diehl I., Kusecek B., Vogler A.J., Wagner D.M., Allender C.J., Easterday W.R., Chenal-Francisque V., Worsham P., Thomson N.R., Parkhill J., Lindler L.E., Carniel E., Keim P. Microevolution and history of the plague bacillus, Yersinia pestis. PNAS, 2004, vol. 101, no. 51, pp. 17837–17842. doi: 10.1073pnas.0408026101
  13. 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. PNAS, 1999, vol. 96, no. 24, pp. 14043–14048. doi: 10.1073/pnas.96.24.14043
  14. Bouma H.R., Carey H.V., Kroese F.G.M. Hibernation: the immune system at rest? J. Leukoc. Biol., 2010, vol. 88, pp. 619–624. doi: 10.1189/jlb.0310174
  15. Brandler O. Molecular diversity and taxonomy in marmots. Marmots of the old and new world: Proceed. 7th Intern. Conf. on the Genus Marmota. Ulan-Bator, 2018, pp. 97–104.
  16. Cui Y., Yu C., Yan Y., Li D., Li Y., Jombart T., 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. PNAS, 2013, vol. 110, no. 2, pp. 577–582. doi: 10.1073/pnas.1205750110
  17. 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., 2019, vol. 20, no. 5, pp. 357–370. doi: 10.1038/s41435-019-0065-0
  18. Fukushima H., Gomyoda M., Hashimoto N., Takashima I., Shubin F.N., Isachikova L.M., Paik I.K., Zheng X.B. Putative origin of Yersinia pseudotuberculosis in western and eastern countries. A comparison of restriction endonuclease analysis of virulence plasmids. Int. J. Med. Microbiol., 1998, vol. 288, pp. 93–102. doi: 10.1016/s0934-8840(98)80105-9
  19. Fukushima H., Matsuda Y., Seki R., Tsubokura M., Takeda N., Shubin F.N., Paik I.K., Zheng X.B. Geographical heterogeneity between Far Eastern and Western countries in prevalence of the virulence plasmid, the superantigen Yersinia pseudotuberculosis-derived mitogen, and the high-pathogenicity island among Yersinia pseudotuberculosis strains. J. Clin. Microbiol., 2001, vol. 39, no. 10, pp. 3541–3547. doi: 10.1128/JCM.39.10.3541–3547.2001
  20. Kutyrev V.V., Eroshenko G.A., Motin V.L., Nosov N.Y., Krasnov J.M., Kukleva L.M., Nikiforov K.A., Al’kova Z.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, vol. 9: 1106. doi: 10.3389/fmicb.2018.01106
  21. 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., Rave J., Yang R., Carniel E., Achtman M. Yersinia pestis genome sequencing identifies patterns of global phylogenetic diversity. Nature Genetics, 2010, vol. 42, no. 12, pp. 1140–1145. doi: 10.1038/ng.705
  22. Octavia S., Lan R. The family Enterobacteriaceae. The prokaryotes. Eds.: Rosenberg E., DeLong E.F., Lory S., Stackebrandt E., Thompson F. Berlin; Heidelberg: Springer, 2014, pp. 225–286.
  23. Owen L.A., Richards B., Rhodes E.J., Cunningham W.D., Windley B.F., Badamgarav J., Dorjnamjaa D. Relict permafrost structures in the Gobi of Mongolia: age and significance. J. Quaternary Sci., 1998, vol. 13, no. 6, pp. 539–547.
  24. Pisarenko S.V., Evchenko A.Yu., Kovalev D.A.,Evchenko Y.M., Bobrysheva O.V., Shapakov N.A., Volynkina A.S., Kulichenko A.N. Yersinia pestis strains isolated in natural plague foci of Caucasus and Transcaucasia in the context of the global evolution of species. Genomics, 2021, vol. 113, pp. 1952–1961. doi: 10.1016/j.ygeno.2021.04.021
  25. Prendergast B.J., Freeman D.A., Zucker I., Nelson R.J. Periodic arousal from hibernation is necessary for initiation of immune responses in ground squirrels. Am. J. Physiol. Regul. Integr. Comp. Physiol., 2002, vol. 282, no. 4, pp. 1054–1062. doi: 10.1152/ajpregu.00562.2001
  26. Rascovan N., Sjogren 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, no. 176, pp. 295–305. doi: 10.1016/j.cell.2018.11.005
  27. Rasmussen S., Allentoft M.E., Nielsen K.,Orlando L., Sikora M., Sjogren K.-G., Pedersen A.G., Schubert M., Dam A.V., Kapel C.M.O., 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-Ponte 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, no. 163: 571e82. doi: 10.1016/j.cell.2015.10.009
  28. Riehm J.M., Vergnaud G., Kiefer D., Damdindorj T., Dashdavaa O., Khurelsukh T., Zoller L., Wolfe R., Le Fleche P., Scholz H.C. Yersinia pestis Lineages in Mongolia. PLoS One, 2012, vol. 7, no. 2: e30624. doi: 10.1371/ journal.pone.0030624
  29. Skurnik M., Peippo A., Ervela E. Characterization of the O-antigen gene cluster of Yersinia pseudotuberculosis and the cryptic O-antigen gene cluster of Yersinia pestis shows that the plague bacillus is most closely related to and has evolved from Y. pseudotuberculosis serotype O:1b. Mol. Microbiol., 2000, vol. 37, no. 2, pp. 316–330. doi: 10.1046/j.1365-2958.2000.01993.x
  30. Suntsov V.V. Origin of the plague: prospects of ecological-molecular-genetic synthesis. Herald of the Russian Academy of Sciences, 2019, vol. 89, no. 3, pp. 271–278. doi: 10.1134/S1019331619010118
  31. Suntsov V.V. Prospects for the synthesis of ecological and molecular-genetic approaches to the problem of the speciation of the plague microbe Yersinia pestis. Biology Bulletin Reviews, 2020, vol. 10, no. 4, pp. 324–337. doi: 10.1134/S2079086420040088
  32. Suntsov V.V. Quantum speciation of Yersinia pestis plague microbe in a heteroimmune environment: in the populations of hibernating tarbagan marmots (Marmota sibirica). Contemporary Problems of Ecology, 2018, vol. 11, no. 4, pp. 343–354. doi: 10.1134/S199542551804008X
  33. Suntsov V.V. Host aspect of territorial expansion of the plague microbe Yersinia pestis from the populations of the tarbagan marmot (Marmota sibirica). Biol. Bull Russ. Acad. Sci., 2021, vol. 48, pp. 1367–1379. doi: 10.1134/S1062359021080288
  34. Suntsov V.V., Suntsova N.I. Ecological aspects of evolution of the plague microbe Yersinia pestis and the genesis of natural foci. Biology Bulletin, 2000, vol. 27, pp. 541–552. doi: 10.1023/A:1026651329721
  35. Valtuena A.A., Neumann G.U., Spyrou M.A., Musralina L., Aronb F., Beisenov A., Belinskiy A.B., Bos K.I., Buzhilova A., Conrad M., Djansugurova L.B., Dobes M., Ernee M., Fernandez-Eraso J., Frohlich B., Furmanek M., Hałuszkon A., Hansen S., Harney E., Hiss A.N., Hubner A., Key F.M., Khussainova E., Kitov E., Kitova A.O., Knipper C., Kuhner D., Lalueza-Foxa C., Littleton J., Ken Massy K., Mittnik A., Mujika-Alustiza J.A., Olald I., Papac L., Penske S., Peska J., Pinhasi R., Reich D., Reinhold S., Stah R., Stauble H., Tukhbatova R.I., Vasilyev S., Veselovskaya E., Warinner C., Philipp W., Stockhammer P.W., Haak W., Krause J., Herbiga A. Stone age Yersinia pestis genomes shed light on the early evolution, diversity, and ecology of plague. PNAS, 2022, vol. 119, no. 17: e2116722119. doi: 10.1073/pnas.2116722119
  36. Wren B.W. The Yersinia — a model genus to study the rapid evolution of bacterial pathogens. Nat. Rev. Microbiol., 2003, vol. 1, no. 1, pp 55–64. doi: 10.1038/nrmicro730

Supplementary files

Supplementary Files
Action
1. JATS XML
Download
2. Figure 1. A typical molecular phylogenetic dendrogram of Yersinia pestis based on the molecular SNP marker analysis [16]

Download (185KB)
Indexing metadata
3. Figure 2. The tritopic origin of the three geneovariantes (subspecies) for the plague microbe Yersinia pestis 2.ANT3, 3.ANT2 and 4.ANT1 in the three geographic populations of the Mongolian marmot Marmota sibirica sibirica (I), M. sibirica caliginosus (II) and M. sibirica ssp. (III) and three independent routes of relevant territorial expansion

Download (164KB)
Indexing metadata

Copyright (c) 2022 Suntsov V.V.

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