Skip to main content
Log in

Ecological aspects of the origin of Yersinia pestis, causative agent of the plague: Concept of intermediate environment

  • Published:
Contemporary Problems of Ecology Aims and scope

Abstract

Modern phylogenies of Yersinia pestis (Logh.), causative agent of the plague, constructed using molecular-genetic methods, do not receive a satisfactory functional and adaptive interpretation and are far from being ecologically valid. We have presented an ecological scenario of the origin of the causative agent of the plague through the transition of the initial pseudotuberculosis microbe Yersinia pseudotuberculosis O:1b to a free hostal ecological niche (and a new adaptive zone) under ultracontinental climatic conditions of the Late Pleistocene (Sartan time, 22000–15000 years ago) in southern Siberia and Central Asia. An intermediate environment, i.e., the “Mongolian marmot Marmota sibirica-flea Oropsylla silatiewi” parasitic system, where the process of adaptation development of the plague microbe took place, has been characterized. A scenario based on the major principles of the modern synthetic theory of evolution opens the way to an ecological-genetic synthesis of the problem of plague origin and is an appropriate model for developing a theory of molecular evolution of pathogenic (plaguelike) microorganisms.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Abramson, N.I., Phylogeography: results, problems, and prospects, Vestn. Vavilov. O-va Genet. Selekts., 2007, vol. 11, no. 2, pp. 307–331.

    Google Scholar 

  • Achtman, M., Insights from genomic comparisons of genetically monomorphic bacterial pathogens, Phil. Trans. R. Soc., 2012, no. 367, pp. 860–867.

    Google Scholar 

  • Achtman, M., Zurth, K., Morelli, G., Torrea, G., Guiyoule, A., and Carniel, E., Yersinia pestis, the cause of plague, is a recently emerged clone of Yersinia pseudotuberculosis, Proc. Natl. Acad. Sci. U.S.A., 1999, vol. 96, no. 24, pp. 14043–14048.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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., and Keim, P., Microevolution and history of the plague bacillus, Yersinia pestis, Proc. Natl. Acad. Sci. U.S.A., 2004, vol. 101, no. 51, pp. 17837–17842.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Arnold, W., Social thermoregulation during hibernation in alpine marmots (Marmota marmota), J. Comp. Physiol. B, 1988, vol. 158, pp. 151–156.

    Article  CAS  PubMed  Google Scholar 

  • Arnold, W., Energetics of social hibernation, Life in the Cold. Ecological, Physiological, and Molecular Mechanisms, Carey, C., Florant, G.L., Wunder, B.A., and Horwitz, B., Eds., Boulder: Westview Press, 1993, pp. 65–80.

    Google Scholar 

  • Beklemishev, V.N., Spatial and functional structure of populations, Byull. Mosk. O-va. Ispyt. Prirod., Otd. Biol., 1960, vol. 65, no. 2, pp. 41–50.

    Google Scholar 

  • Bibikov, D.I., Gornye surki Srednei Azii i Kazakhstana (Mountain Marmots of Central Asia and Kazakhstan), Moscow: Nauka, 1967.

    Google Scholar 

  • Bibikova, V.A. and Klassovskii, L.N., Peredacha chummy blokhami (Fleas as the Plague Transmitters), Moscow: Meditsina, 1974.

    Google Scholar 

  • Bos, K.I., Stevens, P., Nieselt, K., Poinar, H.N., Dewitte, S.N., and Krause, J., Yersinia pestis: New Evidence for an Old Infection, PLoS One, 2012, vol. 7, no. 11, p. e49803. doi 10.1371/journal.pone.0049803

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chouikha, I. and Hinnebusch, B.J., Yersinia-flea interactions and the evolution of the arthropod-borne transmission route of plague, Curr. Opin. Microbiol., 2012, vol. 15, pp. 1–8.

    Article  Google Scholar 

  • Cohan, F.M., Towards a conceptual and operational union of bacterial systematics, ecology, and evolution, Philos. Trans. R. Soc., B, doi 10.1098/rstb.2006.1918

  • Dobzhansky, Th., Genetics and the Origin of Species, New York: Columbia Univ. Press, 1937.

    Google Scholar 

  • Domaradskii, I.V., Chuma (The Plague), Moscow: Meditsina, 1998.

    Google Scholar 

  • Dubinin, N.P., Evolyutsiya populyatsii i radiatsiya (Evolution of Populations and Radiation), Moscow: Atomizdat, 1966.

    Google Scholar 

  • Eppinger, M., Rosovitz, M.J., Fricke, F.W., Rasko, D.A., Kokorina, G., Fayolle, C., Lindler, L.E., Carniel, E., and Ravel, J., The complete genome sequence of Yersinia pseudotuberculosis IP31758, the causative agent of Far East scarlet-like fever, PLoS Genet., 2007, vol. 3, no. 8, p. e142.

    Article  PubMed Central  PubMed  Google Scholar 

  • Eppinger, M., Worsham, P.L., Nikoloch, M.P., Riley, D.R., Sebastian, Y., Mou, S., Achtman, M., Lindler, L.E., and Ravel, J., Genome sequence of the deep-rooted Yersinia pestis strain Angola, J. Bacteriol., 2010, vol. 192, no. 6, pp. 1685–1699.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Erbaeva, M.A., Istoriya antropogenovoi fauny zaitseobraznykh i gryzunov Selenginskogo srednegor’ya (Evolution of Anthropogenic Fauna of Hare-Like Animals and Rodents in Selenga Middle Mountains), Moscow: Nauka, 1970.

    Google Scholar 

  • Erickson, D.L., Waterfield, N.R., Vadyvaloo, V., Long, D., Fischer, E.R., French-Constant, R., and Hinnebusch, B.J., Acute oral toxicity of Yersinia pseudotuberculosis to fleas: implications for the evolution of vector-borne transmission of plague, Cell Microbiol., 2007, vol. 9, pp. 2658–2666.

    Article  CAS  PubMed  Google Scholar 

  • Fukushima, H., Gomyoda, M., Hashimoto, N., Takashima, I., Shubin, F.N., Isachikova, L.M., Paik, I.K., and 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, no. 288, pp. 93–102.

    Google Scholar 

  • Fukushima, H., Matsuda, Y., Seki, R., Tsubokura, M., Takeda, N., Shubin, F.N., Paik, I.K., and 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. 10, pp. 3541–3547.

    Article  Google Scholar 

  • Grant, V., The Evolutionary Process. A Critical Study of Evolutionary Theory, Columbia Univ. Press, 1991.

    Google Scholar 

  • Hinnebusch, B.J., The evolution of flea-borne transmission in Yersinia pestis, Curr. Issues Mol. Biol., 2005, vol. 7, pp. 197–212.

    CAS  PubMed  Google Scholar 

  • Keim, P.S. and Wagner, D.M., Humans, evolutionary and ecologic forces shaped the phylogeography of recently emerged diseases, Nat. Rev. Microbiol., 2009, vol. 7, no. 11, pp. 813–821.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Klein, K.A. and Bliska, J.B., How Yersinia pestis becomes a foreign obstruction in the digestive system of the macrophage, Autophagy, 2009, vol. 5, no. 6, pp. 882–883.

    PubMed  Google Scholar 

  • Klein, K.A., Fukuto, H.S., Pelletier, M., Romanov, G., Grabenstein, J.P., Palmer, L.E., Ernst, R., and Bliska, J.B., A transposon site hybridization screen identifies galU and wecBC as important for survival of Yersinia pestis in marine macrophages, J. Bacteriol., 2012, vol. 194, no. 3, pp. 653–662.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lidicker, J.J., Solving the enigma of microtine “cycles”, J. Mammal., 1988, vol. 69, no. 2, pp. 225–235.

    Article  Google Scholar 

  • Lindler, L.E., Typing Methods for the Plague Pathogen, Yersinia pestis, J. AOAC Int., 2009, vol. 92, no. 4, pp. 1174–1183.

    CAS  PubMed  Google Scholar 

  • Mayr, E., Animal Species and Evolution, Cambridge: Belknap Press of Harvard Univ. Press, 1963.

    Google Scholar 

  • Mayr, E., Populations, Species, and Evolution, Cambridge: Belknap Press of Harvard Univ. Press, 1970.

    Google Scholar 

  • 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., and Achtman, M., Yersinia pestis genome sequencing identifies patterns of global phylogenetic diversity, Nat. Genet., 2010, no. 12, pp. 1140–1143.

    Google Scholar 

  • Naumov, N.P., Structure and changes in size of populations of terrestrial vertebrates, Zool. Zh., 1967, vol. 46, no. 10, pp. 1470–1486.

    Google Scholar 

  • Owen, L.A., Richards, B., Rhodes, E.J., Cunningham, W.D., Windley, B.F., Badamgarav, J., and Dorjnamjaa, D., Relict permafrost structures in the Gobi of Mongolia: age and significance, J. Quat. Sci., 1998, vol. 13, no. 6, pp. 539–547.

    Article  Google Scholar 

  • Pavlinov, I.Ya., Vvedenie v sovremennuyu filogenetiku (Introduction into Modern Phylogeny), Moscow: KMK, 2005a.

    Google Scholar 

  • Pavlinov, I.Ya., “New phylogeny” and composition, Evolyutsionnye factory formirovaniya raznoobraziya zhivotnogo mira (Evolutionary Factors of Diversity of Fauna), Vorob’eva, E.I. and Striganova, B.R., Eds., Moscow: KMK, 2005b, pp. 15–29.

    Google Scholar 

  • Pauller, O.F., Peculiarities of structure of winter burrow of Daurian marmot and their fleas during winter in Transbaikalian plague focus, in IV Sov.-Mongol. konf. spetsialistov protivochumnykh uchrezhdenii “Problemy prirodnoi ochagovosti chumy”, tezisy dokladov (IV Soviet-Mongolian Conference of the Specialists of Antiplague Organizations “Problems of Natural Nidi of Plague”, Abstracts of Papers), Irkutsk: PChI, 1980, part 1, pp. 80–82.

    Google Scholar 

  • Perry, R.D. and Fetherston, J.D., Yersinia pestis-etiologic agent of plague, Clin. Microbiol. Rev., 1997, vol. 10, no. 1, pp. 35–66.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Pulliam, H.R., Sources, sinks, and population regulation, Am. Nat., 1988, vol. 132, pp. 652–661.

    Article  Google Scholar 

  • Rothschild, M., Recent advances in our knowledge of the order Siphonaptera, Annual Rev. Entomol., 1975, vol. 20, pp. 241–244.

    Article  CAS  Google Scholar 

  • Severtsov, A.S., Evolyutsionnyi stzis i mikroevolyutsiya (Evolutionary Stasigenesis and Microevolution), Moscow: KMK, 2008.

    Google Scholar 

  • Shilova, S.A. and Suntsov, V.V., Natural impacts: knock-out or knock-down? Priroda, 2011, no. 8, pp. 34–42.

    Google Scholar 

  • Schmalhausen, I.I., Faktory evolyutsii (Evolutionary Factors), Moscow: Nauka, 1968.

    Google Scholar 

  • Skurnik, M., Peippo, A., and 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.

    Article  CAS  PubMed  Google Scholar 

  • Sokurenko, E.V., Gomulkiewicz, R., and Dykhuizen, D.E., Source-sink dynamics of virulence evolution, Nat. Rev., Microbiol., 2006, vol. 4, pp. 548–555.

    Article  CAS  Google Scholar 

  • Somov, G.P., Pokrovskii, V.I., Besednova, N.N., and Antonenko, F.F., Psevdotuberkulez (Pseudotuberculosis), Moscow: Meditsina, 2001.

    Google Scholar 

  • Suleimenov, B.M., Mekhanizm enzootii chumy (Mechanism of Enzootic Plague), Alma-Ata, 2004.

    Google Scholar 

  • Suntsov, V.V., Territorial structure of population and intraspecific relations between tarbagans (Marmota sibirica) in Tyva, Zool. Zh., 1981, vol. 60, no. 9, pp. 1394–1405.

    Google Scholar 

  • Suntsov, V.V., Origin of the plague microbe Yersinia pestis: structure of the process of speciation, Biol. Bull., 2012, vol. 39, no. 1, pp. 1–9.

    Article  CAS  Google Scholar 

  • Suntsov, V.V. and Suntsova, N.I., Ecological aspects of evolution of the plague microbe Yersinia pestis and the genesis of natural foci, Biol. Bull., 2000, vol. 27, no. 6, pp. 541–552.

    Article  Google Scholar 

  • Suntsov, V.V. and Suntsova, N.I., Chuma. Proiskhozhdenie i evolyutsiya epizooticheskoi sistemy (ekologicheskie, geograficheskie i sotsial’nye aspekty) (The Plague. Origin and Evolution of Epizootic System (Ecological, Geographic, and Social Aspects)), Moscow: KMK, 2006.

    Google Scholar 

  • Suntsov, V.V. and Suntsova, N.I., Concepts of macroand microevolution as related to the problem of origin and global expansion of the plague pathogen Yersinia pestis, Biol. Bull., 2008, vol. 35, no. 4, pp. 333–338.

    Article  Google Scholar 

  • Suntsov, V.V. and Suntsova, N.I., Principles of speciation of the plague causative agent Yersinia pestis: gradualism or saltation? Biol. Bull., 2009, vol. 36, no. 6, pp. 547–554.

    Article  Google Scholar 

  • Suntsov, V.V. and Suntsova, N.I., Speciation and intraspecific adaptive radiation of Yersinia pestis as the gradual evolutionary process, Med. Akad. Zh., 2010a, no. 2, pp. 58–63.

    Google Scholar 

  • Suntsov, V.V. and Suntsova, N.I., Emergence and evolution of Yersinia pestis as classical model of “Darwin” evolution, Mater. Mezhd. nauchn. konf. “Charl’z Darvin i sovremennaya biologiya”, 21–23 sentyabrya 2009 g., Sankt-Peterburg (Proc. Int. Sci. Conf. “Charles Darwin and Modern Biology”, September 21–23, 2009, St. Petersburg), St. Petersburg: Nestor-Istoriya, 2010b, pp. 304–310.

    Google Scholar 

  • Suntsov, V.V., Suntsova, N.I., Rumal, V.S., Dang Tuan Dat, Hong An Tuet, and Lyong Thi Mo, Structure and genesis of epizootic systems “rodent-flea-Yersinia pestis” in Vietnamese cenosises including ecocide territories, Okruzhayushchaya sreda i zdorov’e cheloveka v zagryaznennykh dioksinami regionakh V’etnama (Environment and Human Health in Vietnamese Regions Polluted by Dioxins), Rumak, V.S., Ed., Moscow: KMK, 2011, pp. 202–258.

    Google Scholar 

  • Timofeev-Resovskii, N.V., Vorontsov, N.N., and Yablokov, A.Ya., Kratkii ocherk teorii evolyutsii (Brief Description of the Theory of Evolution), Moscow: Nauka, 1977.

    Google Scholar 

  • Vadyvaloo, V., Jarret, C., Sturdevant, D.E., Sebbane, F., and Hinnebusch, B.J., Transit through the flea vector, PLoS Pathol., 2010, vol. 6, p. e10000783.

    Article  Google Scholar 

  • Variabel’nost’ vozbuditelya chumy i problemy ego diagnostiki (Variability of Plgue Pathogen and Complications in Diagnostics), Lomov, Yu.M., Ed., Rostov-on-Don: Antei, 2009.

    Google Scholar 

  • Vashchenok, V.S., Blokhi (Siphonaptera) — perenoschiki vozbuditelei boleznei cheloveka i zhivotnykh (Fleas (Siphonaptera) are Transmitters of Animal’s and Human Pathogens), Leningrad: Nauka, 1988.

    Google Scholar 

  • Vetter, S.M., Eisen, R.J., Schotthoefer, A.M., Montenieri, J.A., Holmes, J.L., Bobrov, A.G., Bearden, S.W., Perry, R.D., and Gage, K.L., Biofilm formation is not required for early-phase transmission of Yersinia pestis, Microbiology, 2010, vol. 156, pp. 2216–2225.

    Article  CAS  PubMed  Google Scholar 

  • Wang, X., Zhou, D., Qin, L., Dai, E., Zhang, J., Han, Y., Guo, Z., Song, Y., Du, Z., Wang, J., Wang, J., and Yang, R., Genomic comparison of Yersinia pestis and Yersinia pseudotuberculosis by combination of suppression subtractive hybridization and DNA microarray, Arch. Microbiol., 2006, vol. 186, pp. 151–159.

    Article  CAS  PubMed  Google Scholar 

  • Zhou, D. and Yang, R., Molecular Darwinian evolution of virulence in Yersinia pestis, Infect. Immun., 2009, vol. 77, no. 6, pp. 2242–2250.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhou, D. and Yang, R., Formation and regulation of Yersinia biofilms, Protein and Cell., 2011, vol. 2, no. 3, pp. 173–179.

    Article  CAS  PubMed  Google Scholar 

  • Zhovtyi, I.F. and Peshkov, B.I., Observation of wintering of tarbagan fleas in Transbaikalia, Izv. Irkutsk. Gos. Nauchno-Issled. Protivochumn. Inst. Sib. Dal’nego Vostoka, 1958, vol. 17, pp. 27–32.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to V. V. Suntsov.

Additional information

Original Russian Text © V.V. Suntsov, 2014, published in Sibirskii Ekologicheskii Zhurnal, 2014, No. 1, pp. 3–16.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Suntsov, V.V. Ecological aspects of the origin of Yersinia pestis, causative agent of the plague: Concept of intermediate environment. Contemp. Probl. Ecol. 7, 1–11 (2014). https://doi.org/10.1134/S1995425514010144

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1995425514010144

Keywords

Navigation