Abstract
Plague is a zoonotic infection whose pathogenic agent has caused hundreds of million human deaths. A broad range of hosts and vectors, along with the geographical dispersion of natural plague foci characterized by different ecological conditions, contribute to the formation of the polytypic Y. pestis species, the result of selection of the genetic variants specific for certain natural foci. Through the efforts of a world consortium of scientists, a global coordinated phylogram of the SNP types of the plague pathogen has been developed. However, debates on the intraspecies Y. pestis taxonomy still continue on the vast Russian expanses. The work of a taxonomist has many specific, individual features, formed on the basis of individual experience. It is important in this kind of work to follow an old rule which requires that borders should be placed where they have been put by nature, and should not be put where nature has not put them. With that in mind, we suggest here the rational variant of the plague pathogen nomenclature constructed in accordance with the rules set out in the International Code of Bacterial Nomenclature and Evolutionary Taxonomy.
Similar content being viewed by others
REFERENCES
Anisimov, A.P., Lindler, L.E., and Pier, G.B., Intraspecific diversity of Yersinia pestis, Clin. Microbiol., 2004, vol. 17, no. 2, pp. 434–464.
Cui, Y. and Song, Y., Genome and Evolution of Yersinia pestis, Adv. Exp. Med. Biol., 2016, vol. 918, pp. 171–192. https://doi.org/10.1007/978-94-024-0890-4_6
Yersin, A., La peste bubonique à Hong-Kong, Ann. Inst. Pasteur (Paris), 1894, vol. 8, p. 662–667.
Qi, Z., Cui, Y., Zhang, Q., and Yang, R., Taxonomy of Yersinia pestis, Adv. Exp. Med. Biol., 2016, vol. 918, pp. 35–78. https://doi.org/10.1007/978-94-024-0890-4_3
Morelli, G., Song, Y., Mazzoni, C.J., et al., Yersinia pestis genome sequencing identifies patterns of global phylogenetic diversity, Nat. Genet., 2010, vol. 42, no. 12, pp. 1140–1143. https://doi.org/10.1038/ng.705
Devignat, R., Variétés de l’espèce Pasteurella pestis: nouvelle hyphothèse, Bull. W. H. O., 1951, vol. 4, no. 2, pp. 247–263.
Tumanskii, V.M., On classification of varieties of the plague pathogen, Zh. Mikrobiol., Epidemiol. Immunobiol., 1957, vol. 6, pp. 3–7.
Adair, D.M., Worsham, P.L., Hill, K.K., et al., Diversity in a variable-number tandem repeat from Yersinia pestis, J. Clin. Microbiol., 2000, vol. 38, no. 4, pp. 1516–1519.
Klevytska, A.M., Price, L.B., Schupp, J.M., et al., Identification and characterization of variable-number tandem repeats in the Yersinia pestis genome, J. Clin. Microbiol., 2001, vol. 39, no. 9, pp. 3179–3185. https://doi.org/10.1128/JCM.39.9.3179-3185.2001
Motin, V.L., Georgescu, A.M., Elliott, J.M., et al., Genetic variability of Yersinia pestis isolates as predicted by PCR-based IS100 genotyping and analysis of structural genes encoding glycerol-3-phosphate dehydrogenase (glpD), J. Bacteriol., 2002, vol. 184, vol. 4, pp. 1019–1027.
Achtman, M., Morelli, G., Zhu, P., et al., Microevolution and history of the plague bacillus, Yersinia pestis, Proc. Natl. Acad. Sci. U. S. A., 2004, vol. 101, no. 51, pp. 17 837–17 842. https://doi.org/10.1128/jb.184.4.1019-1027.2002
Zhou, D., Tong, Z., Song, Y., et al., Genetics of metabolic variations between Yersinia pestis biovars and the proposal of a new biovar, microtus, J. Bacteriol., 2004, vol. 186, no. 15, pp. 5147–5152. https://doi.org/10.1128/JB.186.15.5147-5152.2004
Valtueña, A.A., Mittnik, A., Key, F.M., et al., The stone age plague and its persistence in Eurasia, Curr. Biol., 2017, vol. 27, no. 23, pp. 3683–3691. https://doi.org/10.1016/j.cub.2017.10.025
Cui, Y., Yang, X., Xiao, X., et al., Genetic variations of live attenuated plague vaccine strains (Yersinia pestis EV76 lineage) during laboratory passages in different countries, Infect. Genet. Evol., 2014, vol. 26, pp. 172–179. https://doi.org/10.1016/j.meegid.2014.05.023
Kingry, L.C., Rowe, L.A., Respicio-Kingry, L.B., et al., Whole genome multilocus sequence typing as an epidemiologic tool for Yersinia pestis, Diagn. Microbiol. Infect. Dis., 2016, vol. 84, no. 4, pp. 275–280. https://doi.org/10.1016/j.diagmicrobio.2015.12.003
Lindler, L.E., Typing methods for the plague pathogen, Yersinia pestis, J. AOAC Int., 2009, vol. 92, no. 4, pp. 1174–1783.
Platonov, M.E., Evseeva, V.V., Dentovskaya, S.V., and Anisimov, A.P., Molecular typing of Yersinia pestis, Mol. Genet., Microbiol. Virol., 2013, vol. 28, no. 2, pp. 41–51. https://doi.org/10.3103/S0891416813020067
Vogler, A.J., Keim, P., and Wagner, D.M., A review of methods for subtyping Yersinia pestis: from phenotypes to whole genome sequencing, Infect., Genet. Evol., 2016, vol. 37, pp. 21–36. https://doi.org/10.1016/j.meegid.2015.10.024
Riehm, J.M., Vergnaud, G., Kiefer, D., et al., Yersinia pestis lineages in Mongolia, PLoS One, 2012, vol. 7, no. 2, p. e30624. https://doi.org/10.1371/journal.pone.0030624
Vogler, A.J., Chan, F., Nottingham, R., et al., A decade of plague in Mahajanga, Madagascar: Insights into the global maritime spread of pandemic plague, mBio, 2013, vol. 4, no. 1, p. e00623-00612. https://doi.org/10.1128/mBio.00623-12
Vogler, A.J., Chan, F., Wagner, D.M., et al., Phylogeography and molecular epidemiology of Yersinia pestis in Madagascar, PLoS Neglected Trop. Dis., 2011, vol. 5, no. 9, p. e1319. https://doi.org/10.1371/journal.pntd.0001319
Kislichkina, A.A., Solomentsev, V.I., Blagodatskikh, S.A., et al., Three genetically different lineages of Yersinia pestis subsp. microtus bv. caucasica (0.PE2) strains circulate among common voles in natural plague loci in the Caucasus, Mol. Genet., Microbiol. Virol., 2017, vol. 3, no. 4, pp. 191–195. https://doi.org/10.3103/S0891416817040024
Riehm, J.M., Projahn, M., Vogler, A.J., et al., Diverse genotypes of Yersinia pestis caused plague in Madagascar in 2007, PLoS Neglected Trop. Dis., 2015, vol. 9, no. 6, p. e0003844. https://doi.org/10.1371/journal.pntd.0003844
Keim, P., Van Ert, M.N., Pearson, T., et al., Anthrax molecular epidemiology and forensics: using the appropriate marker for different evolutionary scales, Infect. Genet. Evol., 2004, vol. 4, no. 3, pp. 205–213. https://doi.org/10.1016/j.meegid.2004.02.005
Rasmussen, S., Allentoft, M.E., and Nielsen, K., Early divergent strains of in Eurasia 5.000 years ago, Cell, 2015, vol. 163, no. 3, pp. 571–582. https://doi.org/10.1016/j.cell.2015.10.009
Achtman, M., Morelli, G., Zhu, P., et al., Microevolution and history of the plague bacillus, Yersinia pestis, Proc. Natl. Acad. Sci. U. S. A., 2004, vol. 101, no. 51, pp. 17 837–17 842. https://doi.org/10.1073/pnas.0408026101
Cui, Y., Yu, C., Yan, Y., et al., Historical variations in mutation rate in an epidemic pathogen, Yersinia pestis, Proc. Natl. Acad. Sci. U. S. A., 2013, vol. 110, no. 2, pp. 577–582. https://doi.org/10.1073/pnas.1205750110
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. https://doi.org/10.1134/S1062359012010104
Eroshenko, G.A. and Kutyrev, V.V., Biochemical and genetic peculiarities and the phylogenetic relationship of the non-main subspecies in the general scheme of the plague agent evolution, Adv. Exp. Med. Biol., 2012, vol. 954, pp. 45–51. https://doi.org/10.1007/978-1-4614-3561-7_6
Eroshenko, G.A., Nosov, N.Y., Krasnov, Y.M., et al., Yersinia pestis strains of ancient phylogenetic branch 0.ANT are widely spread in the high-mountain plague foci of Kyrgyzstan, PLoS One, 2017, vol. 12, no. 10, p. e0187230. https://doi.org/10.1371/journal.pone.0187230
Kislichkina, A.A., Bogun, A.G., Kadnikova, L.A., et al., Nineteen whole-genome assemblies of Yersinia pestis subsp. microtus, including representatives of biovars caucasica, talassica, hissarica, altaica, xilingolensis, and ulegeica, Genome Announce., 2015, vol. 3, no. 6, p. e01342-15. https://doi.org/10.1128/genomeA.01342-15
Kislichkina, A.A., Bogun, A.G., and Kadnikova, L.A., Eight whole-genome assemblies of Yersinia pestis subsp. microtus bv. caucasica isolated from the common vole (Microtus arvalis) plague focus in Dagestan, Russia, Genome Announce., 2017, vol. 5, no. 34, p. e00847-17. https://doi.org/10.1128/genomeA.00847-17
Kislichkina, A.A., Bogun, A.G., Kadnikova, L.A., et al., Nine whole-genome assemblies of Yersinia pestis subsp. microtus bv. altaica strains isolated from the Altai mountain natural plague focus (No. 36) in Russia, Genome Announce., 2018, vol. 6, no. 3, p. e01440-17. https://doi.org/10.1128/genomeA.01440-17
Platonov, M.E., Evseeva, V.V., Dentovskaya, S.V., and Anisimov, A.P., Molecular typing of Yersinia pestis, Mol. Genet., Microbiol. Virol., 2013, vol. 2, pp. 3–12.
Anisimov, A.P., Yersinia pestis factors ensuring circulation and persistence of the plague pathogen in ecosystems of natural foci. Communication 1, Mol. Genet., Microbiol. Virol., 2002, vol. 4, pp. 1–30.
Li, Y., Cui, Y., Hauck, Y., et al., Genotyping and phylogenetic analysis of Yersinia pestis by MLVA: Insights into the worldwide expansion of Central Asia plague foci, PLoS One, 2009, vol. 4, no. 6, p. e6000. https://doi.org/10.1371/journal.pone.0006000
Kiefer, D., Dalantai, G., Damdindorj, T., et al., Phenotypical characterization of Mongolian Yersinia pestis strains, Vector Borne Zoonotic Dis., 2012, vol. 12, no. 3, pp. 183–188. https://doi.org/10.1089/vbz.2011.0748
Platonov, M.E., Evseeva, V.V., Efremenko, D.V., et al., Intraspecies classification of rhamnose-positive Yersinia pestis strains from natural plague foci of Mongolia, Mol. Genet., Microbiol. Virol., 2015, vol. 30, no. 1, pp. 23–28. https://doi.org/10.3103/S0891416815010073
Platonov, M.E., Evseeva, V.V., Svetoch, T.E., et al., Phylogeography of Yersinia pestis vole strains isolated from natural foci of the Caucasus and South Caucasus, Mol. Genet., Microbiol. Virol., 2012, vol. 27, no. 3, pp. 18–21. https://doi.org/10.3103/S089141681203007X
Laukkanen-Ninios, R., Didelot, X., Jolley, K.A., et al., Population structure of the Yersinia pseudotuberculosis complex according to multilocus sequence typing, Environ. Microbiol., 2011, vol. 13, no. 12, pp. 3114–3127. https://doi.org/10.1111/j.1462-2920.2011.02588.x
Bercovier, H., Mollaret, H.H., Alonso, J.M., et al., Intra- and interspecies relatedness of Yersinia pestis by DNA hybridization and its relationship to Yersinia pseudotuberculosis, Curr. Microbiol., 1980, vol. 4, pp. 225–229. https://doi.org/10.1007/BF02605861
Davis, K.M., All Yersinia are not created equal: Phenotypic adaptation to distinct niches within mammalian tissues, Front. Cell. Infect. Microbiol., 2018, vol. 8, p. 261. https://doi.org/10.3389/fcimb.2018.00261
Grácio, A.J.D.S. and Grácio, M.A.A., Plague: a millenary infectious disease reemerging in the XXI century, Biomed. Res. Int., 2017, vol. 2017, article ID 5696542. https://doi.org/10.1155/2017/5696542
Brubaker, R.R., Factors promoting acute and chronic diseases caused by yersiniae, Clin. Microbiol. Rev., 1991, vol. 4, no. 3, pp. 309–324.
McNally, A., Thomson, N.R., Reuter, S., and Wren, B.W., ‘Add, stir and reduce’: Yersinia spp. as model bacteria for pathogen evolution, Nat. Rev. Microbiol., 2016, vol. 14, no. 3, pp. 177–190. https://doi.org/10.1038/nrmicro.2015.29
Wayne, L.G., Actions of the Judicial Commission of the International Committee on Systematic Bacteriology on requests for opinions published in 1983 and 1984, Int. J. Syst. Bacteriol., 1986, vol. 36, pp. 357–358.
Savin, C., Martin, L., Bouchier, C., et al., The Yersinia pseudotuberculosis complex: characterization and delineation of a new species, Yersinia wautersii, Int. J. Med. Microbiol., 2014, vol. 304, nos. 3–4, pp. 452–463. https://doi.org/10.1016/j.ijmm.2014.02.002
Oren, A. and Garrity, G.M., List of new names and new combinations previously effectively, but not validly, published, Int. J. Syst. Evol. Microbiol., 2014, vol. 64, pp. 2184–2187.
Neubauer, H. and Sprague, L.D., Strains of Yersinia wautersii should continue to be classified as the ‘Korean Group’ of the Yersinia pseudotuberculosis complex and not as a separate species, Int. J. Syst. Evol. Microbiol., 2015, vol. 65, part 2, pp. 732–733. https://doi.org/10.1099/ijs.0.070383-0
Kislichkina, A.A., Kadnikova, L.A., Platonov, M.E., et al., Differentiation of Yersinia pseudotuberculosis, Yersinia pestis subsp. pestis and subsp. microti strains and other representatives of Yersinia pseudotuberculosis complex, Mol. Genet., Microbiol. Virol., 2017, vol. 32, no. 2, pp. 67–74. https://doi.org/10.3103/S0891416817020070
Funding
The work was supported by the Russian Science Foundation (grant no. 14-15-00599).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
No experimentation involving human or animals was part of the present work.
Conflict of interest. The authors declare that they have no conflict of interest.
Additional information
Translated by E. Martynova
Abbreviations: bv., biovar; DDBJ/ENA/GenBank, DNA Data Bank of Japan/European Nucleotide Archive/GenBank; DFR, Different Region; IS, insertion sequence; MLVA, multi locus VNTR analysis; s.l., sensu lato, s.s., sensu stricto; SNP, single nucleotide polymorphism; subsp., subspecies; var., variant; b, base pairs.
About this article
Cite this article
Kislichkina, A.A., Platonov, M.E., Vagaiskaya, A.S. et al. Rational Taxonomy of Yersinia pestis. Mol. Genet. Microbiol. Virol. 34, 110–117 (2019). https://doi.org/10.3103/S0891416819020058
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.3103/S0891416819020058