Abstract
The genomic instability of the cholera agent leads to the emergence of its new variants with altered epidemically significant features. This makes investigation of the dynamics in pathogenicity gene structure and cholera vibro persistence changes over extended periods of time important. Bioinformatic analysis of whole genome nucleotide sequences was carried out in 44 toxigenic and nontoxigenic Vibrio cholerae O1 strains, biovar El Tor, isolated before the onset and in different periods of the current pandemic, with 29 of them being found in Russia. SNP-typing was performed using Bayesian evolutionary analysis with BEAST v2.5.1. Based on SNP-analysis, it was demonstrated that the importation of epidemically hazardous strains into the territory of Russia (1970–2014) overlapped with three different waves of the global spread of cholera. Comparison of the nucleotide sequences of genomic regions determining their virulence and ability to spread epidemically confirmed that there were multilayered rapid changes in cholera vibrios during evolution. For the first time ever, it has been established that the genomes of pathogenicity islands, VPI-1 and VPI-2, of prepandemic strains contained different mutations, which distinguish them from the genome of pandemic strains. At the same time, we have revealed conservation of nucleotide sequences of all the studied persistence genes from VPI-2 and EPI of pandemic isolates. On the contrary, the modern nontoxigenic strains ctxA–tcpA– show considerable variability of persistence genes that are parts of the structure of these mobile elements. New data on the structure of regions of the V. cholerae genome associated with persistence can be used to differentiate V. cholerae of different epidemic significance.
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REFERENCES
Kaper, J.B., Morris, J.G., and Levine, M.M., Cholera, Clin. Microbiol. Rev., 1995, vol. 8, pp. 48–86. https://doi.org/10.1128/cmr.8.1.48
Mironova, L.V., Current conceptions concerning the objective laws of a cholera epidemic process: ecological and molecular biological aspects, Epidemiol. Infekts. Bolezn., 2018, vol. 23, no. 5, pp. 242–250.
Tanamal, S.T., Notes on paracholera in Sulawesi (Celebes), Am. J. Trop. Med. Hyg., 1959, vol. 8, no. 1, pp. 72–78. https://doi.org/10.4269/ajtmh.1959.8.72
Mutreja, A., Kim, D.W., Thomson, N., Connor, T.R., Lee, J.H., Kariuki, S., et al., Evidence for several waves of global transmission within the seventh cholera pandemic, Nature, 2011, vol. 477, no. 7365, pp. 462–465. https://doi.org/10.1038/nature10392
Ramamurthy, T., Mutreja, A., Weill, F.X., Das, B., Ghosh, A., and Nair, G.B., Corrigendum: Revisiting the global epidemiology of cholera in conjunction with the genomics of Vibrio cholerae, Front. Public Health, 2019, vol. 7, p. 237. https://doi.org/10.3389/fpubh.2019.00237
Heidelberg, J.F., Elsen, J.A., Nelson, W.C., Clayton, R.A., Gwinn, M.L., Dodson, R.J., et al., DNA sequence of both chromosomes of the cholera pathogen Vibrio cholerae, Nature, 2000, vol. 406, pp. 477–483. https://doi.org/10.1038/35020000
Waldor, M.K. and Mekalanos, J.J., Lysogenic conversion by a filamentous phage encoding cholera toxin, Science, 1996, vol. 272, no. 5270, pp. 1910–1914. https://doi.org/10.1126/science.272.5270.1910
Karaolis, D.K., Johnson, J.A., Bailey, C.C., Boedeker, E.C., Kaper, J.B., and Reeves, P.R., A Vibrio cholerae pathogenicity island associated with epidemic and pandemic strains, Proc. Natl. Acad. Sci. U. S. A., 1998, vol. 95, no. 6, pp. 3134–3139. https://doi.org/10.1073/pnas.95.6.3134
Marsh, J.W. and Taylor, R.K., Genetic and transcriptional analyses of the Vibrio cholerae mannose-sensitive hemagglutinin type 4 pilus gene locus, J. Bacteriol., 1999, vol. 181, no. 4, pp. 1110–1117. https://doi.org/10.1128/jb.181.4.1110-1117.1999
Jermyn, W.S. and Boyd, E.F., Characterization of a novel Vibrio pathogenicity island (VPI-2) encoding neuraminidase (nanH) among toxigenic Vibrio cholerae isolates, Microbiology, 2002, vol. 148, pp. 3681–3693. https://doi.org/10.1099/00221287-148-11-3681
Dziejman, M., Balon, E., Boyd, D., Fraser, C.M., Heidelberg, J.F., and Mekalanos, J.J., Comparative genomic analysis of Vibrio cholerae: Genes that correlate with cholera endemic and pandemic disease, Proc. Natl. Acad. Sci. U. S. A., 2002, vol. 99, no. 3, pp. 1556–1561. https://doi.org/10.3410/f.1004686.53905
Smirnova, N.I., Zadnova, S.P., Agafonov, D.A., Shashkova, A.V., Cheldyshova, N.B., and Cherkasov, A.V., Comparative molecular-genetic analysis of mobile elements in natural strains of cholera agent, Russ. J. Genet., 2013, vol. 49, no. 9, pp. 898–908. https://doi.org/10.1134/S1022795413090081
Nair, G.B., Faruque, S.M., Bhuiyan, N.A., Kamruzzaman, M., Siddique, A.K., and Sack, D.A., New variants of Vibrio cholerae O1 biotype El Tor with attributes of the classical biotype from hospitalized patients with acute diarrhea in Bangladesh, J. Clin. Microbiol., 2002, vol. 40, no. 9, pp. 3296–3299. https://doi.org/10.1128/JCM.40.9.3296-3299.2002
Son, M.S., Megli, C.J., Kovacikova, G., Qadri, F., and Taylor, R.K., Characterization of Vibrio cholerae O1 El Tor biotype variant clinical isolates from Bangladesh and Haiti, including a molecular genetic analysis of virulence genes, J. Clin. Microbiol., 2011, vol. 49, pp. 3739–3749. https://doi.org/10.1128/JCM.01286-11
Kim, E.J., Lee, C.H., Nair, G.B., and Kim, D.W., Whole-genome sequence comparisons reveal the evolution of Vibrio cholerae O1, Trends Microbiol., 2015, vol. 23, no. 8, pp. 479–489. https://doi.org/10.1016/j.tim.2015.03.010
Weill, F.X., Domman, D., Njamkepo, E., Almesbahi, A.A., Naji, M., Nasher, S.S., et al., Genomic insights into the 2016–2017 cholera epidemic in Yemen, Nature, 2019, vol. 565, no. 7738, pp. 230–233. https://doi.org/10.1038/s41586-018-0818-3
Taviani, E., Grim, C.J., Choi, J., Chun, J., Haley, B., Hasan, N.A., et al., Discovery of novel Vibrio cholerae VSP-II genomic islands using comparative genomic analysis, FEMS Microbiol. Lett., 2010, vol. 308, no. 2, pp. 130–137. https://doi.org/10.1111/j.1574-6968.2010.02008.x
Imamura, D., Morita, M., Sekizuka, T., Mizuno, T., Takemura, T., Yamashiro, T., et al., Comparative genome analysis of VSP-II and SNPs reveals heterogenic variation in contemporary strains of Vibrio cholerae O1 isolated from cholera patients in Kolkata, India, PLoS Neglected Trop. Dis., 2017, vol. 11, vol. 2, p. e0005386. https://doi.org/10.1371/journal.pntd.0005386
Baddam, R., Sarker, N., Ahmed, D., Mazumder, R., Abdullah, A., Morshed, R., et al., Genome dynamics of Vibrio cholerae isolates linked to seasonal outbreaks of cholera in Dhaka, Bangladesh, mBio, 2020, vol. 11, no. 1, pii e03339-19. https://doi.org/10.1128/mBio.03339-19
Titova, S.V., Moskvitina, E.A., Kruglikov, V.D., Samorodova, A.V., Tyuleneva, E.G., Monakhova, E.V., et al., Cholera: Analysis of epidemiological situation across the world and in Russia within a period of 2006–2015, Probl. Partic. Dangerous Infect., 2016, vol. 1, pp. 20–27. https://doi.org/10.21055/0370-1069-2016-1-20-27
Smirnova, N.I., Agafonova, E.Yu., Shchelkanova, E.Yu., Agafonov, D.A., Krasnov, Ya.M., Livanova, L.F., and Kutyrev, V.V., Genomic diversity of non-toxigenic Vibrio cholerae O1 strains, isolated in the territory of Russia and neighboring states, Mol. Genet., Microbiol. Virol., 2018, vol. 33, no. 2, pp. 97–109. https://doi.org/10.3103/S089141681802012X
Kuleshov, K.V., Markelov, M.L., Dedkov, V.G., Vodopianov, S.O., Vodop’ianov, A.S., Kermanov, A.V., Pisanov, R.V., et al., Phylogenetic analysis of genomes of Vibrio cholerae strains isolated on the territory of Rostov region, Zh. Mikrobiol., Epidemiol. Immunobiol., 2013, no. 6, pp. 13–20.
Hu, D., Liu, B., Feng, L., Ding, P., Guo, X., Wang, M., et al., Origins of the current seventh cholera pandemic, Proc. Natl. Acad. Sci. U. S. A., 2016, vol. 113, no. 48, pp. 7730–7739. https://doi.org/10.1073/pnas.1608732113
Osin, A.V., Nefedov, K.S., Yaroshenko, G.A., and Smirnova, N.I., Comparative genomic analysis of Vibrio cholerae El Tor preseventh and seventh pandemic strains isolated in various periods, Russ. J. Genet., 2005, vol. 41, no. 1, pp. 44–52. https://doi.org/10.1007/s11177-005-0007-y
Taylor, G., Sialidases: structures, biological significance and therapeutic potential, Curr. Opin. Struct. Biol., 1996, vol. 6, no. 6, pp. 830–837. https://doi.org/10.1016/s0959-440x(96)80014-5
Almagro-Moreno, S. and Boyd, E.F., Sialic acid catabolism confers a competitive advantage to pathogenic Vibrio cholerae in the mouse intestine, Infect. Immun., 2009, vol. 77, no. 9, pp. 3807–3816. https://doi.org/10.1128/IAI.00279-09
Watnick, P.I., Fullner, K.J., and Kolter, R., A role for the mannose-sensitive hemagglutinin in biofilm formation by Vibrio cholerae El Tor, J. Bacteriol., 1999, vol. 181, no. 11, pp. 3606–3609. https://doi.org/10.1128/jb.181.11.3606-3609.1999
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Translated by E. V. Makeeva
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Smirnova N.I.: https://orcid.org/0000-0002-7115-6286; e-mail: rusrapi@microbe.ru
Badanin D.V.: https://orcid.org/0000-0002-9662-8438; e-mail: rusrapi@microbe.ru
Rybal’chenko D.A.: https://orcid.org/0000-0002-3117-8229; e-mail: rusrapi@microbe.ru
Krasnov Ya.M.: https://orcid.org/0000-0002-4909-2394; e-mail: rusrapi@microbe.ru
Kritsky A.A.: https://orcid.org/0000-0002-5506-4285; e-mail: rusrapi@microbe.ru
Lozovsky Yu.V.: https://orcid.org/0000-0003-4382-7254; e-mail: rusrapi@microbe.ru
Fedorov A.V.: https://orcid.org/0000-0001-7190-4427; e-mail: rusrapi@microbe.ru
Kutyrev V.V.: https://orcid.org/0000-0003-3788-3452; e-mail: rusrapi@microbe.ru
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Smirnova, N.I., Badanin, D.V., Rybal’chenko, D.A. et al. Variability of the Genome of El Tor Cholera Vibrios Isolated before the Onset and in Different Periods of the Current Pandemic. Mol. Genet. Microbiol. Virol. 36, 79–91 (2021). https://doi.org/10.3103/S0891416821020087
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DOI: https://doi.org/10.3103/S0891416821020087