Skip to main content
SpringerLink
Log in

The Characteristics of Bacillus cereus Group Strains Isolated from Permafrost in Yakutia for Assessment of Microbiological Risks during Climate Change

  • Published:
Applied Biochemistry and Microbiology Aims and scope Submit manuscript

Abstract

Strains of Bacillus genus were isolated from soil samples in the permafrost region (Yakutia, Russia). The phenotypic characteristics of the strains are given. The analysis of the obtained data made it possible to assign them to the Bacillus cereus complex. PCR analysis made it possible to determine the profile of B. cereus toxin synthesis genes in the genomes of the studied strains. Genetic characterization was obtained by RAPD genotyping and using MLVA loci used for genotyping of the anthrax pathogen. The results of genotyping at different levels of resolution made it possible to differentiate the studied strains from the B. anthracis species and to show their intraspecific genetic differences and the degree of relationship. Whole genome sequencing was carried out, based on the data of which MLST genotyping was carried out, which revealed two known sequence types and one new one that is described for the first time in this work. The results we obtained are of practical importance and are extremely interesting from the point of view of the evolution and phylogeography of the B. cereus group, since the fact that strains were isolated from permafrost suggests that their age may be much older than expected.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.

Similar content being viewed by others

REFERENCES

  1. Stepanov, I., Makarov, I., Makarova, E., et al., Climatic Change, 2023, vol. 176, no. 4, p. 39. https://doi.org/10.1007/s10584-023-03512-5

    Article  Google Scholar 

  2. Baldwin, V.M., Front. Microbiol., 2020, p. 11. https://doi.org/10.3389/fmicb.2020.01731

  3. Carroll, L.M., Kovac, J., Miller, R.A., and Wiedmann, M., Appl. Environ. Microbiol., 2017, vol. 83, no. 17, p. e01096-17. https://doi.org/10.1128/AEM.01096-17

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  4. Jovanovic, J., Ornelis, V.F.M., Madder, A., and Rajkovic, A., Compr. Rev. Food. Sci. Food. Saf., 2021, vol. 20, no. 4, pp. 3719–3761. https://doi.org/10.1111/1541-4337.12785

    Article  PubMed  CAS  Google Scholar 

  5. Marinin, L.I., Onishchenko, G.G., Kravchenko, T.B., Dyatlov, I.A., Tyurin, E.A., and Stepanov, A.V., Sibirskaya yazva cheloveka: epidemiologiya, profilaktika, diagnostika, lechenie (Human Anthrax: Epidemiology, Prevention, Diagnosis, and Treatment), Moscow: ZAO MP Gigiena, 2008.

  6. Marinin, L.I., Dyatlov, I.A., and Mokrievich, A.N., Metody izucheniya biologicheskikh i molekulyarno-geneticheskikh svoistv vozbuditelya sibirskoi yazvy: uchebno-metodicheskoe posobie (Methods of Studying Biological and Molecular-Genetic Properties of the Anthrax Pathogen: Teaching Aid), Dyatlov, I.A., Ed., Moscow: DInastiya, 2021.

  7. Drean, P. and Fox, E.M., Methods Mol. Biol., 2015, no. 1301, pp. 71–83. https://doi.org/10.1007/978-1-4939-2599-5_7

  8. Daffonchio, D., Borin, S., Frova, G., Gallo, R., Mori, E., Fani, R., et al., Appl. Environ. Microbiol., 1999, vol. 65, no. 3, pp. 1298–303. https://doi.org/10.1128/AEM.65.3.1298-1303.1999

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  9. Oh, M.H., Ham, J.S., and Cox, J.M., Int. J. Food Microbiol., 2012, vol. 152, nos. 1–2, pp. 1–8. https://doi.org/10.1016/j.ijfoodmicro.2011.09.018

    Article  PubMed  CAS  Google Scholar 

  10. Ripabelli, G., McLauchlin, J., Mithani, V., and Threlfall, E.J., Lett. Appl. Microbiol., 2000, vol. 30, no. 5, pp. 358–363. https://doi.org/10.1046/j.1472-765x.2000.00729.x

    Article  PubMed  CAS  Google Scholar 

  11. Hill, K.K., Ticknor, L.O., Okinaka, R.T., Asay, M., Blair, H., Bliss, K.A., et al., Appl. Environ. Microbiol., 2004, vol. 70, no. 2, pp. 1068–1080. https://doi.org/10.1128/AEM.70.2.1068-1080.2004

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  12. Helgason, E., Okstad, O.A., Caugant, D.A., Johansen, H.A., Fouet, A., Mock, M., Hegna, I., and Kolsto, A.B., Appl. Environ. Microbiol., 2000, vol. 66, no. 6, pp. 2627–2630. https://doi.org/10.1128/AEM.66.6.2627-2630.2000

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  13. Helgason, E., Tourasse, N.J., Meisal, R., Caugant, D.A., and Kolsto, A.B., Appl. Environ. Microbiol., 2004, vol. 70, no. 1, pp. 191–201. https://doi.org/10.1128/AEM.70.1.191-201.2004

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  14. Priest, F.G., Barker, M., Baillie, L.W., Holmes, E.C., and Maiden, M.C., J. Bacteriol., 2004, vol. 186, no. 23, pp. 7959–7970. https://doi.org/10.1128/JB.186.23.7959-7970.2004

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  15. Keim, P., Price, L.B., Klevytska, A.M., Smith, K.L., Schupp, J.M., Okinaka, R., et al., J. Bacteriol., 2000, vol. 182, no. 10, pp. 2928–2936. https://doi.org/10.1128/JB.182.10.2928-2936.2000

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  16. Timofeev, V., Bahtejeva, I., Mironova, R., Titareva, G., Lev, I., Christiany, D., et al., PLoS One, 2019, vol. 14, no. 5, p. e0209140. https://doi.org/10.1371/journal.pone.0209140

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  17. Ehling-Schulz, M., Guinebretiere, M.H., Monthan, A., and Berge, O., FEMS Microbiol. Lett., 2006, vol. 260, no. 2, pp. 232–240. https://doi.org/10.1111/j.1574-6968.2006.00320.x

    Article  PubMed  CAS  Google Scholar 

  18. Marxen, S., Stark, T.D., Frenzel, E., Rutschle, A., Lucking, G., Purstinger, G., et al., Anal. Bioanal. Chem., 2015, vol. 407, no. 9, pp. 2439–2453. https://doi.org/10.1007/s00216-015-8511-y

    Article  PubMed  CAS  Google Scholar 

  19. Dietrich, R., Jessberger, N., Ehling-Schulz, M., Martlbauer, E., and Granum, P.E., Toxins (Basel), 2021, vol. 13, no. 2, p. 98. https://doi.org/10.3390/toxins13020098

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  20. Kim, J.B., Kim, J.M., Kim, S.Y., Kim, J.H., Park, Y.B., Choi, N.J., et al., J. Food Prot., 2010, vol. 73, no. 7, pp. 1219–1224. https://doi.org/10.4315/0362-028x-73.7.1219

    Article  PubMed  CAS  Google Scholar 

  21. Kim, J.M., Forghani, F., Kim, J.B., Park, Y.B., Park, M.S., Wang, J., et al., Food Sci. Biotechnol., 2012, vol. 21, no. 5, pp. 1439–1444. https://doi.org/10.1007/s10068-012-0189-8

    Article  CAS  Google Scholar 

  22. Tallent, S.M., Hait, J.M., and Bennett, R.W., J. Appl. Microbiol., 2015, vol. 118, no. 4, pp. 1068–1075. https://doi.org/10.1111/jam.12766

    Article  PubMed  CAS  Google Scholar 

  23. Tsilia, V., Devreese, B., de Baenst, I., Mesuere, B., Rajkovic, A., Uyttendaele, M., et al., Anal. Bioanal. Chem, 2012, vol. 404, nos. 6–7, pp. 1691–1702. https://doi.org/10.1007/s00216-012-6254-6

    Article  PubMed  CAS  Google Scholar 

  24. Inatsu, Y., Chotiko, A., and Ananchaipattana, C., Jpn. Agric. Res. Q., 2020, vol. 54, no. 1, pp. 47–51.

    Article  CAS  Google Scholar 

  25. Kuwana, R., Imamura, D., Takamatsu, H., and Watabe, K., Biocontrol Sci., 2012, vol. 17, no. 2, pp. 83–86. https://doi.org/10.4265/bio.17.83

    Article  PubMed  CAS  Google Scholar 

  26. Le Flèche, P., Hauck, Y., Onteniente, L., Prieur, A., Denoeud, F., Ramisse, V., et al., BMC Microbiol., 2001, vol. 1, p. 2. https://doi.org/10.1186/1471-2180-1-2

    Article  PubMed  PubMed Central  Google Scholar 

  27. Lista, F., Faggioni, G., Valjevac, S., Ciammaruconi, A., Vaissaire, J., le Doujet, C., et al., BMC Microbiol., 2006, vol. 6, p. 33. https://doi.org/10.1186/1471-2180-6-33

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  28. Van Ert, M.N., Easterday, W.R., Huynh, L.Y., Okinaka, R.T., Hugh-Jones, M.E., Ravel, J., et al., PLoS One, 2007, vol. 2, no. 5, p. e461. https://doi.org/10.1371/journal.pone.0000461

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  29. Thierry, S., Fourterel, C., Le Fleche, P., Derzelle, S., Dekhil, N., Mendy, C., et al., PLoS One, 2014, vol. 9, no. 6, p. e95131. https://doi.org/10.1371/journal.pone.0095131

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  30. Turnbull, P.C., J. Appl. Microbiol., 1999, vol. 87, no. 2, pp. 237–240. https://doi.org/10.1046/j.1365-2672.1999.00876.x

    Article  PubMed  CAS  Google Scholar 

  31. Marston, C.K., Gee, J.E., Popovic, T., and Hoffmaster, A.R., BMC Microbiol., 2006, vol. 6, p. 22. https://doi.org/10.1186/1471-2180-6-22

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  32. Calvigioni, M., Cara, A., Celandroni, F., Mazzantini, D., Panattoni, A., Tirloni, E., et al., J. Appl. Microbiol., 2022, vol. 133, no. 2, pp. 1078–1088. https://doi.org/10.1111/jam.15636

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  33. Valjevac, S., Hilaire, V., Lisanti, O., Ramisse, F., Hernandez, E., Cavallo, J.D., et al., Appl. Environ. Microbiol., 2005, vol. 71, no. 11, pp. 6613–6623. https://doi.org/10.1128/AEM.71.11.6613-6623.2005

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  34. Antonation, K.S., Grutzmacher, K., Dupke, S., Mabon, P., Zimmermann, F., Lankester, F., et al., PLoS Negl. Trop. Dis., 2016, vol. 10, no. 9, p. e0004923. https://doi.org/10.1371/journal.pntd.0004923

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  35. Goncharova, Y., Bahtejeva, I., Titareva, G., Kravchenko, T., Lev, A., Dyatlov, I., and Timofeev, V., Pathogens, 2021, vol. 10, no. 12, p. 1556. https://doi.org/10.3390/pathogens10121556

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  36. Kolsto, A.B., Tourasse, N.J., and Okstad, O.A., Annu. Rev. Microbiol., 2009, no. 63, pp. 451–476. https://doi.org/10.1146/annurev.micro.091208.073255

  37. Federhen, S., Rossello-Mora, R., Klenk, H.P., Tindall, B.J., Konstantinidis, K.T., Whitman, W.B., et al., Stand. Genomic Sci., 2016, vol. 11, no. 1. https://doi.org/10.1186/s40793-016-0134-1

  38. Ciufo, S., Kannan, S., Sharma, S., Badretdin, A., Clark, K., Turner, S., et al., Int. J. Syst. Evol. Microbiol., 2018, vol. 68, no. 7, pp. 2386–2392. https://doi.org/10.1099/ijsem.0.002809

    Article  PubMed  PubMed Central  Google Scholar 

  39. Stella, E., Mari, L., Gabrieli, J., Barbante, C., and Bertuzzo, E., Sci Rep., vol. 10, no. 1, p. 16460. https://doi.org/10.1038/s41598-020-72440-6

  40. Silva, T.H., Queres Gomes, E.C., Gonçalves, V.N., da Costa, M.C., Valério, A.D., de Assis, SantosD., et al., Fungal Biol., 2022, vol. 126, no. 8, pp. 488–497. https://doi.org/10.1016/j.funbio.2022.04.003

    Article  PubMed  CAS  Google Scholar 

Download references

Funding

The material was prepared within the framework of the sectoral program of Rospotrebnadzor. The work was partly performed under the Agreement on scientific and technological cooperation between the State Research Center for Applied Microbiology and Biotechnology and ANO Gubernskaya Academy.

Author information

Authors and Affiliations

  1. State Research Center for Applied Microbiology and Biotechnology, 142279, Obolensk, Moscow oblast, Russia

    Y. O. Goncharova, V. V. Evseeva, R. I. Mironova, K. V. Khlopova, A. G. Bogun, A. A. Sizova, V. I. Solomentsev, G. M. Titareva, I. V. Bahtejeva, T. B. Kravchenko, V. S. Timofeev & S. G. Ignatov

  2. Moscow State University, 119991, Moscow, Russia

    A. V. Brushkov & S. G. Ignatov

  3. Tyumen State University, 625003, Tyumen, Russia

    A. V. Brushkov

Authors
  1. Y. O. Goncharova
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. V. V. Evseeva
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. R. I. Mironova
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. K. V. Khlopova
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. A. G. Bogun
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. A. A. Sizova
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. V. I. Solomentsev
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. G. M. Titareva
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. I. V. Bahtejeva
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. T. B. Kravchenko
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. A. V. Brushkov
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. V. S. Timofeev
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. S. G. Ignatov
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Y. O. Goncharova or S. G. Ignatov.

Ethics declarations

CONFLICT OF INTEREST

The authors of this work declare that they have no conflicts of interest.

ETHICS APPROVAL AND CONSENT TO PARTICIPATE

This work does not contain any studies involving human and animal subjects.

Additional information

Publisher’s Note.

Pleiades Publishing remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Goncharova, Y.O., Evseeva, V.V., Mironova, R.I. et al. The Characteristics of Bacillus cereus Group Strains Isolated from Permafrost in Yakutia for Assessment of Microbiological Risks during Climate Change. Appl Biochem Microbiol 59, 808–817 (2023). https://doi.org/10.1134/S0003683823060054

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0003683823060054

Keywords:

Search

Navigation