The development of antibiotic resistance of the probiotic strain Lactiplantibacillus plantarum 8P-A3 is associated with changes in the structure of extracellular vesicules and the character of their effect on bacterial biofilms

Cover Page

Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription or Fee Access

Abstract

For the first time, it was shown that the development of resistance to antibiotics (amoxicillin and clarithromycin) in vitro in the probiotic strain Lactiplantibacillus plantarum 8p-a3, associated with large-scale genomic rearrangements, a change in the profile of phenotypic sensitivity to antimicrobials of different groups, and the evolution of virulence, is also accompanied by significant changes in the lactobacillus-derived extracellular membrane vesicles transferring lipids, polysaccharides, proteins, and nucleic acids. The changes are related to the structure and cargo of vesicles, as well as their activity against biofilms of opportunistic bacteria. The data obtained are relevant for understanding the molecular mechanisms of survival of microorganisms under the selective pressure of antimicrobials, the functional potential of the probiotic vesicles and assessing their safety.

Full Text

Restricted Access

About the authors

O. A. Chernova

Kazan Institute of Biochemistry and Biophysics of Kazan Science Centre of the Russian Academy of Science

Email: kairatr@yandex.ru
Russian Federation, Kazan

A. R. Kayumov

Kazan Federal University

Author for correspondence.
Email: kairatr@yandex.ru
Russian Federation, Kazan

M. I. Markelova

Kazan Institute of Biochemistry and Biophysics of Kazan Science Centre of the Russian Academy of Science; Kazan Federal University

Email: kairatr@yandex.ru
Russian Federation, Kazan; Kazan

V. V. Salnikov

Kazan Institute of Biochemistry and Biophysics of Kazan Science Centre of the Russian Academy of Science

Email: kairatr@yandex.ru
Russian Federation, Kazan

M. P. Kutyreva

Kazan Federal University

Email: kairatr@yandex.ru
Russian Federation, Kazan

A. A. Khannanov

Kazan Federal University

Email: kairatr@yandex.ru
Russian Federation, Kazan

M. S. Fedorova

Kazan Federal University

Email: kairatr@yandex.ru
Russian Federation, Kazan

D. E. Zhuravleva

Kazan Federal University

Email: kairatr@yandex.ru
Russian Federation, Kazan

N. B. Baranova

Kazan Institute of Biochemistry and Biophysics of Kazan Science Centre of the Russian Academy of Science; Kazan Federal University

Email: kairatr@yandex.ru
Russian Federation, Kazan; Kazan

D. A. Faizullin

Kazan Institute of Biochemistry and Biophysics of Kazan Science Centre of the Russian Academy of Science

Email: kairatr@yandex.ru
Russian Federation, Kazan

Y. F. Zuev

Kazan Institute of Biochemistry and Biophysics of Kazan Science Centre of the Russian Academy of Science

Email: kairatr@yandex.ru
Russian Federation, Kazan

V. M. Chernov

Kazan Institute of Biochemistry and Biophysics of Kazan Science Centre of the Russian Academy of Science

Email: kairatr@yandex.ru
Russian Federation, Kazan

References

  1. Gill S., Catchpole R., Forterre P. // FEMS Microbiol. Rev. 2019. V. 43,3. P. 273–303.
  2. Kim W., Lee E. J., Bae I. H., et al. // J. Extracell. Vesicles. 2020. V. 9,1. P. 1793514.
  3. Charpentier L.A., Dolben E.F., Hendricks M.R., et al. // Membranes. 2023. V. 13,9. P. 752.
  4. Dominguez Rubio A.P., D’Antoni C.L., Piuri O.E., et al. // Front. microbiol. 2022. V. 13. P. 864720.
  5. Krzyzek P., Marinacci B., Vitale I., et al. // Pharmaceutics. 2023. V. 15,2. P. 522.
  6. da Silva Barreira D., Laurent J., Lourenco J., et al. // Sci. Rep. 2023. V. 13,1. P. 1163.
  7. Mancino W., Lugli G. A., van Sinderen D., et al. // Microorganisms. 2019. V. 7,12. P. 638.
  8. Tardy L., Giraudeau M., Hill G. E., et al. // Proc. Natl. Acad. Sci. USA. 2019. V. 116,34. P. 16927–16932.
  9. Card K.J., Thomas M.D., Graves Jr.J.L., et al. // Proc. Natl. Acad. Sci. USA. 2019. V.118,5. P. e2016886118.
  10. Chernova O.A., Chernov V.M., Mouzykantov A.A., et al. // Int. J. Antimicrob. Agents. 2021. V. 57,2. P. 106253.
  11. Kostenko V.V., Mouzykantov A.A., Baranova N.B., et al. // Microbiol. Spectr. 2022. V. 10,3. P. e0236021.
  12. Chernov V.M., Chernova O.A., Mouzykantov A.A., et al. // Sci. World J. 2011. V. 11. P. 1120–1130.
  13. Burmatova A., Khannanov A., Gerasimov A., et al. // Polymers. 2023. V. 15,15. P. 3248.
  14. Zucchiatti P., Mitri E., Kenig S., et al. // Anal. Chem. 2016. V. 88,24. P. 12090–12098.
  15. Chernov V.M., Mouzykantov A.A., Baranova N.B., et al. // J. Proteom. 2014. V. 110. P. 117–128.
  16. Baidamshina D.R., Trizna E.Y., Holyavka, M.G., et al. // Sci. Rep. 2017. V.7. P. 46068
  17. Hobby C.R., Herndon J.L., Morrow C.A., et al. // Microbiologyopen. 2019. V. 8,2. P. e00635.
  18. Bai Y., Luo B., Zhang Y., et al. // Int. J. Biol. Macromol. 2021. V.185. P.1036–1049.
  19. Slavetinsky С., Hauser J., Cordula Gekeler C., et al. // eLife . 2022. 11:e66376.
  20. Arias-Rojas A, Arifah A, Angelidou G., et al. // PLoS Pathog. 2024. V.20,8. P. e1012462.

Supplementary files

Supplementary Files
Action
1. JATS XML
2. 1. Micrographs of isolated cells (A) and vesicles (B) of the probiotic strain L. plantarum 8p-a3 obtained by transmission electron microscopy.

Download (319KB)
3. 2. Distribution of sizes and concentrations of isolated vesicles of L. plantarum 8p-a3 (A) and L. plantarum 8p-a3-Clr-Amx (B) strains, the data were obtained by analyzing the trajectories of nanoparticles.

Download (235KB)
4. 3. Infrared spectra of vesicular suspensions of L. plantarum 8p-a3 (solid line) and L. plantarum 8p-a3-Clr-Amx (dashed line).

Download (93KB)
5. 4. Biomass of biofilms of S. aureus, P. aeruginosa, and S. marcescens formed in the absence (assumed to be 100%, black column) and presence of extracellular vesicles of L. plantarum 8p-a3 (light gray) and L. plantarum 8p-a3-Clr-Amx (dark gray). The graphs show the average values and the standard deviations, * p < 0.05.

Download (231KB)

Copyright (c) 2024 Russian Academy of Sciences