Skip to main content
Log in

Effect of Cell-Free Culture Fluid of Staphylococcus aureus on the Structure and Biochemical Composition of Klebsiella pneumoniae and Pseudomonas aeruginosa Biofilms

  • SHORT COMMUNICATIONS
  • Published:
Microbiology Aims and scope Submit manuscript

Abstract

Recently, there has been increasing evidence that many infections are associated with the formation of multispecies biofilms, in which there is a change in the sensitivity of bacteria to antibiotics and a change in the permeability of the extracellular matrix compared to monocultures. In this work, we show that the addition of cell-free culture liquid (CFCL) of Staphylococcus aureus to Klebsiella pneumoniae and Pseudomonas aeruginosa biofilms increases the content of α-, and β-polysaccharides in the matrix up to 2 times, which likely affects the structure of the biofilm. The increase in the polysaccharide component is also confirmed by a significant rise in the expression level of the K. pneumoniae pgaA and P. aeruginosa pelA, pslA genes in the presence of S. aureus culture liquid.

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.

Fig. 1.
Fig. 2.

Similar content being viewed by others

REFERENCES

  1. Baidamshina, D., Trizna, E., and Holyavka, M., Targeting microbial biofilms using Ficin, a nonspecific plant protease, Sci. Rep., 2017, vol. 7, p. 46068.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Bogachev, M., Volkov, V., Markelov, O., Trizna, E., Baydamshina, D., Melnikov, V., Zelenikhin, P., Murtazina, R., Sharafutdinov, I., and Kayumov A., Fast and simple tool for the quantification of biofilm-embedded cells sub-populations from fluorescent microscopic images, PLoS One, 2018, vol. 13, no. 5, p. e0193267.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Bottery, M.J., Pitchford, J.W., and Friman, V.P., Ecology and evolution of antimicrobial resistance in bacterial communities, The ISME J., 2021, vol. 15, no. 4, pp. 939‒948.

    Article  PubMed  Google Scholar 

  4. Chen, K.M., Chiang, M.K., Wang, M., Ho, H.C., Lu, M.C., and Lai, Y.C., The role of pgaC in Klebsiella pneumoniae virulence and biofilm formation, Microb. Pathog., 2014, vol. 10, pp. 89‒99.

    Article  Google Scholar 

  5. Chew, S.C., Kundukad, B., Seviour, T., Van der Maarel, J.R.C., Yang, L., Rice, S.A., Doyle, P., and Kjelleberg, S., Dynamic remodeling of microbial biofilms by functionally distinct exopolysaccharides, mBio, 2014, vol. 5, no. 4, p. e01536-14.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Ciofu, O., Moser, C., Jensen, P.Ø., and Høiby, N., Tolerance and resistance of microbial biofilms, Nature Rev. Microbiol., 2022, vol. 20, no. 10, pp. 621‒635.

    Article  CAS  Google Scholar 

  7. Colvin, K.M., Gordon, V.D., Murakami, K., Borlee, B.R., Wozniak, D.J., and Wong, G.C.L., The Pel polysaccharide can serve a structural and protective role in the biofilm matrix of Pseudomonas aeruginosa, PLoS Pathog., 2011, vol. 7, no. 1, p. e1001264.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Dalton, T., Dowd, S.E., Wolcott, R.D., Sun, Y., Watters, C., Griswold, J.A., and Rumbaugh, K.P., An in vivo polymicrobial biofilm wound infection model to study interspecies interactions, PLoS One, 2011, nos. 6−11, p. e27317.

  9. Eick, S., Biofilms. Oral Biofilms, 2020.

    Google Scholar 

  10. Fedorova, M.S., Mironova, A.V., and Kayumov, A.R., Cell-free supernatant of Staphylococcus aureus culture increases antimicrobials susceptibility of Pseudomonas aeruginosa, Opera Med. Physiol., 2022, vol. 9, pp. 113‒120.

    Google Scholar 

  11. Hobley, L., Harkins, C., MacPhee, C., and Stanley-Wall, N.R., Giving structure to the biofilm matrix: an overview of individual strategies and emerging common themes, FEMS Microbiol. Rev., 2015, vol. 39, no. 5, pp. 649‒669.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Itoh, Y., Rice, J.D., Goller, C., Pannuri, A., Taylor, J., Meisner, J., Beveridge, T.J., Preston, J.F., and Romeo, T., Roles of pgaABCD genes in synthesis, modification, and export of the Escherichia coli biofilm adhesin poly-beta-1,6-N-acetyl-D-glucosamine, J. Bacteriol., 2008, vol. 10, pp. 3670‒3680.

    Article  Google Scholar 

  13. Kayumov, A., Khakimullina, E., Sharafutdinov, I., Triz-na, E., Latypova, L., Lien, H., Margulis, A., Bogachev, M., and Kurbangalieva, A., Inhibition of biofilm formation in Bacillus subtilis by new halogenated furanones, The J. Antibiot., 2015, vol. 68, no. 5, pp. 297‒301.

    Article  CAS  Google Scholar 

  14. Kot, B., Sytykiewicz, H., and Sprawka, I., Expression of the biofilm-associated genes in methicillin-resistant Staphylococcus aureus, in biofilm and planktonic conditions, Int. J. Mol. Sci., 2018, vol. 19, no. 11, p. 3487.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Kranjec, C., Morales Angeles, D., Torrissen Mårli, M., Fernández, L., García, P., Kjos, M., and Diep, D.B., Staphylococcal biofilms: challenges and novel therapeutic perspectives, Antibiotics, 2021, vol. 10, no. 2, p. 131.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Mironova, A.V., Karimova, A.V., Bogachev, M.I., Kayumov, A.R., and Trizna, E.Y., Alterations in antibiotic susceptibility of Staphylococcus aureus and Klebsiella pneumoniae in dual species biofilms, Int. J. Mol. Sci., 2023, vol. 24, p. 10.

    Article  Google Scholar 

  17. Orazi, G. and O’Toole, G.A., “It takes a village”: mecha-nisms underlying antimicrobial recalcitrance of polymicrobial biofilms, J. Bacteriol., 2019, vol. 202, no. 1, p. e00530-19.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Otto, M., Staphylococcal biofilms, Microbiol. Spectr., 2018, vol. 6, pp. 1–26.

    Article  CAS  Google Scholar 

  19. Radlinski, L.C., Rowe, S.E., Brzozowski, R., Wilkinson, A.D., Huang, R., Eswara, P., and Conlon, B.P., Chemical induction of aminoglycoside uptake overcomes antibiotic tolerance and resistance in Staphylococcus aureus, Cell Chem. Biol., 2019, vol. 26, no. 10, pp. 1355‒1364.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Ryder, C., Byrd, M., and Wozniak, D.J., Role of polysaccharides in Pseudomonas aeruginosa biofilm development, Curr. Opin. Microbiol., 2007, vol. 10, no. 6, pp. 644‒648.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Sambrook, J., Fritsch, E.F., and Maniatis, T., Molecular Cloning: A Laboratory Manual, Cold Spring Habor Laboratory press, 1989.

    Google Scholar 

  22. Sharma, D., Misba, L., and Khan, A.U., Antibiotics versus biofilm: an emerging battleground in microbial communities, Antimicrob. Resist. Infect. Control, 2019, vol. 8, no. 1, pp. 1‒10.

    Article  Google Scholar 

  23. Trizna, E.Y., Yarullina, M.N., Baidamshina, D.R., Mironova, A.V., Akhatova, F.S., Rozhina, E., Fakhrullin, R.F., Khabibrakhmanova, A.M., Kurbangalieva, A.R., Bogachev, M.I., and Kayumov, A.R., Bidirectional alterations in antibiotics susceptibility in Staphylococcus aureusPseudomonas aeruginosa dual-species biofilm, Sci. Rep., 2018, vol. 10, p. 14849.

    Article  Google Scholar 

Download references

Funding

The work was carried out with financial support from the Russian Science Foundation (project no. 20-64-47014).

Author information

Authors and Affiliations

Authors

Contributions

M.A.V., F.M.S., Z.N.D., S.A.R.—experimental procedures, K.A.R., T.E.Yu.—work management; all authors contributed to the writing and approval of the manuscript.

Corresponding author

Correspondence to A. R. Kayumov.

Ethics declarations

ETHICS APPROVAL AND CONSENT TO PARTICIPATE

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

CONFLICT OF INTEREST

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

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

Mironova, A.V., Fedorova, M.S., Zakarova, N.D. et al. Effect of Cell-Free Culture Fluid of Staphylococcus aureus on the Structure and Biochemical Composition of Klebsiella pneumoniae and Pseudomonas aeruginosa Biofilms. Microbiology 93, 375–379 (2024). https://doi.org/10.1134/S0026261723604748

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0026261723604748

Keywords:

Navigation