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.
Similar content being viewed by others
REFERENCES
Baidamshina, D., Trizna, E., and Holyavka, M., Targeting microbial biofilms using Ficin, a nonspecific plant protease, Sci. Rep., 2017, vol. 7, p. 46068.
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.
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.
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.
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.
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.
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.
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.
Eick, S., Biofilms. Oral Biofilms, 2020.
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.
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.
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.
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.
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.
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.
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.
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.
Otto, M., Staphylococcal biofilms, Microbiol. Spectr., 2018, vol. 6, pp. 1–26.
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.
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.
Sambrook, J., Fritsch, E.F., and Maniatis, T., Molecular Cloning: A Laboratory Manual, Cold Spring Habor Laboratory press, 1989.
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.
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 aureus‒Pseudomonas aeruginosa dual-species biofilm, Sci. Rep., 2018, vol. 10, p. 14849.
Funding
The work was carried out with financial support from the Russian Science Foundation (project no. 20-64-47014).
Author information
Authors and Affiliations
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
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
About this article
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
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S0026261723604748