Influence of sugars on biofilm formation of Staphylococcus epidermidis

  • A. O. Vashchenko Oles Honchar Dnipro National University
  • Y. S. Voronkova Oles Honchar Dnipro National University
  • E. E. Kulyk Oles Honchar Dnipro National University
  • O. S. Snisar Oles Honchar Dnipro National University
  • O. I. Sidashenko Ukrainian State University of Chemical Technology
  • O. S. Voronkova Oles Honchar Dnipro National University
Keywords: staphylococci; biofilm growth; glucose; sucrose; lactose; galactose; dysbiosis

Abstract

The problem of biofilm formation by clinical strains of opportunistic bacteria is one of the most significant for medicine, because in a state of biofilm bacteria become more resistant to environmental factors, including antibiotics, a situation that can cause failure of treatment. Among opportunistic pathogens staphylococci are of special interest. Knowledge about the peculiarities of biofilm formation of these strains, in particular the polysaccharide biosynthesis, can be used for creation of a strategy of prophylaxis of different lesions that bind with staphylococci. The effect of different concentrations of the most widespread sugars (glucose, sucrose, lactose, galactose) on the activity of biofilm formation by strains of Staphylococcus epidermidis was investigated. Strains of S. epidermidis (n = 7) were isolated from the reproductive tract of women with dysbiosis. The cultures were grown in universal synthetic media with concentration of one of the listed sugars (0.5–3.0%) during 72 h. Results were obtained colorimetrically. We studied the number of cells in biofilm and the index of biofilm formation. The largest number of cells in the biofilm was observed when the culture incubated in a medium with 2.0% of glucose (increase of 25.3 times compared to control). The amount of CFU in the control biofilm was 9.96 lg CFU/mL. The glucose concentration of 3.0% inhibited the biofilm formation: the number of cells in the biofilm was 569 times less compared to the control. The highest value of biofilm formation index was 7.2, which was 1.3 times higher than the control (5.4). In the presence of lactose and galactose in nutrient medium in concentrations from 1.0% a decrease in the number of cells and biofilm formation index were observed. The received data show that process of biofilm formation is significantly dependent on external sources of sugars, which can indicate the possibility of their use as antibiofilm drug compounds, which inhibit membrane transport of sugars in bacteria.

References

Arciola, C. R., Campoccia, D., Ravaioli, S., & Montanaro, L. (2015). Polysaccharide intercellular adhesin in biofilm: Structural and regulatory aspects. Frontiers in Cellular and Infection Microbiology, 5, 7.

Becker, K., Heilmann, C., & Peters, G. (2014). Coagulase-negative staphylococci. Clinical Microbiology Review, 27, 870–926.

Ben Slama, R., Bekir, K., Miladi, H., Noumi, A., & Bakhrouf, A. (2012). Adhesive ability and biofilm metabolic activity of Listeria monocytogenes strains before and after cold stress. African Journal of Biotechnology, 11(61), 12475–12482.

Bester, E., Kroukamp, O., Hausner, M., Edwards, E. A., & Wolfaardt, G. M. (2010). Biofilm form and function: Carbon availability affects biofilm architecture, metabolic activity and planktonic cell yield. Journal of Applied Microbiology, 110, 387–398.

Brotman, R. M., Klebanoff, M. A., Nansel, T. R., Andrews, W. W., Schwebke, J. R., Zhang, J., Yu, K. F., Zenilman, J. M., & Scharfstein, D. O. (2008). A longitudinal study of vaginal douching and bacterial vaginosis – a marginal structural modeling analysis. American Journal of Epidemiology, 168, 188–196.

Buzon-Duran, L., Alonso-Calleja, C., & Riesco-Pelaez, F. (2017). Effect of sub-inhibitory concentrations of biocides on the architecture and viability of MRSA biofilms. Food Microbiology, 65, 294–301.

Coenye, T., & Nelis, H. J. (2010). In vitro and in vivo model systems to study microbial biofilm formation. Journal of Microbiological Methods, 83, 89–105.

Costerton, J. W., Cheng, K. J., Geesey, G. G., Ladd, T. I., Nickel, J. C., Dasgupta, M., & Marrie, T. J. (1987). Bacterial biofilms in nature and disease. Annual Review of Microbiology, 41, 435–464.

Croes, S., Deurenberg, R. H., Boumans, M. L., Beisser, P. S., Neef, C., & Stobberingh, E. E. (2009). Staphylococcus aureus biofilm formation at the physiologic glucose concentration depends on the S. aureus lineage. BMC Microbiology, 9, 229.

Diemond-Hernandez, B. (2010). Production of icaADBC encoded polysaccharide intercellular adhesin and therapeutic failure in pediatric patients with staphylococcal device-related infections. BMC Infectious Disease, 10, 68–74.

Dobinsky, S., Kiel, K., Rohde, H., Bartscht, K., Knobloch, J. K., Horstkotte, M. A., & Mack, D. (2003). Glucose-related dissociation between icaADBC transcription and biofilm expression by Staphylococcus epidermidis: Evidence for an additional factor required for polysaccharide intercellular adhesin synthesis. Journal of Bacteriology, 185(9), 2879–2886.

Evglevsky, D. А., Evlevsky, A. A., Semenyutin, V. V., Smirnov, I. I., & Tatarnikov, K. V. (2011). Universalnaya sinteticheskaya sreda dlya vyraschivaniya patogennyih i probioticheskih mikroorganizmov pri poluchenii biopreparatov [Universal synthetic nutrient medium for growing of pathogenic and probiotic microorganisms in the creation of biological preparation]. Vestnik Kurskoy Gosudarstvennoy Selskohozyaystvennoy Akademii, 4, 64–66 (in Russian).

Fabres-Klein, M. H., Caizer Santos, M. J., Contelli Klein, R., de Souza, G. N., & de Oliveira Barros Ribon, A. (2015). An association between milk and slime increases biofilm production by bovine Staphylococcus aureus. BMC Veterinary Research, 11, 3.

Høiby, N., Bjarnsholt, T., Givskov, M., Molin, S., & Ciofu, O. (2010). Antibiotic resistance of bacterial biofilms. International Journal of Antimicrobial Agents, 35, 322–332.

Hou, W., Sun, X., Wang, Z., & Zhang, Y. (2012). Biofilm-forming capacity of Staphylococcus epidermidis, Staphylococcus aureus, and Pseudomonas aeruginosa from ocular infections. Investigative Ophthalmology and Visual Science, 53(9), 5624–5631.

Jacqueline, C., & Caillon, J. (2014). Impact of bacterial biofilm on the treatment of prosthetic joint infections. The Journal of Antimicrobial Chemotherapy, 69(Suppl 1), i37–i40.

Kiedrowski, M. R., & Horswill, A. R. (2011). New approaches for treating staphylococcal biofilm infections. Annals of the New York Academy of Sciences, 1241, 104–121.

Korobov, V. P., Lemkina, L. M., & Monakhov, V. I. (2010). Analiz chuvstvitel’nosti processov formirovaniya bioplenok Staphylococcus epidermidis 33 k nekotorym faktoram vneshnej sredy [Sensitivity assay for the processes of Staphylococcus epidermidis 33 biofilm formation with respect to several environmental factors]. Vestnik Permskogo Universiteta, Biologiya, 1(1), 59–63 (in Russian).

Kroukampand, O., & Wolfaardt, G. M. (2009). CO2 production as an indicator of biofilm metabolism. Applied and Environmental Microbiology, 75(13), 4391–4397.

Kuchtyn, M. D., Perkiy, Y. B., & Krushelnytska, N. V. (2013). Formuvannia zmishanykh bioplivok mikroorhanizmamy, yaki vydileni z doilnoho ustatkuvannia ta moloka syroho [Formation of mixed biofilms of microorganisms isolated from milking equipment and raw milk]. Veterynarna Medytsyna, 97, 442–443 (in Ukrainian).

Lagun, L. V., & Zhavoronok, S. V. (2013). Bakterialnyye bioplenki i ikh rol’ v razvitii infektsiy mochevyvodyashchikh putey [Bacterial biofilms and their role in urinary tract infections]. Meditsinskiy Zhurnal, 4, 21–27 (in Russian).

Lavryk, G., & Kornijchuk, O. (2015). Bioplivkova forma stafilokokiv u mono- ta bivydovij kulturi v poiednanni z laktobatsylamy [Biofilm forms in mono- and mixed staphylococci species culture in combination with lactobacilli]. Studia Biologica, 9(3–4), 89–98 (in Ukrainian).

Lebeaux, D., Chauhan, A., Rendueles, O., & Beloin, C. (2013). From in vitro to in vivo models of bacterial biofilm-related infections. Pathogens, 2, 288–356.

Liu, Y., Zhang, J., & Ji, Y. (2020). Environmental factors modulate biofilm formation by Staphylococcus aureus. Science Progress, 103(1), 36850419898659.

Maianskii, A. N., & Chebotar, I. V. (2011). Stafilokokkovye bioplenki: Struktura, regulyaciya, ottorzhenie [Staphylococcal biofilms: Structure, regulation, rejection]. Zhurnal Mikrobiologii, Epidemiologii, i Immunobiologii, 1, 101–108 (in Russian).

Manandhar, S., Singh, A., Varma, A., Pandey, S., & Shrivastava, N. (2018). Evaluation of methods to detect in vitro biofilm formation by staphylococcal clinical isolates. BMC Research Notes, 11, 714.

McKew, B. A., Taylor, J. D., McGenity, T. J., & Underwood, G. J. C. (2011). Resistance and resilience of benthic biofilm communities from a temperate saltmarsh to desiccation and rewetting. ISME Journal, 5, 30–41.

O'Neill, E., Pozzi, C., Houston, P., Smyth, D., Humphreys, H., Robinson, D. A., & O’Gara, J. P. (2007). Association between methicillin susceptibility and biofilm regulation in Staphylococcus aureus isolates from device-related infections. Journal of Clinical Microbiology, 45(5), 1379–1388.

Paharik, A. E., & Horswill, A. R. (2016). The staphylococcal biofilm: Adhesins, regulation, and host response. Microbiology Spectrum, 4(2), VMBF-0022-2015.

Palchykov, V. A., Zazharskyi, V. V., Brygadyrenko, V. V., Davydenko, P. O., Kulishenko, O. M., Borovik, I. V., Chumak, V., Kryvaya, A., & Boyko, O. O. (2019). Bactericidal, protistocidal, nematodicidal properties and chemical composition of ethanol extract of Punica granatum peel. Biosystems Diversity, 27(3), 300–306.

Patterson, J. L., Stull-Lane, A., Girerd, P. H., & Jefferson, K. K. (2010). Analysis of adherence, biofilm formation and cytotoxicity suggests a greater virulence potential of Gardnerella vaginalis relative to other bacterial-vaginosis-associated anaerobes. Microbiology, 156(2), 392–399.

Rupp, M. E. (2014). Clinical characteristics of infections in humans due to Staphylococcus epidermidis. Methods in Molecular Biology, 1106, 1–16.

Santos, A. P., & Soviero, V. M. (2007). Comparison between a simplified and a conventional biofilm index in relation to caries activity and gingivitis in the primary dentition. European Archives of Paediatric Dentistry, 8(4), 201–205.

Schilcher, K., & Horswill, A. R. (2020). Staphylococcal biofilm development: Structure, regulation, and treatment strategies. Microbiology and Molecular Biology Reviews, 84(3), e00026-19.

Seidl, K., Goerke, C., Wolz, C., Mack, D., Berger-Bächi, B., & Bischoff, M. (2008). Staphylococcus aureus CcpA affects biofilm formation. Infection and Immunity, 76(5), 2044–2050.

Sobkova, Z. V., Filonenko, H. V., Surmasheva, O. V., & Rosada, M. O. (2017). Vyvchennia vydovoho skladu mikroorhanizmiv v bioplivkakh na sudynnykh ta sechovykh kateterakh u bahatoprofilnomu statsionari [Study of the species composition of microorganisms in biofilms on vascular and urinary catheters in a multiprofiled hospital]. Science Rise: Biological Science, 2(5), 38–42 (in Ukrainian).

Sousa, C., Henriques, M., Azeredo, J., Teixeira, P., & Oliveira, R. (2006). Metabolic activity of Staphylococcus epidermidis in biofilm versus planktonic cells. International Conference on BIOFILMS, Leipzig, Germany, 2006 – “BIOFILMS II: Attachment and detachment in pure and mixed cultures”. P. 101.

Stepanovic, S., Vukovic, D., Dakic, I., Savic, B., & Svabic-Vlahovic, M. (2000). A modified microtiter-plate test for quantification of staphylococcal biofilm formation. Journal of Microbiological Methods, 40(2), 175–179.

Sun, F., Qu, F., Ling, Y., Mao, P., Xia, P., Chen, H., & Zhou, D. (2013). Biofilm-associated infections: Antibiotic resistance and novel therapeutic strategies. Future Microbiology, 8(7), 877–886.

Vergara-Irigaray, M., Maira-Litrán, T., Merino, N., Pier, G. B., Penadés, J. R., & Lasa, I. (2008). Wall teichoic acids are dispensable for anchoring the PNAG exopolysaccharide to the Staphylococcus aureus cell surface. Microbiology, 154(3), 865–877.

Voronkova, O. S., & Shevchenko, Т. M. (2017). Influence of different concentrations of sugars on the Stаphylococcus aureus biofilm formation. Social Science and Humanity, 2, 29–36.

Weiner, L. M., Webb, A. K., Limbago, B., Dudeck, M. A., Patel, J., Kallen, A. J., Edwards, J. R., & Sievert, D. M. (2016). Antimicrobial-resistant pathogens associated with healthcare-associated infections: Summary of data reported to the national healthcare safety network at the Centers for Disease Control and Prevention, 2011–2014. Infection Control and Hospital Epidemiology, 37(11), 1288–1301.

Zazharskyi, V. V., Davydenko, P. О., Kulishenko, O. М., Borovik, I. V., & Brygadyrenko, V. V. (2019a). Antimicrobial activity of 50 plant extracts. Biosystems Diversity, 27(2), 163–169.

Zazharskyi, V., Davydenko, P., Kulishenko, O., Borovik, I., Brygadyrenko, V., & Zazharska, N. (2019b). Antibacterial activity of herbal infusions against Staphylococcus aureus, Staphylococcus epidermidis and Pseudomonas aeruginosa in vitro. Magyar Állatorvosok Lapja, 141, 693–704.

Zou, M., & Liu, D. (2020). Effects of carbon sources and temperature on the formation and structural characteristics of food-related Staphylococcus epidermidis biofilms. Food Science and Human Wellness, 9(4), 370–376.

Published
2021-04-25
How to Cite
Vashchenko, A. O., Voronkova, Y. S., Kulyk, E. E., Snisar, O. S., Sidashenko, O. I., & Voronkova, O. S. (2021). Influence of sugars on biofilm formation of Staphylococcus epidermidis . Regulatory Mechanisms in Biosystems, 12(2), 321-325. https://doi.org/10.15421/022143