Adhesive properties of film-forming strains of staphylococci, isolated from different compartments of the human gastrointestinal tract

  • T. M. Shevchenko Oles Honchar Dnіpro Natіonal Unіversity
  • O. Y. Hovorukha Oles Honchar Dnіpro Natіonal Unіversity
  • Y. S. Voronkova Oles Honchar Dnіpro Natіonal Unіversity
  • O. S. Voronkova Oles Honchar Dnіpro Natіonal Unіversity
Keywords: Staphylococcus, adhesive properties, biofilm, gastrointestinal tract, dysbiosis


Dysbiotic disorders, realized as changes in the composition of microbiota of different biotopes, are among the most difficult conditions to cure. This is due primarily to the fact that opportunistic microorganisms that actually mediate the development of such states are characterized by an increased colonization potential, which at the first stage of penetration into a biotope is realized as adhesion to the cell surface. When a microorganism successfully realises this stage it enters into a competitive relationship with the autochthonous flora and begins to inhibit its development. Such strategy becomes especially successful if the colonist has the ability to form a biofilm. It is known that the initial stage of biofilm formation is adhesion onto the surface, therefore, the study of adhesive properties of clinical strains opens the way for understanding the initial processes of development of dysbiosis and allows for the development of preventive measures. The aim of our research was to investigate the differences in the manifestation of adhesive properties of film-forming strains of staphylococci isolated from different compartments of the human gastrointestinal tract. We established that the frequency of detection of film-forming strains of staphylococci in different compartments of the gastrointestinal tract in the norm or during the development of lesions was for Staphylococcus aureus from 23.8% to 79.4%, and for S. epidermidis from 15.4% to 100%, which indicates the significant role of these microorganisms in the development of complications at the specified biotope. It was determined that the maximal manifestation of adhesive properties was typical for biofilm-forming strains of S. epidermidis and S. aureus isolated during intestinal dysbiosis. The average values of the adhesion index were 6.00 ± 1.41 and 5.88 ± 2.22 and the index of adhesion of microorganisms was 6.61 ± 1.46 and 6.64 ± 2.48 respectively. The lowest value of these indices for film-forming strains was determined for strains of staphylococci isolated from the gastrointestinal tracts of patients suffering from food poisoning – 2.60 ± 1.14 and 2.86 ± 1.23 respectively. The obtained data suggest that the ability for biofilm-formation and a high level of adhesion indexes indicate with a high probability that a strain will cause long-lasting lesions, such as dysbiosis. The determination of these markers at the diagnostic stage will allow a broader study of the biological properties of the strain, which may be the basis for the development of an individual, optimal therapeutic scheme that conforms with the tasks of personalized medicine. 


Akinkunmi, E. O., Adeyemi, O. I., Igbeneghu, O. A., Olaniyan, E. O., Omonisi, A. E., & Lamikanra, A. (2014). The pathogenicity of Staphylococcus epidermidis on the intestinal organs of rats and mice: An experimental investigation. BMC Gastroenterology, 14, 126.

Archer, N. K., Mazaitis, M. J., Costerton, J. W., Leid, J. G., Powers, M. E., & Shirtliff, M. E. (2011). Staphylococcus aureus biofilms: Properties, regulation, and roles in human disease. Virulence, 2(5), 445–459.

Becker, K., Heilmann, C., & Peters, G. (2014). Coagulase-negative Staphylococci. Clinical Microbiology Reviews, 27(4), 870–926.

Brilis, V. I., Brilene, T. A., Lentsner, H. P., & Lentsner, A. A. (1986). Metodika izucheniya adgezivnogo protsessa mikroorganizmov [Method for studying the adhesive process of microorganisms]. Laboratornoe Delo, 4, 210–212 (in Russian).

Buharin, O. V. (2009). Infektsiya – modelnaya sistema assotsiativnogo simbioza [Infection is a model system of associative symbiosis]. Journal of Microbiology, Epidemiology and Immunobiology, 1, 83–86 (in Russian).

Giaouris, E., Heir, E., Desvaux, M., Hebraud, M., Mеretrе, T., Langsrud, S., Doulgeraki, A., Nychas, G.-J., Kacaniova, M., Czaczyk, K., Olmez, H., & Simoes, M. (2015). Intra- and inter-species interactions within biofilms of important foodborne bacterial pathogens. Frontiers in Microbiology, 6, 841.

Gostev, V. V., & Sidorenko, S. V. (2012). Bakterialnyie bioplenki i infektsii [Bacterial biofilms and infections]. Journal of Infectology, 2(3), 4–15 (in Russian).

Hobley, L., Harkins, C., MacPhee, C. E., & Stanley-Wall, N. R. (2015). Giving structure to the biofilm matrix: An overview of individual strategies and emerging common themes. FEMS Microbiology Reviews, 39(5), 649–669.

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

Holt, J. G., Кrieg, N. R., Sneath, P. H. A., Staley, J. T., & Williams, S. T. (Eds.). (1994). Bergey’s manual of determinative bacteriology. Williams & Wilkins, Baltimore.

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.

Kovalenko, N. K., Livinska, O. P., Poltavska, O. A., Garmasheva, I. L., Shinkarenko, L. M., & Oleshchenko, L. T. (2010). Probiotychni vlastyvosti promyslovykh shtamiv laktobatsyl i bifidobakteriy [Probiotic properties of industrial strains of lactobacilli and bifidobacteria]. Microbiologichny Zhurnal, 72(1), 9–17 (in Ukrainian).

Labinskaia, А. S., & Volina, Y. H. (Eds.). (2008). Rukovodstvo po medicinskoi mikrobiolohii. Obshaia i sanitarnaia mikrobiolohiia [Manual of medical microbiology. General and sanitary microbiology]. Binom, Мoscow (in Russian).

Lin, M. H., Shu, J. C., Lin, L. P., Chong, K. Y., Cheng, Y. W., Du, J. F., & Liu, S. T. (2015). Elucidating the crucial role of poly N-acetylglucosamine from Staphylococcus aureus in cellular adhesion and pathogenesis. PLoS One, 10(4), e0124216.

Lyamin, A. V., Botkin, E. A., & Zhestkov, A. V. (2012). Metodyi vyiyavleniya bioplenok v meditsine: Vozmozhnosti i perspektivyi [Methods of biofilm evaluation: Opportunities and perspectives]. Clinical Microbiology and Antimicrobial Chemotherapy, 14(1), 17–22 (in Russian).

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

Misawa, Y., Kelley, K. A., Wang, X., Wang, L., Park, W. B., Birtel, J., Saslowsky, D., & Lee, J. C. (2015). Staphylococcus aureus colonization of the mouse gastrointestinal tract is modulated by wall teichoic acid, capsule, and surface proteins. PLOS Pathogens, 11(7), e1005061.

Moormeier, D. E., Bose, J. L., Horswill, A. R., & Bayles, K. W. (2014). Temporal and stochastic control of Staphylococcus aureus biofilm development. mBio, 5(5), e01341-14.

Murashkin, N., Gluzmin, M., Skoblikow, N., Bakulev, A., Materikin, A., Gluzmina, M., & Khotko, A. (2012). Rol metitsillinrezistentnyih shtammov zolotistogo stafilokokka v patogeneze tyazhelyih form atopicheskogo dermatita v detskom vozraste. Puti dostizheniya remissii [Role of MRSA strains in the pathogenesis of severe atopic dermatitis in childhood. Ways of achieving remission]. Vestnik Dermatologii i Venerologii, 1, 66–74 (in Russian).

Nair, N., Biswas, R., Gotz, F., & Biswas, L. (2014). Impact of Staphylococcus aureus on pathogenesis in polymicrobial infections. Infection and Immunity, 82(6), 2162–2169.

Naumenko, Z. S., & Shipitsyna, I. V. (2011). Sravnitelnaya otsenka adgezivnoy aktivnosti bakteriy, vyidelennyih u bolnyih iz osteomieliticheskogo ochaga i iz ran otkryityih perelomov [Comparative evaluation of adhesive activity of the bacterii, isolated in patients from their osteomyelitic focus, as well as from open fracture wounds]. Orthopaedic Genius, 4, 31–34 (in Russian).

Nishihara, T., & Koseki, T. (2004). Microbial etiology of periodontitis. Periodontology, 36, 14–26.

Orazi, G., & O’Toole, G. A. (2017). Pseudomonas aeruginosa alters Staphylococcus aureus sensitivity to vancomycin in a biofilm model of cystic fibrosis infection. mBio, 8(4), e00873-17.

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

Paster, B. J., Boches, S. K., Galvin, J. L., Ericson, R. E., Lau, C. N., Levanos, V. A., Sahasrabudhe, A., & Dewhirst, F. E. (2001). Bacterial diversity in human subgingival plaque. Journal of Bacteriology, 183(12), 3770–3783.

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, 392–399.

Ponomarenko, S. V., Voronkina, I. A., Osolodchenko, T. P., Port, О. V., & Pirtskhalava, T. V. (2014). Zdatnist do bioplivkoutvorennya izolyativ S. aureus, vydilenykh z riznykh ekonish [The ability to biofilm formation isolates S. aureus, received by different ecological niches]. Bulletin of Problems Biology and Medicine, 112, 245–248 (in Ukrainian).

Sannasiddappa, T. H., Costabile, A., Gibson, G. R., & Clarke, S. R. (2011). The influence of Staphylococcus aureus on gut microbial ecology in an in vitro continuous culture human colonic model system. PLoS One, 6(8), e23227.

Tchebotar, I. V., & Guryev, E. L. (2012). Laboratornaya diagnostika klinicheski znachimyih bioplyonochnyih protsessov [Laboratory diagnostics of clinically significant microbial biofilms]. Voprosyi Diagnostiki v Pediatrii, 4, 15–20 (in Russian).

Tsarev, V., Trefilov, A., Kleymenova, G., & Levkin, A. (2011). Prostranstvenno-vremennaya model formirovaniya bioplyonki polosti rta: Vzaimosvyaz protsessov pervichnoy adgezii i mikrobnoy kolonizatsii [The space-time model of oral biofilm formation: The interrelation of primary adhesion and microbial colonization]. Sovremennaya Stomatologiya, 2, 22–27 (in Russian).

Wright, C. J., Burns, L. H., Jack, A. A., Back, C. R., Dutton, L. C., Nobbs, A. H., Lamont, R. J., & Jenkinson, H. F. (2013). Microbial interactions in building of communities. Molecular Oral Microbiology, 28(2), 83–101.

How to Cite
Shevchenko, T. M., Hovorukha, O. Y., Voronkova, Y. S., & Voronkova, O. S. (2017). Adhesive properties of film-forming strains of staphylococci, isolated from different compartments of the human gastrointestinal tract. Regulatory Mechanisms in Biosystems, 8(4), 527–531.