Archives of Microbiology

, Volume 197, Issue 8, pp 1027–1032 | Cite as

Inhibitory effects of Lactobacillus fermentum on microbial growth and biofilm formation

  • Oxana V. Rybalchenko
  • Viktor M. Bondarenko
  • Olga G. Orlova
  • Alexander G. Markov
  • S. AmashehEmail author
Original Paper


Beneficial effects of Lactobacilli have been reported, and lactic bacteria are employed for conservation of foods. Therefore, the effects of a Lactobacillus fermentum strain were analyzed regarding inhibitory effects on staphylococci, Candida albicans and enterotoxigenic enterobacteria by transmission electron microscopy (TEM). TEM of bacterial biofilms was performed using cocultures of bacteriocin-producing L. fermentum 97 with different enterotoxigenic strains: Staphylococcus epidermidis expressing the ica gene responsible for biofilm formation, Staphylococcus aureus producing enterotoxin type A, Citrobacter freundii, Enterobacter cloaceae, Klebsiella oxytoca, Proteus mirabilis producing thermolabile and thermostable enterotoxins determined by elt or est genes, and Candida albicans. L. fermentum 97 changed morphological features and suppressed biofilm formation of staphylococci, enterotoxigenic enterobacteria and Candida albicans; a marked transition to resting states, a degradation of the cell walls and cytoplasm, and a disruption of mature bacterial biofilms were observed, the latter indicating efficiency even in the phase of higher cell density.


Biofilm destruction Lactobacillus fermentum 97 Enterotoxigenic enterobacteria Staphylococcus 



This research was sponsored by St. Petersburg State University Grant, by Russian Foundation for Basic Research Grant 13-04-01107, and by the Center of International Cooperation of Freie Universität Berlin.


  1. Belfiore C, Castellano P, Vignolo G (2007) Reduction of Escherichia coli population following treatment with bacteriocins from lactic acid bacteria and chelators. J Food Microbiol 24:223–229CrossRefGoogle Scholar
  2. Cotter PJ, Hill S, Ross RP (2005) Bacteriocins: developing innate immunity for food. Nat Rev Microbiol 3:777–788CrossRefPubMedGoogle Scholar
  3. De Vos WM, Kuipers JR, Van der Meer JR, Slesen RJ (1995) Maturation pathway of nisin and other lantibiotics: post-translationally modified antimicrobial peptides exported by gram-positive bacteria. Mol Microbiol 17:427–437CrossRefPubMedGoogle Scholar
  4. Diep DB, Nes IF (2002) Ribosomally synthesized antibacterial peptides in gram-positive bacteria. Curr Drug Targets 3:107–122CrossRefPubMedGoogle Scholar
  5. Donlan RM, Costerton JW (2002) Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev 15:167–193PubMedCentralCrossRefPubMedGoogle Scholar
  6. Garver KI, Muriana PM (1993) Detection, identification and characterization of bacteriocin-producing lactic acid bacteria from retail food products. Int J Food Microbiol 19:241–258CrossRefPubMedGoogle Scholar
  7. Holm A, Vikström E (2014) Quorum sensing communication between bacteria and human cells: signals, targets, and functions. Front Plant Sci 5:309. doi: 10.3389/fpls.2014.00309 PubMedCentralCrossRefPubMedGoogle Scholar
  8. Knobloch JK, Jäger S, Horstkotte MA, Rohde H, Mack D (2004) Rsb U-dependent regulation of Staphylococcus epidermidis biofilm formation is mediated via the alternative sigma factor sigma B by repression of the negative regulator gene ica R. Infect Immun 72:3838–3848PubMedCentralCrossRefPubMedGoogle Scholar
  9. Kouakou P, Dortu C, Dubois-Dauphin R, Vandenbol M, Thonart P (2010) Plasmid-associated bacteriocin production by Lactobacillus LMG21688 suppresses Listeria monocytogenes growth rebound in a food system. FEMS Microbiol Lett 306:37–44CrossRefPubMedGoogle Scholar
  10. Lebeer S, Vanderleydes G, De Keersmaecker SCJ (2008) Genes and molecules of Lactobacillus supporting probiotic action. Microbiol Mol Biol Rev 72:728–764PubMedCentralCrossRefPubMedGoogle Scholar
  11. Lim Y, Jana M, Luong TT, Lee CY (2004) Control of glucose- and NaCl-induced biofilm formation by rbf in Staphylococcus aureus. J Bacteriol 186:722–729PubMedCentralCrossRefPubMedGoogle Scholar
  12. Macfarlane S (2008) Microbial biofilm communities in the gastrointestinal tract. J Clin Gastroenterol 42:S142–S143CrossRefPubMedGoogle Scholar
  13. Madden JA, Plummer SF, Tang J, Garaiova I et al (2005) Effect of probiotics on preventing disruption of the intestinal microflora following antibiotic therapy: a double-blind, placebo-controlled pilot study. Int Immunopharmacol 5:1091–1097CrossRefPubMedGoogle Scholar
  14. Manzoni P (2007) Use of Lactobacillus casei subspecies Rhamnosus GG and gastrointestinal colonization by Candida species in preterm neonates. J Pediatr Gastroenterol Nutr 45:S190–S194CrossRefPubMedGoogle Scholar
  15. Miller MB, Bassler BL (2001) Quorum sensing in bacteria. Ann Rev Microbiol 55:165–199CrossRefGoogle Scholar
  16. Nielsen DS, Moller PL, Rosenfeld V, Paerregaard A et al (2003) Case study of the distribution of mucosa-associated Bifidobacterium species, Lactobacillus species, and other lactic acid bacteria in the human colon. Appl Environ Microbiol 69:7545–7548PubMedCentralCrossRefPubMedGoogle Scholar
  17. O’Gara JP (2007) Ica and beyond: biofilm mechanism and regulation in Staphylococcus epidermidis and Staphylococcus aureus. FEMS Microbiol Lett 270:179–188CrossRefPubMedGoogle Scholar
  18. Pinto TS, de Oliveira CP, da Costa AC, Lima CO et al (2013) Evidence for production of a bacteriocin-like substance by Staphylococcus pseudintermedius, inhibitory to Staphylococcus aureus from foods. Nat Prod Res 27:1098–1101CrossRefPubMedGoogle Scholar
  19. Rivas-Santiago B, Serrano CJ, Ensico-Moreno JA (2009) Susceptibility to infectious diseases based on antimicrobial peptide production. Infect Immun 77:4690–4695PubMedCentralCrossRefPubMedGoogle Scholar
  20. Rybalchenko OV (2006) The electron microscopic study of cell-to-cell interactions between antagonistic microorganisms. Mikrobiologiia 75:550–555Google Scholar
  21. Rybalchenko OV, Bondarenko VM, Orlova OG, Larionov IV, Fialkina SV (2010) Disorganization of biofilms of clinical strains of staphylococci by metabolites of lactobacilli. Zh Mikrobiol Epidemiol Immunobiol 6:66–70Google Scholar
  22. Rybalchenko OV, Bondarenko VM, Orlova OG (2014) Ultrastructure of microbial biofilms during interspecies and intraspecies interactions of bacteria in communities. Zh Mikrobiol Epidemiol Immunobiol 2:97–101Google Scholar
  23. Sadowska B, Walencka E, Wieckowska-Szakiel M, Różalska B (2010) Bacteria competing with the adhesion and biofilm formation by Staphylococcus aureus. Folia Microbiol 55:497–501CrossRefGoogle Scholar
  24. Swidsinski A, Weber J, Loening-Baucke V, Hale LP, Lochs H (2005) Spatial organization and composition of the mucosal flora in patients with inflammatory bowel disease. J Clin Microbiol 43:3380–3389PubMedCentralCrossRefPubMedGoogle Scholar
  25. Tagg JR, Bannister LV (1979) ‘Fingerprinting’ ß-haemolytic streptococci by their production of and sensitivity to bacteriocine-like inhibitors. J Med Microbiol 12:397–411CrossRefPubMedGoogle Scholar
  26. Tenke P, Köves B, Nagy K, Hultgren SJ et al (2012) Update on biofilm infections in the urinary tract. World J Urol 30:51–57CrossRefPubMedGoogle Scholar
  27. Tormo MA, Martí M, Valle J, Manna AC et al (2005) SarA is an essential positive regulator of Staphylococcus epidermidis biofilm development. J Bacteriol 187:2348–2356PubMedCentralCrossRefPubMedGoogle Scholar
  28. Tuma P, Hubbard AL (2003) Transcytosis: crossing cellular barriers. Physiol Rev 83:871–932CrossRefPubMedGoogle Scholar
  29. Turovskiy Y, Ludescher RD, Aroutcheva AA, Faro S, Chikindas ML (2009) Lactocin 160, a bacteriocin produced by vaginal Lactobacillus rhamnosus, targets cytoplasmic membranes of the vaginal pathogen, Gardnerella vaginalis. Probiotics Antimicrob Proteins 1:67–74PubMedCentralCrossRefPubMedGoogle Scholar
  30. Zaeim D, Soleimanian-Zad S, Sheikh-Zeinoddin M (2014) Identification and partial characterization of a bacteriocin-like inhibitory substance (BLIS) from Lb. bulgaricus K41 isolated from indigenous yogurts. J Food Sci 79:M67–M73CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Oxana V. Rybalchenko
    • 1
  • Viktor M. Bondarenko
    • 2
  • Olga G. Orlova
    • 1
  • Alexander G. Markov
    • 3
  • S. Amasheh
    • 4
    Email author
  1. 1.Faculty of MedicineSt. Petersburg State UniversitySt. PetersburgRussia
  2. 2.Gamaleya Research Institute of Epidemiology and MicrobiologyMoscowRussia
  3. 3.Institute of General PhysiologySt. Petersburg State UniversitySt. PetersburgRussia
  4. 4.Institute of Veterinary PhysiologyFreie Universität BerlinBerlinGermany

Personalised recommendations