Health-promoting properties exhibited by Lactobacillus helveticus strains
Languages of publication
Many strains belonging to lactobacilli exert a variety of beneficial health effects in humans and some of the bacteria are regarded as probiotic microorganisms. Adherence and capabilities of colonization by Lactobacillus strains of the intestinal tract is a prerequisite for probiotic strains to exhibit desired functional properties. The analysis conducted here aimed at screening strains of Lactobacillus helveticus possessing a health-promoting potential. The molecular analysis performed, revealed the presence of a slpA gene encoding the surface S-layer protein SlpA (contributing to the immunostimulatory activity of L. helveticus M 92 probiotic strain) in all B734, DSM, T80, and T105 strains. The product of gene amplification was also identified in a Bifidobacterium animalis ssp. lactis BB12 probiotic strain. SDS-PAGE of a surface protein extract demonstrated the presence of a protein with a mass of about 50 kDa in all strains, which refers to the mass of the S-layer proteins. These results are confirmed by observations carried with transmission electron microscopy, where a clearly visible S-layer was registered in all the strains analyzed. The in vitro study results obtained indicate that the strongest adhesion capacity to epithelial cells (HT-29) was demonstrated by L. helveticus B734, while coaggregation with pathogens was highly diverse among the tested strains. The percentage degree of coaggregation was increasing with the incubation time. After 5 h of incubation, the strongest ability to coaggregate with Escherichia coli was expressed by T104. The T80 strain demonstrated a significant ability to co-aggregate with Staphylococcus aureus, while DSM with Bacillus subtilis. For B734, the highest values of co-aggregation coefficient was noted in samples with Salmonella. The capability of autoaggregation, antibiotic susceptibility, resistance to increasing salt concentrations, and strain survival in simulated small intestinal juice were also analyzed.
- Avall-Jääskeläinen S, Palva A (2005) Lactobacillus surface layers and their applications. FEMS Microbiol Rev 29: 511-29.
- Beganović J, Frece J, Kos B, Leboš Pavunc A, Habjanič K, Šušković J (2011a) Functionality of the S-layer protein from the probiotic strain Lactobacillus helveticus M92. Antonie van Leeuwenhoek 100: 43-53.
- Beganović J, Kos B, Leboš Pavunc A, Uroić K, Jokić M, Šušković J (2014) Traditionally produced sauerkraut as source of autochthonous functional starter cultures. Microbiol Res 169: 623-632.
- Beganović J, Pavunc AL, Gjuračić K, Spoljarec M, Sušković J, Kos B (2011b) Improved sauerkraut production with probiotic strain Lactobacillus plantarum L4 and Leuconostoc mesenteroides LMG 7954. J Food Sci 76: M124-M129.
- Buck BL, Altermann E, Svingerud T, Klaenhammer TR (2005) Functional analysis of putative adhesion factors in Lactobacillus acidophilus NCFM. Appl Environ Microbiol 71: 8344-8351.
- Castagliuolo I, Galeazzi F, Ferrari S, Elli M, Brun P, Cavaggioni A, Tormen D, Sturniolo GC, Morelli L, Palù G (2005) Beneficial effect of auto-aggregating Lactobacillus crispatus on experimentally induced colitis in mice. FEMS Immunol Med Microbiol 43: 197-204.
- Delcour J, Ferain T, Deghorain M, Palumbo E, Hols P (1999) The biosynthesis and functionality of the cell-wall of lactic acid bacteria. Antonie van Leeuwenhoek 76: 159-184.
- European Food Safety Authority (2008) Technical guidance prepared by the Panel on Additives and Products or Substances Used in Animal Feed (FEEDAP) on the update of the criteria used in the assessment of bacterial resistance to antimicrobials of human or veterinary importance. EFSA J 732: 1-15
- Ferreira CL, Grześkowiak L, Collado MC, Salminen S (2011) In vitro evaluation of Lactobacillus gasseri strains of infant origin on adhesion and aggregation of specific pathogens. J Food Prot 74: 1482-1487.
- Frece J, Kos B, Svetec IK, Zgaga Z, Mrsa V, Susković J (2005) Importance of S-layer proteins in probiotic activity of Lactobacillus acidophilus M92. J Appl Microbiol 98: 285-292.
- Gatti M, Fornasari E, Neviani E (1997) Cell-wall protein profiles of dairy thermophilic lactobacilli. Lett Appl Microbiol 25: 345-348.
- Giraffa G (2014) Lactobacillus helveticus: importance in food and health. Front Microbiol 5: 338,
- Golowczyc MA, Mobili P, Garrote GL, Abraham AG, De Antoni GL (2007) Protective action of Lactobacillus kefir carrying S-layer protein against Salmonella enterica serovar Enteritidis. Int J Food Microbiol 118: 264-273.
- Gopal PK, Prasad J, Smart J, Gill HS (2001) In vitro adherence properties of Lactobacillus rhamnosus DR20 and Bifidobacterium lactis DR10 strains and their antagonistic activity against an enterotoxigenic Escherichia coli. Int J Food Microbiol 67: 207-216.
- Gueimonde M, Jalonen L, He F, Hiramatsu M, Salminen S (2006) Adhesion and competitive inhibition and displacement of human enteropathogens by selected lactobacilli. Food Res Int 39: 467-471.
- Hynönen U, Palva A (2013) Lactobacillus surface layer proteins: structure, function and applications. Appl Microbiol Biotechnol 97: 5225-5243.
- Johnson-Henry KC, Hagen KE, Gordonpour M, Tompkins TA, Sherman PM (2007) Surface-layer protein extracts from Lactobacillus helveticus inhibit enterohaemorrhagic Escherichia coli O157:H7 adhesion to epithelial cells. Cell Microbiol 9: 356-367.
- Kos B, Susković J, Vuković S, Simpraga M, Frece J, Matosić S (2003) Adhesion and aggregation ability of probiotic strain Lactobacillus acidophilus M92. J Appl Microbiol 94: 981-987.
- Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
- Lebeer S, Vanderleyden J, De Keersmaecker SC (2008) Genes and molecules of lactobacilli supporting probiotic action. Microbiol Mol Biol Rev 72: 728-764.
- Liu TS, Zhang P, Ma Y, Qin H (2010) Lactobacillus plantarum surface layer adhesive protein protects intestinal epithelial cells against tight junction injury induced by enteropathogenic Escherichia coli. Mol Biol Rep 38: 3471-3480.
- Macfarlane GT, Macfarlane S, Gibson GR (1998) Validation of a three-stage compound continuous culture system for investigating the effect of retention time on the ecology and metabolism of bacteria in the human colon. Microb Ecol 35: 180-187.
- Matto J, Fondén R, Tolvanen T, von Wright Atte, Vilpponen-Salmela T, Satokari R, Saarela M (2006) Intestinal survival and persistence of probiotic Lactobacillus and Bifidobacterium strains administered in triple-strain yoghurt. Int Dairy J 16: 1174-1180.
- Mobili P, Serradell Mde L, Trejo SA, Avilés Puigvert FX, Abraham AG, De Antoni GL (2009) Heterogeneity of S-layer proteins from aggregating and non-aggregating Lactobacillus kefir strains. Antonie van Leeuwenhoek 95: 363-372.
- Nazzaro F, Fratianni F, Nicolaus B, Poli A, Orlando P (2012) The prebiotic source influences the growth, biochemical features and survival under simulated gastrointestinal conditions of the probiotic Lactobacillus acidophilus. Anaerobe 18: 280-285.
- Nikolic M, Jovcic B, Kojic M, Topisirovic L (2010) Surface properties of Lactobacillus and Leuconostoc isolates from homemade cheeses showing autoaggregation ability. Eur Food Res Technol 231: 925-931.
- Nikolic M, López P, Strahinic I, Suárez A, Kojic M, Fernández-García M, Topisirovic L, Golic N, Ruas-Madiedo P (2012) Characterisation of the exopolysaccharide (EPS)-producing Lactobacillus paraplantarum BGCG11 and its non-EPS producing derivative strains as potential probiotics. Int J Food Microbiol 158: 155-162.
- Ocaña VS, Nader-Macías ME (2002) Vaginal lactobacilli: self- and co-aggregating ability. Br J Biomed Sci 59: 183-190.
- Ongol MP, Iguchi T, Tanaka M, Sone T, Ikeda H, Asano K, Nishimura T (2008) Potential of selected strains of lactic acid bacteria to induce a Th1 immune profile. Biosci Biotechnol Biochem 72: 2847-2857.
- Perdigon G, Maldonado GC, Valdez JC, Medici M (2002) Interaction of lactic acid bacteria with the gut immune system. Eur J Clin Nutr 56 Suppl 4: S21-S26.
- Polak-Berecka M, Waśko A, Paduch R, Skrzypek T, Sroka-Bartnicka A (2014) The effect of cell surface components on adhesion ability of Lactobacillus rhamnosus. Antonie Van Leeuwenhoek 106: 751-762.
- Polak-Berecka M, Waśko A, Szwajgier D, Choma A (2013) Bifidogenic and antioxidant activity of exopolysaccharides produced by Lactobacillus rhamnosus E/N on different carbon sources. Pol J Microbiol 62: 181-189.
- Ramiah K, van Reenen CA, Dicks LM (2008) Surface-bound proteins of Lactobacillus plantarum 423 that contribute to adhesion of Caco-2 cells and their role in competitive exclusion and displacement of Clostridium sporogenes and Enterococcus faecalis. Res Microbiol 159: 470-475.
- Rogers TR (2002) Antifungal drug resistance: does it matter? Int J Infect Dis 6: S47-S53.
- Rosenfeldt V, Pærregaard A, Larsen CN, Møller PL, Tvede M, Sandström B, Jakobsen M, Michaelsen KF (2003) Faecal recovery, mucosal adhesion, gastrointestinal effects and tolerance of mixed cultures of potential probiotic lactobacilli. Microb Ecol Health D 5: 2-9.
- Servin AL, Coconnier MH (2003) Adhesion of probiotic strains to the intestinal mucosa and interaction with pathogens. Best Pract Res Clin Gastroenterol 17: 741-754.
- Sherman PM, Johnson-Henry KC, Yeung HP, Ngo PS, Goulet J, Tompkins TA (2005) Probiotics reduce enterohemorrhagic Escherichia coli O157H7: H7-induced changes in polarized T84 epithelial cell monolayers by reducing bacterial adhesion and cytoskeletal rearrangements. Infect Immun 73: 5183-5188.
- Taverniti V, Guglielmetti S (2012) Health-promoting properties of Lactobacillus helveticus. Front Microbiol 3: 392,
- Todorov SD, Botes M, Guigas C, Schillinger U, Wiid I, Wachsman MB, Holzapfel WH, Dicks LM (2008) Boza, a natural source of probiotic lactic acid bacteria. J Appl Microbiol 104: 465-477.
- van der Mei HC, van de Belt-Gritter B, Pouwels PH, Martinez B, Busscher HJ (2003) Cell surface hydrophobicity is conveyed by S-layer: a study in recombinant lactobacilli. Colloids Surf B 28: 127-134
- Vlková E, Rada V, Smehilová M, Killer J (2008) Auto-aggregation and co-aggregation ability in bifidobacteria and clostridia. Folia Microbiol (Praha) 53: 263-269.
- von Ossowski I, Reunanen J, Satokari R, Vesterlund S, Kankainen M, Huhtinen H, Tynkkynen S, Salminen S, de Vos WM, Palva A (2010) Mucosal adhesion properties of the probiotic Lactobacillus rhamnosus GG SpaCBA and SpaFED pilin subunits. Appl Environ Microbiol 76: 2049-2057.
- Waśko A, Szwajgier D, Polak-Berecka M (2014) The role of ferulic acid esterase in the growth of Lactobacillus helveticus in the presence of phenolic acids and their derivatives. Eur Food Res Technol 238: 299-236.
- Wiatrzyk A, Polak M, Czajka U, Krysztopa-Grzybowska K, Lutyńska A (2013) Phenotypic and genotypic characterization of probiotic bacterial strains used in medicinal products. Med Dosw Mikrobiol 65: 47-56.
Publication order reference