Skip to main content
Log in

Functionality of the S-layer proteins from Lactobacillus in the competitive against enteropathogens infection

  • Original Paper
  • Published:
European Food Research and Technology Aims and scope Submit manuscript

Abstract

The interest of probiotics as remedy for a broad number of infectious diseases has gained wide interest over the last few years, but little is known about their underlying mechanism of action. In this study, five selected Lactobacillus isolated from human intestinal and ferment milk were preliminarily identified by 16S rDNA gene sequencing and assessed the ability to inhibit the adhesion of enteropathogens using HT-29 cells model through a process which may be related to specific components of the bacterial surface. Surface layer proteins are located in a paracrystalline layer outside the bacterial cell wall and are thought to play a role in tissue adherence. Removal of S-layer proteins from the Lactobacillus (treated with 5 M LiCl) reduced inhibition activity as revealed in exclusion, competition and displacement assays, which suggested that S-layer proteins had involved in the adhesion of probiotics. SDS-PAGE analysis confirmed the presence of S-layer proteins with dominant band which was approximately 60 kDa. Further analysis of S-layer proteins revealed that the hydrophobic amino acids accounted for 43.2 % of the total amino acid for the Lactobacillus paracasei M7. So, these probiotics could be used in the health-promoting food products, which could prevent the diarrhea caused by pathogens.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. FAO/WHO (2002) Joint FAO/WHO working group report on drafting guidelines for the evaluation of probiotics in food. FAO/WHO, London

    Google Scholar 

  2. Guo XH, Kim JM, Nam HM, Park S, Kim JM (2010) Screening lactic acid bacteria from swine origins for multi strain probiotics based on in vitro functional properties. Anaerobe 16:321–326

    Article  Google Scholar 

  3. Castagliuolo I, Galeazzi F, Ferrari S, Elli M, Brun P, Cavaggioni A, Tormen D, Sturniolo GC, Morelli L, Palu G (2005) Beneficial effect of auto-aggregating Lactobacillus crispatus on experimentally indiced colitis in mice. FEMS Immunol Med Microbiol 43:197–204

    Article  CAS  Google Scholar 

  4. Kajander K, Hatakka K, Poussa T, Farkkila M, Korpela RA (2005) probiotic mixture alleviates symptoms in irritable bowel syndrome patients: a controlled 6-month intervention. Aliment Pharmacol Ther 22(5):87–394

    Article  Google Scholar 

  5. Yong Z, Ruiting D, Lifeng W, Heping Z (2010) The antioxidative effects of probiotic Lactobacillus casei Zhang on the hyperlipidemic rats. Eur Food Res Technol 231:151–158

    Article  Google Scholar 

  6. Zsolt Z, Jaroslav H, Jiří S, Jana C, Anna H (2010) Production of organic acids by Lactobacillus strains in three different media. Eur Food Res Technol 230:395–404

    Article  Google Scholar 

  7. Lebeer S, Vanderleyden J, De Keersmaecker SCJ (2008) Genes and molecules of lactobacilli supporting probiotic action. Microbiol Mol Biol Rev 72:728–764

    Article  CAS  Google Scholar 

  8. Fayol-Messaoudi D, Berger CN, Coconnier-Polter MH, Lie′vin-Le Moal V, Servin AL (2005) pH-, lactic acid-, and non lactic acid-dependent activities of probiotic lactobacilli against Salmonella enterica Serovar Typhimurium. Appl Environ Microbiol 71(10):6008–6013

    Article  CAS  Google Scholar 

  9. Baccigalupi L, Donato A, Luongo D, Carbone V, Rossi M, Ricca E, De Felice M, Parlato M (2005) Small surface associated factors mediate adhesion of a food- isolated strain of Lactobacillus fermentum to Caco-2 cells. Res Microbiol 156:830–836

    Article  CAS  Google Scholar 

  10. Bergonzelli GE, Granato D, Pridmore RD, Marvin-Guy LF, Donnicola D, Corthesy-Theulaz IE (2006) GroEl of Lactobacillus johnsonii La1 (NCC533) is cell surface associated: potential role in interactions with the host and the gastric pathogen Helicobacter pylori. Infect Immun 74:425–434

    Article  CAS  Google Scholar 

  11. Corr SC, Hill C, Gahan CGM (2009) Understanding the mechanisms by which probiotics inhibit gastrointestinal pathogens. Adv Food Nutr Res 56:1–15

    Article  CAS  Google Scholar 

  12. Servin AL (2004) Antagonistic activities of lactobacilli and bifidobacteria against microbial pathogens. FEMS Microbiol Rev 28:405–440

    Article  CAS  Google Scholar 

  13. Valerio F, Lavermicocca P, Pascale M, Visconti A (2004) Production of phenyllactic acid by lactic acid bacteria: an approach to the selection of strains contributing to food quality and preservation. FEMS Microbiol Lett 233:289–295

    Article  CAS  Google Scholar 

  14. Velez MP, De Keersmaecker SC, Vanderleyden J (2007) Adherence factors of Lactobacillus in the human gastrointestinalact. FEMS Microbiol Lett 276:140–148

    Article  CAS  Google Scholar 

  15. Buck BL, Altermann E, Svingerud T, Klaenhammer TR (2005) Functional Analysis of putative adhesion factors in Lactobacillus acidophilus NCFM. Appl Environ Microbiol 71(12):8344–8351

    Article  CAS  Google Scholar 

  16. Akhilesh SD, Sandeep BG, Tamishraha B (2011) The ability of Lactobacillus adhesin EF-Tu to interfere with pathogen adhesion. Eur Food Res Technol 232:777–785

    Article  Google Scholar 

  17. Sára M, Sleytr UB (2000) S-layer proteins. J Bacteriol 182:859–868

    Article  Google Scholar 

  18. Åvall-Jääskeläinen S, Palva A (2005) Lactobacillus surface layers and their applications. FEMS Microbiol Rev 29:511–529

    Article  Google Scholar 

  19. Kathene C, Johnson H, Karen EH, Mahsa G, Thomas A, Philip MS (2007) Surface-layer protein extracts from Lactobacillus helveticus inhibit enterohaemorrhagic Escherichia coli O157:H7 adhesion to epithelial cells. Cell Microbiol 9:356–367

    Article  Google Scholar 

  20. Frece J, Kos B, Svetec IK, Zgaga Z, Mrsa V, Šušković J (2005) Importance of S-layer proteins in probiotic activity of Lactobacillus acidophilus M92. J Appl Microbiol 98:285–292

    Article  CAS  Google Scholar 

  21. Kos B, Šušković J, Beganovic′ J, Gjuračić J, Frece J, Iannaccone C, Canganella F (2008) Characterization of the three selected probiotic strains for the application in food industry. World J Microbiol Biotechnol 24:699–707

    Article  CAS  Google Scholar 

  22. Coconnier MH, Liévin V, Lorrot M, Servin AL (2000) Antagonistic activity of Lactobacillus acidophilus LB against intracellular Salmonella enterica serovar typhimurium infecting human enterocyte-like Caco-2/TC-7 cells. Appl Environ Microbiol 66:1152–1157

    Article  CAS  Google Scholar 

  23. Antikainen J, Anton L, Sillanpaa J, Korhonen TK (2002) Domains in the S-layer protein CbsA of Lactobacillus crispatus involved in adherence to collagens, laminin and lipoteichoic acids and in self-assembly. Mol Microbiol 46:381–394

    Article  CAS  Google Scholar 

  24. Vidal K, Donnet-Hughes A, Granato D (2002) Lipoteichoic acids from Lactobacillus johnsonii strain La1 and Lactobacillus acidophilus strain La10 antagonize the responsiveness of human intestinal epithelial HT29 cells to lipopolysaccharide and Gram-negative bacteria. Infect Immun 70:2057–2064

    Article  CAS  Google Scholar 

  25. Gueimonde M, Jalonen L, Hiramatsu HM, Salminen S (2006) Adhesion and competitive inhibition and displacement of human enteropathogens by selected lactobacilli. Food Res Int 39:467–471

    Article  CAS  Google Scholar 

  26. Collado MC, Gueimonde M, Hernandez M, Sanz Y, Salminen S (2005) Adhesion of selected Bifidobacterium strains to human intestinal mucus and the role of adhesion in enteropathogens exclusion. J Food Prot 68:2672–2678

    Google Scholar 

  27. 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

    Article  CAS  Google Scholar 

  28. Ley RE, Peterson DA, Gordon JI (2006) Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 124:837–848

    Article  CAS  Google Scholar 

  29. Šušković J, Šušković J, Kos B, Beganovic′ J, Leboš Pavunc A, Habjanič K (2010) Antimicrobial activity—the most important property of probiotic and starter lactic acid bacteria. Food Technol Biotechnol 48:296–307

    Google Scholar 

  30. Lee YK, Puong KY, Ouwehand AC, Salminen S (2003) Displacement of bacterial pathogens from mucus and Caco-2 cell surface by lactobacilli. J Med Microbiol 52:925–930

    Article  Google Scholar 

  31. Chen XY, Xu JJ, Shuai JB, Chen JS, Zhang ZF, Fang WH (2007) The S-layer proteins of Lactobacillus crispatus strain ZJ001 is responsible for competitive exclusion against Escherichia coli O157: H7 and Salmonella typhimurium. Int J Food Microbiol 115:307–312

    Article  CAS  Google Scholar 

  32. Ni XQ, Gong J, Zeng D, Yu H, Si W, Zhou XQ (2008) Ability of pig lactobacilli strains to inhibit Salmonella Typhimurium DT104 adhesion and invasion on pig intestinal epithelial IPEC-J2 cells. Microbiology 35:1072–1077

    Google Scholar 

  33. Horie M, Ishiyama A, Fujihira-Ueki Y, Sillanpaa J, Korhonen TK, Toba T (2002) Inhibition of the adherence of Escherichia coli strains to basement membrane by Lactobacillus crispatus expressing an S-layer. J Appl Microbiol 92:396–403

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We would like to thank Wei Song for valuable discussions and critical reading of the manuscript. We also thank all my colleagues in the laboratory. This work was supported by Technology of the People’s Republic of China (2007AA10Z354) and the National Natural Science Foundation of China (30900996).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Lanwei Zhang.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Xue, C., Zhang, L., Li, H. et al. Functionality of the S-layer proteins from Lactobacillus in the competitive against enteropathogens infection. Eur Food Res Technol 236, 249–255 (2013). https://doi.org/10.1007/s00217-012-1871-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00217-012-1871-z

Keywords

Navigation