Hostname: page-component-78c5997874-4rdpn Total loading time: 0 Render date: 2024-11-10T07:58:54.377Z Has data issue: false hasContentIssue false
  • English
  • Français

Adhesion properties of potentially probiotic Lactobacillus kefiri to gastrointestinal mucus

Published online by Cambridge University Press:  29 October 2013

Paula Carasi ,
Nicolás M. Ambrosis ,
Graciela L. De Antoni ,
Philippe Bressollier ,
María C. Urdaci  and
María de los Angeles Serradell
Paula Carasi
Affiliation:
Cátedra de Microbiología, Departamento de Ciencias Biológicas, Facultad de Ciencias Exactas, Universidad Nacional de La Plata, Argentina Laboratoire de Microbiologie et Biochimie Appliquée (LBMA), Université de Bordeaux, UMR 5248 CNRS, Bordeaux Sciences Agro, Gradignan, France
Nicolás M. Ambrosis
Affiliation:
Cátedra de Microbiología, Departamento de Ciencias Biológicas, Facultad de Ciencias Exactas, Universidad Nacional de La Plata, Argentina
Graciela L. De Antoni
Affiliation:
Cátedra de Microbiología, Departamento de Ciencias Biológicas, Facultad de Ciencias Exactas, Universidad Nacional de La Plata, Argentina Centro de Investigación y Desarrollo en Criotecnología de Alimentos (CIDCA), CCT La Plata, CONICET, Argentina
Philippe Bressollier
Affiliation:
Laboratoire de Microbiologie et Biochimie Appliquée (LBMA), Université de Bordeaux, UMR 5248 CNRS, Bordeaux Sciences Agro, Gradignan, France Laboratoire de Génie Enzymatique et Biovalorisation, Université de Limoges, IUT, Limoges, France
María C. Urdaci
Affiliation:
Laboratoire de Microbiologie et Biochimie Appliquée (LBMA), Université de Bordeaux, UMR 5248 CNRS, Bordeaux Sciences Agro, Gradignan, France
María de los Angeles Serradell*
Affiliation:
Cátedra de Microbiología, Departamento de Ciencias Biológicas, Facultad de Ciencias Exactas, Universidad Nacional de La Plata, Argentina
*
*For correspondence; e-mail: maserr@biol.unlp.edu.ar
Get access Rights & Permissions [Opens in a new window]

Abstract

We investigated the mucus-binding properties of aggregating and non-aggregating potentially probiotic strains of kefir-isolated Lactobacillus kefiri, using different substrates. All the strains were able to adhere to commercial gastric mucin (MUCIN) and extracted mucus from small intestine (SIM) and colon (CM). The extraction of surface proteins from bacteria using LiCl or NaOH significantly reduced the adhesion of three selected strains (CIDCA 8348, CIDCA 83115 and JCM 5818); although a significant proportion (up to 50%) of S-layer proteins were not completely eliminated after treatments. The surface (S-layer) protein extracts from all the strains of Lb. kefiri were capable of binding to MUCIN, SIM or CM, and no differences were observed among them. The addition of their own surface protein extract increased adhesion of CIDCA 8348 and 83115 to MUCIN and SIM, meanwhile no changes in adhesion were observed for JCM 5818. None of the seven sugars tested had the ability to inhibit the adhesion of whole bacteria to the three mucus extracts. Noteworthy, the degree of bacterial adhesion reached in the presence of their own surface protein (S-layer) extract decreased to basal levels in the presence of some sugars, suggesting an interaction between the added sugar and the surface proteins. In conclusion, the ability of these food-isolated bacteria to adhere to gastrointestinal mucus becomes an essential issue regarding the biotechnological potentiality of Lb. kefiri for the food industry.

Keywords

Lactobacillus kefirimucuskefirsurface proteins
Type
Research Article
Information
Journal of Dairy Research , Volume 81 , Issue 1 , February 2014 , pp. 16 - 23
Copyright
Copyright © Proprietors of Journal of Dairy Research 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Antikainen, J, Antón, L, Sillanpaa, J & Coronen, TK 2002 Domains in the S-layer protein CbsA of Lactobacillus crispatus involved in adherence to collagens, laminin and lipoteichoic acids and self-assembly. Molecular Microbiology 2 381–394 CrossRefGoogle Scholar
Avall-Jääskeläinen, S, Lindholm, A & Palva, A 2003 Surface display of the receptor-binding region of the Lactobacillus brevis S-layer protein in Lactococcus lactis provides nonadhesive lactococci with the ability to adhere to intestinal epithelial cells. Applied and Environmetal Microbiology 69 2230–2236 CrossRefGoogle ScholarPubMed
Bradford, MM 1976 A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72 248–254 CrossRefGoogle ScholarPubMed
Buck, BL, Altermann, E, Svingerud, T & Klaenhammer, TM 2005 Functional analysis of putative adhesion factors in Lactobacillus acidophilus NCFM. Applied and Environmental Microbiology 71 8344–8351 CrossRefGoogle ScholarPubMed
Carasi, P, Trejo, FM, Pérez, PF, De Antoni, GL & Serradell, MA 2012 Surface proteins from Lactobacillus kefir antagonize in vitro cytotoxic effect of Clostridium difficile toxins. Anaerobe 18 135–142 CrossRefGoogle ScholarPubMed
Chan, RC, Reid, G, Irvin, RT, Bruce, AW & Costerton, JW 1985 Competitive exclusion of uropathogens from human uroepithelial cells by Lactobacillus whole cells and cell wall fragments. Infection and Immunity 47 84–89 CrossRefGoogle ScholarPubMed
Conway, PL, Welin, A & Cohen, PS 1990 Presence of K88-specific receptors in porcine ileal mucus is age dependent. Infection and Immunity 58 3178–3182 CrossRefGoogle ScholarPubMed
Deepika, G & Charalampopoulos, D 2010 Surface and adhesion properties of lactobacilli. Advances in Applied Microbiology 70 127–152 CrossRefGoogle ScholarPubMed
De Leeuw, E, Li, X & Lu, W 2006 Binding characteristics of the Lactobacillus brevis ATCC 8287 surface layer to extracellular matrix. FEMS Microbiology Letters 260 210–215 Google ScholarPubMed
Farnworth, E 2005 Kefir – a complex probiotic. Food Science and Technology Bulletin 2 1–17 Google Scholar
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. Journal of Applied Microbiology 98 285–292 CrossRefGoogle ScholarPubMed
Garrote, GL, Abraham, AG & De Antoni, GL 2001 Chemical and microbiological characterisation of kefir grains. Journal of Dairy Research 68 639–652 CrossRefGoogle ScholarPubMed
Garrote, GL, Delfederico, L, Bibiloni, R, Abraham, AG, Pérez, PF, Semorile, L & De Antoni, GL 2004 Lactobacillus isolated from kefir grains: evidence of the presence of S-layer proteins. Journal of Dairy Research 71 222–230 CrossRefGoogle ScholarPubMed
Garrote, GL, Serradell, MA, Abraham, AG, Añon, MC, Fossati, A & De Antoni, GL 2005 Development of an immunochemical method to detect Lactobacillus kefir . Food and Agricultural Immunology 16 221–233 CrossRefGoogle Scholar
Golowczyc, M, Mobili, P, Garrote, GL, Abraham, AG & De Antoni, GL 2007 Protective action of Lactobacillus kefir carrying S-layer protein against Salmonella enterica serovar enteritidis. International Journal of Food Microbiology 118 264–273 CrossRefGoogle ScholarPubMed
Golowczyc, M, Mobili, P, Garrote, GL, Serradell, MA, Abraham, AG & De Antoni, GL 2009 Interaction between Lactobacillus kefir and Saccharomyces lipolytica isolated from kefir grains: evidence for lectin-like activity of bacterial surface proteins. Journal of Dairy Research 76 111–116 CrossRefGoogle ScholarPubMed
Granato, D, Bergonzelli, GE, Pridmore, RD, Marvin, L, Rouvet, M & Corthesy-Theulaz, IE 2004 Cell surface-associated elongation factor Tu mediates the attachment of Lactobacillus johnsonii NCC533 (La1) to human intestinal cells and mucins. Infection and Immunity 72 2160–2169 CrossRefGoogle ScholarPubMed
Henriksson, A & Conway, PL 1996 Adhesion of Lactobacillus fermentum 104-S to porcine stomach mucus. Current Microbiology 33 31–34 CrossRefGoogle ScholarPubMed
Hynönen, U, Westerlund-Wikström, B, Palva, A & Korhonen, TK 2002 Identification by flagellum display of an epithelial cell- and fibronectin-binding function in the SlpA surface protein of Lactobacillus brevis . Journal of Bacteriology 184 3360–3367 CrossRefGoogle ScholarPubMed
Jakava-Viljanen, M & Palva, A 2007 Isolation of surface (S) layer protein carrying Lactobacillus species from porcine intestine and faeces and characterization of their adhesion properties to different host tissues. Veterinary Microbiology 124 264–273 CrossRefGoogle Scholar
Kleerebezem, M, Hols, P, Bernard, E, Rolain, T, Zhou, M, Siezen, RJ & Bron, PA 2010 The extracellular biology of lactobacilli. FEMS Microbiology Reviews 34 199–230 CrossRefGoogle ScholarPubMed
Laemmli, UK 1970 Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 680–685 CrossRefGoogle ScholarPubMed
Lebeer, S, Vanderleyden, J & De Keersmaecker, SCJ 2008 Genes and molecules of lactobacilli supporting probiotic action. Microbiology and Molecular Biology Reviews 72 728–764 CrossRefGoogle ScholarPubMed
Londero, A, Abraham, AG, Gomez Zavaglia, A, Illanes Frontaura, A, León Pelaez, A, Serna Cataño, CA, Quintero Yepes, E, Kakisu, EJ, Tymczyszyn, EE, De Antoni, GL, Garrote, GL, Serradell, M, Golowczyc, M, Gerbino, E, Mobili, P, Perez, PF & Carasi, P 2009 Aprovechamiento integral de efluentes de quesería para la elaboración y preservación de probióticos. In Agroindústria para o MERCOSUL, pp. 91–115 Ed. CNPq/IBIC/UNESCO. Brasília Google Scholar
MacKenzie, DA, Jeffers, F, Parker, ML, Vibert-Vallet, A, Bongaerts, RJ, Roos, S, Walter, J & Juge, N 2010 Strain-specific diversity of mucus-binding proteins in the adhesion and aggregation properties of Lactobacillus reuteri . Microbiology 156 3368–3378 CrossRefGoogle ScholarPubMed
Mastromarino, P, Cacciotti, F, Masci, A & Mosca, L 2011 Antiviral activity of Lactobacillus brevis towards herpes simplex virus type 2: role of cell wall associated components. Anaerobe 17 334–336 CrossRefGoogle ScholarPubMed
McGuckin, M, Lindén, SK, Sutton, P& Florin, TH 2011 Mucin dynamics and enteric pathogens. Nature Reviews Microbiology 9 265–278 CrossRefGoogle ScholarPubMed
Miyoshi, Y, Okada, S, Uchimura, T & Satoh, E 2006 A mucus adhesion promoting protein, MapA, mediates the adhesion of Lactobacillus reuteri to Caco-2 human intestinal epithelial cells. Bioscience Biotechnology and Biochemistry 70 1622–1628 CrossRefGoogle ScholarPubMed
Mobili, P, Serradell, MA, Trejo, S, Avilés-Puigvert, X, 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 CrossRefGoogle ScholarPubMed
Muñoz-Provencio, D, Llopis, M, Antolín, M, de Torres, I, Guarner, F, Pérez-Martínez, G & Monedero, V 2009 Adhesion properties of Lactobacillus casei strains to resected intestinal fragments and components of extracelular matrix. Archives of Microbiology 191 153–161 CrossRefGoogle Scholar
Ouwehand, AC, Kirjavainen, PV, Grönlund, MM, Isolauri, E & Salminen, SJ 1999 Adhesion of probiotic micro-organisms to intestinal mucus. International Dairy Journal 9 623–630 CrossRefGoogle Scholar
Ouwehand, AC, Tölkko, S, Kulmala, J, Salminen, S & Salminen, E 2000 Adhesion of inactivated probiotic strains to intestinal mucus. Letters in Applied Microbiology 31 82–86 CrossRefGoogle ScholarPubMed
Pretzer, G, Snel, J, Molenaar, D, Wiersma, A, Bron, PA, Lambert, J, de Vos, WM, van der Meer, R, Smits, MA & Kleerebezem, M 2005 Biodiversity-based identification and functional characterization of mannose-specific adhesin of Lactobacillus plantarum . Journal of Bacteriology 187 6128–6136 CrossRefGoogle ScholarPubMed
Rojas, M, Ascencio, F & Conway, PL 2002 Purification and characterization of a surface protein from Lactobacillus fermentum 104R that binds to porcine small intestinal mucus and gastric mucin. Applied and Environmental Microbiology 68 2330–2336 CrossRefGoogle ScholarPubMed
Roos, S & Jonsson, H 2002 A high-molecular-mass cell-surface protein from Lactobacillus reuteri 1063 adheres to mucus components. Microbiology 148 433–442 CrossRefGoogle ScholarPubMed
Sánchez, B, Arias, S, Chaignepain, S, Denayrolles, M, Schmitter, JM, Bressollier, P & Urdaci, MC 2009 Identification of surface proteins involved in the adhesion of a probiotic Bacillus cereus strain to mucin and fibronectin. Microbiology 155 1708–1716 CrossRefGoogle ScholarPubMed
Sára, M & Sleytr, UB 2000 S-layer proteins. Journal of Bacteriology 182 859–868 CrossRefGoogle ScholarPubMed
Schneitz, C, Nuotio, L & Lounatma, K 1993 Adhesion of Lactobacillus acidophilus to avian intestinal epithelial cells mediated by the crystalline bacterial cell surface layer (S-layer). Journal of Applied Bacteriology 74 290–294 CrossRefGoogle ScholarPubMed
Schuster, B & Sleytr, UB 2009 Composite S-layer lipid structures. Journal of Structural Biology 168 207e16 CrossRefGoogle ScholarPubMed
Tallon, R, Arias, S, Bressollier, P & Urdaci, MC 2007 Strain- and matrix-dependent adhesion of Lactobacillus plantarum is mediated by proteinaceous bacterial compounds. Journal of Applied Microbiology 102 442–451 CrossRefGoogle ScholarPubMed
Tuomola, EM, Ouwehand, AC & Salminen, S 2000 Chemical, physical and enzymatic pre-treatments of probiotic lactobacilli alter their adhesion to human intestinal mucus glycoproteins. International Journal of Food Microbiology 60 75–81 CrossRefGoogle ScholarPubMed
Van Tassell, ML & Miller, MJ 2011 Lactobacillus adhesion to mucus. Nutrients 3 613–636 CrossRefGoogle ScholarPubMed
Wang, B, Wei, H, Yuan, J, Li, Q, Li, Y, Li, N & Li, J 2008 Identification of surface protein from Lactobacillus reuteri JCM1081 that adheres to porcin gastric mucin and human enterocyte-like HT-29 cells. Current Microbiology 57 33–38 CrossRefGoogle Scholar
Weisburg, WG, Barns, SM, Pelletier, D & Lane, DJ 1991 16S ribosomal DNA amplification for phylogenetic study. Journal of Bacteriology 173 697–703 CrossRefGoogle ScholarPubMed