1887

Abstract

Bacterial aggregation and/or adhesion are key factors for colonization of the digestive ecosystem and the ability of probiotic strains to exclude pathogens. In the present study, two probiotic strains, CNCM-I-3698 and CNCM-I-3699, were evaluated as viable or heat-killed forms and compared with probiotic reference strains ( GG and CIP 103136). The autoaggregation potential of both forms was higher than that of reference strains and twice that of pathogenic strains. The coaggregation potential of these two beneficial micro-organisms was evaluated against several pathogenic agents that threaten the global safety of the feed/food chain: spp spp. and . The strongest coaggregative interactions were demonstrated with spp. by a coaggregation test, confirmed by electron microscopic examination for the two forms. Viable forms were investigated for the nature of the bacterial cell-surface molecules involved, by sugar reversal tests and chemical and enzymic pretreatments. The results suggest that the coaggregation between both probiotic strains and CIP 70.2 is mediated by a carbohydrate–lectin interaction. The autoaggregation potential of the two probiotics decreased upon exposure to proteinase, SDS or LiCl, showing that proteinaceous components on the surface of the two lactobacilli play an important role in this interaction. Adhesion abilities of both strains were also demonstrated at significant levels on Caco-2 cells, mucin and extracellular matrix material. Both viable and heat-killed forms of the two probiotic lactobacilli inhibited the attachment of CIP 70.2 to mucin. In conclusion, assays showed that CNCM-I-3698 and CNCM-I-3699, as viable or heat-killed forms, are adherent to different intestinal matrix models and are highly aggregative with pathogens, especially spp., the most commonly reported zoonotic agent in the European Union. This study supports the need for further investigations to demonstrate the potential food safety benefits of CNCM-I-3698 and CNCM-I-3699, live or heat-killed, in the global feed/food chain.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.049965-0
2013-04-01
2019-10-21
Loading full text...

Full text loading...

/deliver/fulltext/jmm/62/4/637.html?itemId=/content/journal/jmm/10.1099/jmm.0.049965-0&mimeType=html&fmt=ahah

References

  1. Alemka A. , Clyne M. , Shanahan F. , Tompkins T. , Corcionivoschi N. , Bourke B. . ( 2010; ). Probiotic colonization of the adherent mucus layer of HT29MTXE12 cells attenuates Campylobacter jejuni virulence properties. . Infect Immun 78:, 2812–2822. [CrossRef] [PubMed]
    [Google Scholar]
  2. Alfredson D. A. , Korolik V. . ( 2007; ). Antibiotic resistance and resistance mechanisms in Campylobacter jejuni and Campylobacter coli . . FEMS Microbiol Lett 277:, 123–132. [CrossRef] [PubMed]
    [Google Scholar]
  3. Bernardeau M. , Guilmoto H. . ( 2008; ). Diet supplementation with fermentative heat-inactivated lactobacilli based product can help to prevent swine dysentery in pigs. Proceedings of the 20th IPV Congress, Durban, South Africa. P09.012, 517.
  4. Bernardeau M. , Gueguen M. , Smith D. G. E. , Corona-Barrera E. , Vernoux J. P. . ( 2009; ). In vitro antagonistic activities of Lactobacillus spp. against Brachyspira hyodysenteriae and Brachyspira pilosicoli . . Vet Microbiol 138:, 184–190. [CrossRef] [PubMed]
    [Google Scholar]
  5. Boris S. , Suárez J. E. , Vázquez F. , Barbés C. . ( 1998; ). Adherence of human vaginal lactobacilli to vaginal epithelial cells and interaction with uropathogens. . Infect Immun 66:, 1985–1989.[PubMed]
    [Google Scholar]
  6. Bouzaine T. , Dauphin R. D. , Thonart P. , Urdaci M. C. , Hamdi M. . ( 2005; ). Adherence and colonization properties of Lactobacillus rhamnosus TB1, a broiler chicken isolate. . Lett Appl Microbiol 40:, 391–396. [CrossRef] [PubMed]
    [Google Scholar]
  7. Byrd J. A. , Hargis B. M. , Caldwell D. J. , Bailey R. H. , Herron K. L. , McReynolds J. L. , Brewer R. L. , Anderson R. C. , Bischoff K. M. . & other authors ( 2001; ). Effect of lactic acid administration in the drinking water during preslaughter feed withdrawal on Salmonella and Campylobacter contamination of broilers. . Poult Sci 80:, 278–283.[PubMed] [CrossRef]
    [Google Scholar]
  8. Byrne C. M. , Clyne M. , Bourke B. . ( 2007; ). Campylobacter jejuni adhere to and invade chicken intestinal epithelial cells in vitro. . Microbiology 153:, 561–569. [CrossRef] [PubMed]
    [Google Scholar]
  9. Castagliuolo I. , Galeazzi F. , Ferrari S. , Elli M. , Brun P. , Cavaggioni A. , Tormen D. , Sturniolo G. C. , 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. [CrossRef] [PubMed]
    [Google Scholar]
  10. Cesena C. , Morelli L. , Alander M. , Siljander T. , Tuomola E. , Salminen S. , Mattila-Sandholm T. , Vilpponen-Salmela T. , von Wright A. . ( 2001; ). Lactobacillus crispatus and its nonaggregating mutant in human colonization trials. . J Dairy Sci 84:, 1001–1010. [CrossRef] [PubMed]
    [Google Scholar]
  11. Chauvière G. , Coconnier M.-H. , Kernéis S. , Fourniat J. , Servin A. L. . ( 1992; ). Adhesion of human Lactobacillus acidophilus strain LB to human enterocyte-like Caco-2 cells. . J Gen Microbiol 138:, 1689–1696. [CrossRef] [PubMed]
    [Google Scholar]
  12. Collado M. C. , Gueimonde M. , Hernández M. , Sanz Y. , Salminen S. . ( 2005; ). Adhesion of selected Bifidobacterium strains to human intestinal mucus and the role of adhesion in enteropathogen exclusion. . J Food Prot 68:, 2672–2678.[PubMed]
    [Google Scholar]
  13. Collado M. C. , Surono I. , Meriluoto J. , Salminen S. . ( 2007; ). Indigenous dadih lactic acid bacteria: cell-surface properties and interactions with pathogens. . J Food Sci 72:, M89–M93. [CrossRef] [PubMed]
    [Google Scholar]
  14. Collado M. C. , Meriluoto J. , Salminen S. . ( 2008; ). Adhesion and aggregation properties of probiotic and pathogen strains. . Eur Food Res Technol 226:, 1065–1073. [CrossRef]
    [Google Scholar]
  15. Crushell E. , Harty S. , Sharif F. , Bourke B. . ( 2004; ). Enteric Campylobacter: purging its secrets?. Pediatr Res 55:, 3–12. [CrossRef] [PubMed]
    [Google Scholar]
  16. Dibner J. J. , Buttin P. . ( 2002; ). Use of organic acids as a model to study the impact of gut microflora on nutrition and metabolism. . J Appl Poult Res 11:, 453–463.[CrossRef]
    [Google Scholar]
  17. EFSA ( 2012; ). The European Union Summary Report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2010. . EFSA J 10:, 2598. [CrossRef]
    [Google Scholar]
  18. Fosse J. , Seegers H. , Magras C. . ( 2009; ). Prevalence and risk factors for bacterial food-borne zoonotic hazards in slaughter pigs: a review. . Zoonoses Public Health 56:, 429–454. [CrossRef] [PubMed]
    [Google Scholar]
  19. Goh Y. J. , Klaenhammer T. R. . ( 2010; ). Functional roles of aggregation-promoting-like factor in stress tolerance and adherence of Lactobacillus acidophilus NCFM. . Appl Environ Microbiol 76:, 5005–5012. [CrossRef] [PubMed]
    [Google Scholar]
  20. Golowczyc M. A. , Mobili P. , Garrote G. L. , Abraham A. G. , De Antoni G. L. . ( 2007; ). Protective action of Lactobacillus kefir carrying S-layer protein against Salmonella enterica serovar Enteritidis. . Int J Food Microbiol 118:, 264–273. [CrossRef] [PubMed]
    [Google Scholar]
  21. Golowczyc M. A. , Mobili P. , Garrote G. L. , de Los Angeles Serradell M. , Abraham A. G. , De Antoni G. L. . ( 2009; ). Interaction between Lactobacillus kefir and Saccharomyces lipolytica isolated from kefir grains: evidence for lectin-like activity of bacterial surface proteins. . J Dairy Res 76:, 111–116. [CrossRef] [PubMed]
    [Google Scholar]
  22. Hudault S. , Liévin V. , Bernet-Camard M. F. , Servin A. L. . ( 1997; ). Antagonistic activity exerted in vitro and in vivo by Lactobacillus casei (strain GG) against Salmonella typhimurium C5 infection. . Appl Environ Microbiol 63:, 513–518.[PubMed]
    [Google Scholar]
  23. Hugas M. , Tsigarida E. , Robinson T. , Calistri P. . ( 2009; ). The EFSA Scientific Panel on Biological Hazards first mandate: May 2003–May 2006. Insight into foodborne zoonoses. . Trends Food Sci Technol 20:, 188–193. [CrossRef]
    [Google Scholar]
  24. Ishikawa H. , Kutsukake E. , Fukui T. , Sato I. , Shirai T. , Kurihara T. , Okada N. , Danbara H. , Toba M. . & other authors ( 2010; ). Oral administration of heat-killed Lactobacillus plantarum strain b240 protected mice against Salmonella enterica serovar Typhimurium. . Biosci Biotechnol Biochem 74:, 1338–1342. [CrossRef] [PubMed]
    [Google Scholar]
  25. Jankovic I. , Ventura M. , Meylan V. , Rouvet M. , Elli M. , Zink R. . ( 2003; ). Contribution of aggregation-promoting factor to maintenance of cell shape in Lactobacillus gasseri 4B2. . J Bacteriol 185:, 3288–3296. [CrossRef] [PubMed]
    [Google Scholar]
  26. Kirjavainen P. V. , Ouwehand A. C. , Isolauri E. , Salminen S. J. . ( 1998; ). The ability of probiotic bacteria to bind to human intestinal mucus. . FEMS Microbiol Lett 167:, 185–189. [CrossRef] [PubMed]
    [Google Scholar]
  27. Kleinman H. K. , McGarvey M. L. , Hassell J. R. , Star V. L. , Cannon F. B. , Laurie G. W. , Martin G. R. . ( 1986; ). Basement membrane complexes with biological activity. . Biochemistry 25:, 312–318. [CrossRef] [PubMed]
    [Google Scholar]
  28. Kolenbrander P. E. . ( 2000; ). Oral microbial communities: biofilms, interactions, and genetic systems. . Annu Rev Microbiol 54:, 413–437. [CrossRef] [PubMed]
    [Google Scholar]
  29. Lebeer S. , Vanderleyden J. , De Keersmaecker S. C. J. . ( 2008; ). Genes and molecules of lactobacilli supporting probiotic action. . Microbiol Mol Biol Rev 72:, 728–764. [CrossRef] [PubMed]
    [Google Scholar]
  30. Ledder R. G. , Timperley A. S. , Friswell M. K. , Macfarlane S. , McBain A. J. . ( 2008; ). Coaggregation between and among human intestinal and oral bacteria. . FEMS Microbiol Ecol 66:, 630–636. [CrossRef] [PubMed]
    [Google Scholar]
  31. Mackenzie D. A. , Jeffers F. , Parker M. L. , Vibert-Vallet A. , Bongaerts R. J. , 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. [CrossRef] [PubMed]
    [Google Scholar]
  32. Marcotte H. , Ferrari S. , Cesena C. , Hammarström L. , Morelli L. , Pozzi G. , Oggioni M. R. . ( 2004; ). The aggregation-promoting factor of Lactobacillus crispatus M247 and its genetic locus. . J Appl Microbiol 97:, 749–756. [CrossRef] [PubMed]
    [Google Scholar]
  33. Mercier-Bonin M. , Da Silva S. , Ferrari L. , Mercade M. , Cratier C. , Ait Belgnaoui A. , Ferries L. , Loubière P. , Theodorou V. . ( 2011; ). Muco-adhesive proprieties of the probiotic Lactobacillus farciminis: coupling in vitro and in vivo approaches. Tenth Symposium on Lactic Acid Bacteria, LAB10, Egmond aan Zee, The Netherlands. Poster C040. Section C: Host–Microbe Interactions, Nutrition and Health.
  34. Modesto M. , D’Aimmo M. R. , Stefanini I. , Trevisi P. , De Filippi S. , Casini L. , Mazzoni M. , Bosi P. , Biavati B. . ( 2009; ). A novel strategy to select Bifidobacterium strains and prebiotics as natural growth promoters in newly weaned pigs. . Livest Sci 122:, 248–258. [CrossRef]
    [Google Scholar]
  35. Ng S. C. , Hart A. L. , Kamm M. A. , Stagg A. J. , Knight S. C. . ( 2009; ). Mechanisms of action of probiotics: recent advances. . Inflamm Bowel Dis 15:, 300–310. [CrossRef] [PubMed]
    [Google Scholar]
  36. O’ Brien S. J. , de Valk H. . ( 2003; ). Salmonella – ‘old’ organism, continued challenges!. Euro Surveill 8:, 29–31.[PubMed]
    [Google Scholar]
  37. O’Hara A. M. , Shanahan F. . ( 2007; ). Mechanisms of action of probiotics in intestinal diseases. . ScientificWorldJournal 7:, 31–46. [CrossRef] [PubMed]
    [Google Scholar]
  38. Ocaña V. S. , Nader-Macías M. E. . ( 2002; ). Vaginal lactobacilli: self- and co-aggregating ability. . Br J Biomed Sci 59:, 183–190.[PubMed]
    [Google Scholar]
  39. Ostad S. N. , Salarian A. A. , Ghahramani M. H. , Fazeli M. R. , Samadi N. , Jamalifar H. . ( 2009; ). Live and heat-inactivated lactobacilli from feces inhibit Salmonella typhi and Escherichia coli adherence to Caco-2 cells. . Folia Microbiol (Praha) 54:, 157–160. [CrossRef] [PubMed]
    [Google Scholar]
  40. Ou C. C. , Lin S. L. , Tsai J. J. , Lin M. Y. , Ou C. , Lin S. , Tsai J. , Lin M. . ( 2011; ). Heat-killed lactic acid bacteria enhance immunomodulatory potential by skewing the immune response toward Th1 polarization. . J Food Sci 76:, M260–M267. [CrossRef] [PubMed]
    [Google Scholar]
  41. Ouwehand A. C. , Tölkkö S. , Kulmala J. , Salminen S. , Salminen E. . ( 2000; ). Adhesion of inactivated probiotic strains to intestinal mucus. . Lett Appl Microbiol 31:, 82–86. [CrossRef] [PubMed]
    [Google Scholar]
  42. Patterson J. A. , Burkholder K. M. . ( 2003; ). Application of prebiotics and probiotics in poultry production. . Poult Sci 82:, 627–631.[PubMed] [CrossRef]
    [Google Scholar]
  43. Rickard A. H. , Leach S. A. , Buswell C. M. , High N. J. , Handley P. S. . ( 2000; ). Coaggregation between aquatic bacteria is mediated by specific-growth-phase-dependent lectin–saccharide interactions. . Appl Environ Microbiol 66:, 431–434. [CrossRef] [PubMed]
    [Google Scholar]
  44. Rickard A. H. , Gilbert P. , High N. J. , Kolenbrander P. E. , Handley P. S. . ( 2003; ). Bacterial coaggregation: an integral process in the development of multi-species biofilms. . Trends Microbiol 11:, 94–100. [CrossRef] [PubMed]
    [Google Scholar]
  45. Rickard A. H. , Gilbert P. , Handley P. S. . ( 2004; ). Influence of growth environment on coaggregation between freshwater biofilm bacteria. . J Appl Microbiol 96:, 1367–1373. [CrossRef] [PubMed]
    [Google Scholar]
  46. Servin A. L. , Coconnier M.-H. . ( 2003; ). Adhesion of probiotic strains to the intestinal mucosa and interaction with pathogens. . Best Pract Res Clin Gastroenterol 17:, 741–754. [CrossRef] [PubMed]
    [Google Scholar]
  47. Sherman P. M. , Ossa J. C. , Johnson-Henry K. . ( 2009; ). Unraveling mechanisms of action of probiotics. . Nutr Clin Pract 24:, 10–14. [CrossRef] [PubMed]
    [Google Scholar]
  48. Smulders F. J. M. , Vågsholm I. , Korkeala H. . ( 2008; ). Food-borne zoonoses, the EU zoonosis legislation and the prospects for food safety and consumer protection during primary animal production. . Wien Klin Wochenschr 120:, 587–598. [CrossRef] [PubMed]
    [Google Scholar]
  49. Tallon R. , Arias S. , Bressollier P. , Urdaci M. C. . ( 2007; ). Strain- and matrix-dependent adhesion of Lactobacillus plantarum is mediated by proteinaceous bacterial compounds. . J Appl Microbiol 102:, 442–451. [CrossRef] [PubMed]
    [Google Scholar]
  50. Tu Q. V. , McGuckin M. A. , Mendz G. L. . ( 2008; ). Campylobacter jejuni response to human mucin MUC2: modulation of colonization and pathogenicity determinants. . J Med Microbiol 57:, 795–802. [CrossRef] [PubMed]
    [Google Scholar]
  51. Tuomola E. M. , Ouwehand A. C. , Salminen S. J. . ( 1999; ). The effect of probiotic bacteria on the adhesion of pathogens to human intestinal mucus. . FEMS Immunol Med Microbiol 26:, 137–142. [CrossRef] [PubMed]
    [Google Scholar]
  52. Turpin W. , Humblot C. , Thomas M. , Guyot J. P. . ( 2010; ). Lactobacilli as multifaceted probiotics with poorly disclosed molecular mechanisms. . Int J Food Microbiol 143:, 87–102. [CrossRef] [PubMed]
    [Google Scholar]
  53. Van den Abbeele P. , Roos S. , Eeckhaut V. , MacKenzie D. A. , Derde M. , Verstraete W. , Marzorati M. , Possemiers S. , Vanhoecke B. . & other authors ( 2012; ). Incorporating a mucosal environment in a dynamic gut model results in a more representative colonization by lactobacilli. . Microb Biotechnol 5:, 106–115. [CrossRef] [PubMed]
    [Google Scholar]
  54. van Netten P. , Mossel D. A. , Huis In ’t Veld J. . ( 1995; ). Lactic acid decontamination of fresh pork carcasses: a pilot plant study. . Int J Food Microbiol 25:, 1–9. [CrossRef] [PubMed]
    [Google Scholar]
  55. Voltan S. , Castagliuolo I. , Elli M. , Longo S. , Brun P. , D’Incà R. , Porzionato A. , Macchi V. , Palù G. . & other authors ( 2007; ). Aggregating phenotype in Lactobacillus crispatus determines intestinal colonization and TLR2 and TLR4 modulation in murine colonic mucosa. . Clin Vaccine Immunol 14:, 1138–1148. [CrossRef] [PubMed]
    [Google Scholar]
  56. von Ossowski I. , Reunanen J. , Satokari R. , Vesterlund S. , Kankainen M. , Huhtinen H. , Tynkkynen S. , Salminen S. , de Vos W. M. , Palva A. . ( 2010; ). Mucosal adhesion properties of the probiotic Lactobacillus rhamnosus GG SpaCBA and SpaFED pilin subunits. . Appl Environ Microbiol 76:, 2049–2057. [CrossRef] [PubMed]
    [Google Scholar]
  57. von Ossowski I. , Satokari R. , Reunanen J. , Lebeer S. , De Keersmaecker S. C. J. , Vanderleyden J. , de Vos W. M. , Palva A. . ( 2011; ). Functional characterization of a mucus-specific LPXTG surface adhesin from probiotic Lactobacillus rhamnosus GG. . Appl Environ Microbiol 77:, 4465–4472. [CrossRef] [PubMed]
    [Google Scholar]
  58. Vu B. , Chen M. , Crawford R. J. , Ivanova E. P. . ( 2009; ). Bacterial extracellular polysaccharides involved in biofilm formation. . Molecules 14:, 2535–2554. [CrossRef] [PubMed]
    [Google Scholar]
  59. Walter J. , Schwab C. , Loach D. M. , Gänzle M. G. , Tannock G. W. . ( 2008; ). Glucosyltransferase A (GtfA) and inulosucrase (Inu) of Lactobacillus reuteri TMW1.106 contribute to cell aggregation, in vitro biofilm formation, and colonization of the mouse gastrointestinal tract. . Microbiology 154:, 72–80. [CrossRef] [PubMed]
    [Google Scholar]
  60. Wine E. , Gareau M. G. , Johnson-Henry K. , Sherman P. M. . ( 2009; ). Strain-specific probiotic (Lactobacillus helveticus) inhibition of Campylobacter jejuni invasion of human intestinal epithelial cells. . FEMS Microbiol Lett 300:, 146–152. [CrossRef] [PubMed]
    [Google Scholar]
  61. Witters N. A. , Duhamel G. E. . ( 1999; ). Motility-regulated mucin association of Serpulina pilosicoli, the agent of colonic spirochetosis of humans and animals. . Adv Exp Med Biol 473:, 199–205. [CrossRef] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.049965-0
Loading
/content/journal/jmm/10.1099/jmm.0.049965-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error