Skip to main content
Log in

Fructooligosaccharides decreased the ability of probiotic Escherichia coli Nissle 1917 to adhere to co-cultures of human intestinal cell lines

  • Article
  • Published:
Journal of the Korean Society for Applied Biological Chemistry Submit manuscript

Abstract

In the present study, we investigated effects of prebiotic fructooligosaccharides (FOS) on the ability of Escherichia coli Nissle 1917 (EcN), a probiotic bacterial strain, to adhere to co-cultures of human intestinal cells (Caco-2 and HT29-MTX). For the bacterial adhesion assay, the co-cultures were seeded together at a ratio of 3:1 and then incubated EcN in the presence of various prebiotics including FOS. To eliminate possible bias, both manual and automated cell counting methods were utilized. In results, FOS significantly suppressed the adhesion abilities of probiotic EcN to the co-cultures. Taken altogether, we carefully suggest that an unbalanced supplementation of prebiotics may adversely impact on gut microflora; hence, further investigations are warranted in regards to such unexpected adverse effects and responsible mechanisms on colonization of probiotics in the gastrointestinal tract utilizing in vivo models.

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

Access this article

Subscribe and save

Springer+
from $39.99 /Month
  • Starting from 10 chapters or articles per month
  • Access and download chapters and articles from more than 300k books and 2,500 journals
  • Cancel anytime
View plans

Buy Now

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

Abbreviations

ATCC:

American Type Culture Collection

ANOVA:

Analysis of variance

DMSO:

Dimethyl sulfoxide

DMEM:

Dulbecco’s Modified Eagle Media

EcN:

Escherichia coli Nissle 1917

FOS:

Fructooligosaccharide

FRU:

Fructose

GI:

Gastrointestinal

GFP:

Green fluorescent protein

INU:

Inulin

LB:

Luria–Bertani

MTT:

3-(4,5-Dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide

PBS:

Phosphate-buffered saline

SUC:

Sucrose

pGFPuv:

UV-variant green fluorescent protein

References

  • Aronson M, Medalia O, Schori L, Mirelman D, Sharon N, Ofek I (1979) Prevention of colonization of the urinary tract of mice with Escherichia coli by blocking of bacterial adherence with methyl alpha-d-mannopyranoside. J Infect Dis 139:329–332

    Article  CAS  Google Scholar 

  • Beachey EH, Giampapa CS, Abraham SN (1988) Bacterial adherence. Adhesin receptor-mediated attachment of pathogenic bacteria to mucosal surfaces. Am Rev Respir Dis 138:S45–S48

    Article  CAS  Google Scholar 

  • Bickert T, Trujillo-Vargas CM, Duechs M, Wohlleben G, Polte T, Hansen G et al (2009) Probiotic Escherichia coli Nissle 1917 suppresses allergen-induced Th2 responses in the airways. Int Arch Allergy Immunol 149:219–230

    Article  CAS  Google Scholar 

  • Buddington KK, Donahoo JB, Buddington RK (2002) Dietary oligofructose and inulin protect mice from enteric and systemic pathogens and tumor inducers. J Nutr 132:472–477

    CAS  Google Scholar 

  • Coudray C, Tressol JC, Gueux E, Rayssiguier Y (2003) Effects of inulin-type fructans of different chain length and type of branching on intestinal absorption and balance of calcium and magnesium in rats. Eur J Nutr 42:91–98

    Article  CAS  Google Scholar 

  • Dunne C, O’Mahony L, Murphy L, Thornton G, Morrissey D, O’Halloran S et al (2001) In vitro selection criteria for probiotic bacteria of human origin: correlation with in vivo findings. Am J Clin Nutr 73:386S–392S

    CAS  Google Scholar 

  • Firon N, Ashkenazi S, Mirelman D, Ofek I, Sharon N (1987) Aromatic alpha-glycosides of mannose are powerful inhibitors of the adherence of type 1 fimbriated Escherichia coli to yeast and intestinal epithelial cells. Infect Immun 55:472–476

    CAS  Google Scholar 

  • Flock JI (1999) Extracellular-matrix-binding proteins as targets for the prevention of Staphylococcus aureus infections. Mol Med Today 5:532–537

    Article  CAS  Google Scholar 

  • Forstner JF, Forstner GG (1994) Gastrointestinal mucus. In: Johnson LR (ed) Physiology of the gastrointestinal tract, 3rd edn. Raven Press, New York, pp 1255–1283

  • Gibson GR (1999) Dietary modulation of the human gut microflora using the prebiotics oligofructose and inulin. J Nutr 129:1438S–1441S

    CAS  Google Scholar 

  • Gibson GR, Roberfroid MB (1995) Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J Nutr 125:1401–1412

    CAS  Google Scholar 

  • Gibson GR, Wang X (1994) Enrichment of bifidobacteria from human gut contents by oligofructose using continuous culture. FEMS Microbiol Lett 118:121–127

    Article  CAS  Google Scholar 

  • Kamada N, Maeda K, Inoue N, Hisamatsu T, Okamoto S, Hong KS et al (2008) Nonpathogenic Escherichia coli strain Nissle 1917 inhibits signal transduction in intestinal epithelial cells. Infect Immun 76:214–220

    Article  CAS  Google Scholar 

  • Kim JK, Choi SJ, Cho HY, Kim YJ, Lim ST, Kim CJ et al (2010) Ipomoea batatas attenuates amyloid beta peptide-induced neurotoxicity in ICR mice. J Med Food 14:304–309

    Article  Google Scholar 

  • Kruis W, Fric P, Pokrotnieks J, Lukas M, Fixa B, Kascak M et al (2004) Maintaining remission of ulcerative colitis with the probiotic Escherichia coli Nissle 1917 is as effective as with standard mesalazine. Gut 53:1617–1623

    Article  CAS  Google Scholar 

  • Laparra JM, Sanz Y (2009) Comparison of in vitro models to study bacterial adhesion to the intestinal epithelium. Lett Appl Microbiol 49:695–701

    Article  CAS  Google Scholar 

  • Lodinova-Zadnikova R, Sonnenborn U (1997) Effect of preventive administration of a nonpathogenic Escherichia coli strain on the colonization of the intestine with microbial pathogens in newborn infants. Biol Neonate 71:224–232

    Article  CAS  Google Scholar 

  • Mahler GJ, Shuler ML, Glahn RP (2009) Characterization of Caco-2 and HT29-MTX cocultures in an in vitro digestion/cell culture model used to predict iron bioavailability. J Nutr Biochem 20:494–502

    Article  CAS  Google Scholar 

  • McBain AJ, Macfarlane GT (1997) Investigations of bifidobacterial ecology and oligosaccharide metabolism in a three-stage compound continuous culture system. Scand J Gastroenterol Suppl 222:32–40

    CAS  Google Scholar 

  • Michel C, Kravtchenko TP, David A, Gueneau S, Kozlowski F, Cherbut C (1998) In vitro prebiotic effects of Acacia gums onto the human intestinal microbiota depends on both botanical origin and environmental pH. Anaerobe 4:257–266

    Article  CAS  Google Scholar 

  • Mugambi MN, Musekiwa A, Lombard M, Young T, Blaauw R (2012) Synbiotics, probiotics or prebiotics in infant formula for full term infants: a systematic review. Nutr J 11:81

    Article  Google Scholar 

  • Navarro G, Cheng AT, Peach KC, Bray WM, Bernan VS, Yildiz FH et al (2013) Image-based 384-well high-throughput screening method for the discovery of skyllamycins A to C as biofilm inhibitors and inducers of biofilm detachment in Pseudomonas aeruginosa. Antimicrob Agents Chemother 58:1092–1099

    Article  Google Scholar 

  • Oelschlaeger TA (2010) Mechanisms of probiotic actions—a review. Int J Med Microbiol 300:57–62

    Article  CAS  Google Scholar 

  • Oku T (1996) Oligosaccharides with beneficial health effects: a Japanese perspective. Nutr Rev 54:S59–S66

    Article  CAS  Google Scholar 

  • Reissbrodt R, Hammes WP, dal Bello F, Prager R, Fruth A, Hantke K et al (2009) Inhibition of growth of Shiga toxin-producing Escherichia coli by nonpathogenic Escherichia coli. FEMS Microbiol Lett 290:62–69

    Article  CAS  Google Scholar 

  • Roberfroid MB, Delzenne NM (1998) Dietary fructans. Annu Rev Nutr 18:117–143

    Article  CAS  Google Scholar 

  • Roberfroid MB, Van Loo JA, Gibson GR (1998) The bifidogenic nature of chicory inulin and its hydrolysis products. J Nutr 128:11–19

    CAS  Google Scholar 

  • Rumessen JJ, Gudmand-Hoyer E (1998) Fructans of chicory: intestinal transport and fermentation of different chain lengths and relation to fructose and sorbitol malabsorption. Am J Clin Nutr 68:357–364

    CAS  Google Scholar 

  • Sanchez B, Bressollier P, Urdaci MC (2008) Exported proteins in probiotic bacteria: adhesion to intestinal surfaces, host immunomodulation and molecular cross-talking with the host. FEMS Immunol Med Microbiol 54:1–17

    Article  CAS  Google Scholar 

  • Saulnier DM, Spinler JK, Gibson GR, Versalovic J (2009) Mechanisms of probiosis and prebiosis: considerations for enhanced functional foods. Curr Opin Biotechnol 20:135–141

    Article  CAS  Google Scholar 

  • Schroeder B, Duncker S, Barth S, Bauerfeind R, Gruber AD, Deppenmeier S et al (2006) Preventive effects of the probiotic Escherichia coli strain Nissle 1917 on acute secretory diarrhea in a pig model of intestinal infection. Dig Dis Sci 51:724–731

    Article  CAS  Google Scholar 

  • Schultz M, Strauch UG, Linde HJ, Watzl S, Obermeier F, Gottl C et al (2004) Preventive effects of Escherichia coli strain Nissle 1917 on acute and chronic intestinal inflammation in two different murine models of colitis. Clin Diagn Lab Immunol 11:372–378

    Google Scholar 

  • Simons K, Fuller SD (1985) Cell surface polarity in epithelia. Annu Rev Cell Biol 1:243–288

    Article  CAS  Google Scholar 

  • Tiihonen K, Ouwehand AC, Rautonen N (2010) Human intestinal microbiota and healthy ageing. Ageing Res Rev 9:107–116

    Article  Google Scholar 

  • Tzortzis G, Goulas AK, Gee JM, Gibson GR (2005) A novel galactooligosaccharide mixture increases the bifidobacterial population numbers in a continuous in vitro fermentation system and in the proximal colonic contents of pigs in vivo. J Nutr 135:1726–1731

    CAS  Google Scholar 

  • Van Loo J, Cummings J, Delzenne N, Englyst H, Franck A, Hopkins M et al (1999) Functional food properties of non-digestible oligosaccharides: a consensus report from the ENDO project (DGXII AIRII-CT94-1095). Br J Nutr 81:121–132

    Google Scholar 

  • Wang X, Gibson GR (1993) Effects of the in vitro fermentation of oligofructose and inulin by bacteria growing in the human large intestine. J Appl Bacteriol 75:373–380

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Research Foundation of Korea Grant funded by the Korean Government (Ministry of Education, Science, and Technology (357-2011-1-F00040).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to H. G. Park.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kim, J.K., Shin, E.C. & Park, H.G. Fructooligosaccharides decreased the ability of probiotic Escherichia coli Nissle 1917 to adhere to co-cultures of human intestinal cell lines. J Korean Soc Appl Biol Chem 58, 45–52 (2015). https://doi.org/10.1007/s13765-015-0002-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13765-015-0002-5

Keywords