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Effect of Lactobacillus rhamnosus NCDC 298 with FOS in Combination on Viability and Toxin Production of Enterotoxigenic Escherichia coli

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Abstract

The present study was to investigate the utilization of prebiotics by Lactobacillus rhamnosus NCDC 298 and its synergistic adversary effect on both population and production of heat-labile (LT) toxin in enterotoxigenic Escherichia coli (ETEC). To select suitable prebiotic in order to enhance functionality, its utilization and the prebiotic activity score was examined. Antivirulence effect on ETEC was inspected by its inactivation rate and heat-labile toxin production in presence of different synbiotic combination. L. rhamnosus NCDC 298 strain grown well on media supplemented with fructooligosaccharides (FOS) and galactooligosaccharides (GOS), whereas significant inactivation of ETEC was observed when FOS was added to the co-culture medium. Significant decrease in LT enterotoxin was seen through GM1 ganglioside enzyme linked immunoassay (GM1 ELISA), when ETEC has grown with L. rhamnosus NCDC 298 and FOS. Short-chain FOS proved to be the most effective substrate, improving antagonistic activity for L. rhamnosus NCDC 298. Both L. rhamnosus NCDC 298 with FOS can be used as an effective synbiotic combination for secretory antidiarrheal fermented dairy formulations.

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References

  1. Casburn-Jones AC, Farthing M (2004) Management of infectious diarrhoea. Gut 53:296–305

    Article  CAS  Google Scholar 

  2. Dubreuil JD (2008) Escherichia coli STb toxin and colibacillosis: knowing is half the battle. FEMS Microbiol Lett 278:137–145

    Article  CAS  Google Scholar 

  3. FAO/WHO Working Group Report on Drafting Guidelines for the Evaluation of Probiotics in Food. London, Ontario, Canada, April 30 and May 1, 2002. http://www.who.int/foodsafety/fs_management/en/probiotic_guidelines.pdf

  4. Anand S, Mandal S, Patil P, Tomar SK (2016) Pathogen-induced secretory diarrhea and its prevention. Eur J Clin Microbiol Infect Dis 35(11):1721–1739

    Article  CAS  Google Scholar 

  5. Lebeer S, Vanderleyden J, De Keersmaecker SC (2008) Genes and molecules of lactobacilli supporting probiotic action. Microbiol Mol Bio Rev 72(4):728–764

    Article  CAS  Google Scholar 

  6. Sudhakaran VA, Panwar H, Chauhan R, Duary RK, Rathore RK, Batish VK, Grover S (2013) Modulation of anti-inflammatory response in lipopolysaccharide stimulated human THP-1 cell line and mouse model at gene expression level with indigenous putative probiotic lactobacilli. Genes Nutr 8(6):637–648

    Article  Google Scholar 

  7. Buddington KK, Donahoo JB, Buddington RK (2002) Dietary oligofructose and inulin protect mice from enteric and systemic pathogens and tumor inducers. J Nutr 132(3):472–477

    Article  CAS  Google Scholar 

  8. Quintero M, Maldonado M, Perez-Munoz M, Jimenez R, Fangman T, Rupnow J, Wittke A, Russell M, Hutkins R (2011) Adherence inhibition of Cronobacter sakazakii to intestinal epithelial cells by prebiotic oligosaccharides. Curr Microbiol 62(5):1448–1454

    Article  CAS  Google Scholar 

  9. Sangwan V, Tomar SK, Ali B, Singh RR, Singh AK (2015) Galactooligosaccharides reduce infection caused by Listeria monocytogenes and modulate IgG and IgA levels in mice. Int Dairy J 28(41):58–63

    Article  Google Scholar 

  10. Servin AL, Coconnier MH (2004) Adhesion of probiotic strains to the intestinal mucosa and interaction with pathogens. Best Pract Res Clin Gastroenterol 17:741–754

    Article  Google Scholar 

  11. Araya-Kojima T, Yaeshima T, Ishibashi N, Shimamura S, Hayasawa H (1995) Inhibitory effects of Bifidobacterium longum BB536 on harmful intestinal bacteria. Bifidobacteria and Microflora 14(2):59–66

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  13. Preidis GA, Versalovic J (2009) Targeting the human microbiome with antibiotics, probiotics, and prebiotics: gastroenterology enters the metagenomics era. Gastroenterology 136:2015–2031

    Article  CAS  Google Scholar 

  14. Asahara T, Nomoto K, Shimizu K, Watanuki M, Tanaka R (2001) Increased resistance of mice to Salmonella enterica serovar Typhimurium infection by synbiotic administration of Bifidobacteria and transgalactosylated oligosaccharides. J Appl Microbiol 91(6):985–996

    Article  CAS  Google Scholar 

  15. Fooks LJ, Fuller R, Gibson GR (1999) Prebiotics, probiotics and human gut microbiology. Int Dairy J 9(1):53–61

    Article  Google Scholar 

  16. Frece J, Kos B, Svetec IK, Zgaga Z, Beganovic J, Lebos A, Suskovic J (2009) Synbiotic effect of Lactobacillus helveticus M92 and prebiotics on the intestinal microflora and immune system of mice. J Dairy Res 76(01):98–104

    Article  CAS  Google Scholar 

  17. Bomba A, Nemcova R, Gancarcikova S, Herich R, Guba P, Mudronova D (2002) Improvement of the probiotic effect of micro-organisms by their combination with maltodextrins, fructo-oligosaccharides and polyunsaturated fatty acids. Br J Nutr 88(S1):S95–S99

    Article  CAS  Google Scholar 

  18. Likotrafiti E, Tuohy KM, Gibson GR, Rastall RA (2013) Development of antimicrobial synbiotics using potentially-probiotic faecal isolates of Lactobacillus fermentum and Bifidobacterium longum. Anaerobe 20:5–13

    Article  CAS  Google Scholar 

  19. Huebner J, Wehling RL, Hutkins RW (2007) Functional activity of commercial prebiotics. Int Dairy J 17(7):770–775

    Article  CAS  Google Scholar 

  20. Geeraerd AH, Valdramidis VP, Van Impe JF (2005) GInaFiT, a freeware tool to assess non-log-linear microbial survivor curves. Int J Food Microbiol 102:95–105

    Article  CAS  Google Scholar 

  21. Ristaino PA, Levine MM, Young CR (1983) Improved GM1-enzyme-linked immunosorbent assay for detection of Escherichia coli heat-labile enterotoxin. J Clin Microbiol 18(4):808–815

    Article  CAS  Google Scholar 

  22. Mei GY, Carey CM, Tosh S, Kostrzynska M (2011) Utilization of different types of dietary fibres by potential probiotics. Can J Microbiol 57(10):857–865

    Article  CAS  Google Scholar 

  23. Munoz JAM, Chenoll E, Casinos B, Bataller E, Ramon D, Genoves S, Montava R, Ribes JM, Buesa J, Fabrega J (2011) Novel probiotic Bifidobacterium longum subsp. infantis CECT 7210 strain active against rotavirus infections. Appl Environ Microbiol 77:8775–8783

    Article  CAS  Google Scholar 

  24. Likotrafiti E, Valavani P, Argiriou A, Rhoades J (2015) In vitro evaluation of potential antimicrobial synbiotics using Lactobacillus kefiri isolated from kefir grains. Int Dairy J 45:23–30

    Article  CAS  Google Scholar 

  25. Saulnier DM, Spinler JK, Gibson GR, Versalovic J (2009) Mechanisms of probiosis and prebiosis: considerations for enhanced functional foods. Curr Opinion Biotechnol 20(2):135–141

    Article  CAS  Google Scholar 

  26. Falony G, Verschaeren A, De Bruycker F, De Preter V, Verbeke K, Leroy F, De Vuyst L (2009) In vitro kinetics of prebiotic inulin-type fructan fermentation by butyrate producing colon bacteria: implementation of online gas chromatography for quantitative analysis of carbon dioxide and hydrogen gas production. Appl Environ Microbiol 75:5884–5892

    Article  CAS  Google Scholar 

  27. Barrangou R, Altermann E, Hutkins R, Cano R, Klaenhammer TR (2003) Functional and comparative genomic analyses of an operon involved in fructooligosaccharide utilization by Lactobacillus acidophilus. Proc Natl Acad Sci U S A 100:8957–8962

    Article  CAS  Google Scholar 

  28. Gonzalez-Fandos ME, Sierra M, Garcia-Lopez ML, Fernandez-Alvarez MF, Prieto M, Ote-Ro A (1997) Effect of lactic acid bacteria on growth of Staphylococcus aureus and enterotoxins, and the thermonuclease production in broth. Arch Leb 48(2):38–41

    Google Scholar 

  29. Fooks LJ, Gibson GR (2002) In vitro investigations of the effect of probiotics and prebiotics on selected human intestinal pathogens. FEMS Microbiol Ecol 39(1):67–75

    Article  CAS  Google Scholar 

  30. Ogawa M, Shimizu K, Nomoto K, Tanaka R, Hamabata T, Yamasaki S, Takeda T, Takeda Y (2001) Inhibition of in vitro growth of Shiga toxin-producing Escherichia coli O157:H7 by probiotic Lactobacillus strains due to production of lactic acid. Int J Food Microbiol 68:135–140

    Article  CAS  Google Scholar 

  31. Snijders JM, Van Logtestijn JG, Mossel DA, Smulderst FJ (1985) Lactic acid as a decontaminant in slaughter and processing procedures. Veter Quart 7(4):277–282

    Article  CAS  Google Scholar 

  32. Kostrzynska M, Bachand A (2006) Use of microbial antagonism to reduce pathogen levels on produce and meat products: a review. Can J Microbiol 52(11):1017–1026

    Article  CAS  Google Scholar 

  33. Zhou M, Yu H, Yin X, Sabour PM, Chen W, Gong J (2014) Lactobacillus zeae protects Caenorhabditis elegans from enterotoxigenic Escherichia coli-caused death by inhibiting enterotoxin gene expression of the pathogen. PLoS One 18:9(2)

    Google Scholar 

  34. Dubreuil JD (2017) Enterotoxigenic Escherichia coli and probiotics in swine: what the bleep do we know? Biosci Microbiota Food Health 36:75–90

    Article  CAS  Google Scholar 

  35. Hegde A, Bhat GK, Mallya S (2009) Effect of stress on production of heat-labile enterotoxin by Escherichia coli. Indian J Med Microbiol 27:325–328

    Article  CAS  Google Scholar 

  36. Carey CM, Kostrzynska M, Ojha S, Thompson S (2008) The effect of probiotics and organic acids on Shiga-toxin 2 gene expression in enterohemorrhagic Escherichia coli O157:H7. J Microbiol Meth 73:125–132

    Article  CAS  Google Scholar 

  37. Medellin-Pena MJ, Wang H, Johnson R, Anand S, Griffiths MW (2007) Probiotics affect virulence-related gene expression in Escherichia coli O157:H7. Appl Environ Microbiol 73:4259–4267

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors thank the Director of ICAR-NDRI for supporting the work.

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Correspondence to Surajit Mandal.

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Anand, S., Mandal, S. & Tomar, S.K. Effect of Lactobacillus rhamnosus NCDC 298 with FOS in Combination on Viability and Toxin Production of Enterotoxigenic Escherichia coli . Probiotics & Antimicro. Prot. 11, 23–29 (2019). https://doi.org/10.1007/s12602-017-9327-1

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  • DOI: https://doi.org/10.1007/s12602-017-9327-1

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