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
Casburn-Jones AC, Farthing M (2004) Management of infectious diarrhoea. Gut 53:296–305
Dubreuil JD (2008) Escherichia coli STb toxin and colibacillosis: knowing is half the battle. FEMS Microbiol Lett 278:137–145
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
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
Lebeer S, Vanderleyden J, De Keersmaecker SC (2008) Genes and molecules of lactobacilli supporting probiotic action. Microbiol Mol Bio Rev 72(4):728–764
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
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
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
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
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
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
Gibson GR, Roberfroid MB (1995) Dietary modulation of the colonic micro biota: introducing the concept of prebiotics. J Nutr 125:1401–1412
Preidis GA, Versalovic J (2009) Targeting the human microbiome with antibiotics, probiotics, and prebiotics: gastroenterology enters the metagenomics era. Gastroenterology 136:2015–2031
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
Fooks LJ, Fuller R, Gibson GR (1999) Prebiotics, probiotics and human gut microbiology. Int Dairy J 9(1):53–61
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
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
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
Huebner J, Wehling RL, Hutkins RW (2007) Functional activity of commercial prebiotics. Int Dairy J 17(7):770–775
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
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
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
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
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
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
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
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
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
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
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
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
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
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)
Dubreuil JD (2017) Enterotoxigenic Escherichia coli and probiotics in swine: what the bleep do we know? Biosci Microbiota Food Health 36:75–90
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
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
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
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The authors thank the Director of ICAR-NDRI for supporting the work.
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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