Abstract
The present study attempted to partially characterize and elucidate the viability-enhancing effect of a yeast strain Saccharomyces cerevisiae EC-1118 on a probiotic strain Lactobacillus rhamnosus HN001 under acidic conditions using a model system (non-growing cells). The yeast was found to significantly enhance (P < 0.05) the viability of the probiotic strain under acidic conditions (pH 2.5 to 4.0) by 2 to 4 log cycles, and the viability-enhancing effects were observed to be influenced by pH, and probiotic and yeast concentrations. Microscopic observation and co-aggregation assay revealed that the viability-enhancing effect of the yeast could be attributed to direct cell-cell contact co-aggregation mediated by yeast cell surface and/or cell wall components or metabolites. Furthermore, non-viable yeast cells killed by thermal means were observed to enhance the viability of the probiotic strain as well, suggesting that the surface and/or cell wall component(s) of the yeast contributing to co-aggregation was heat-stable. Cell-free yeast supernatant was also found to enhance the viability of the probiotic strain, indicating the presence of protective yeast metabolite(s) in the supernatant. These findings laid the foundation for further understanding of the mechanism(s) involved and for developing novel microbial starter cultures possibly without the use of live yeast for ambient-stable high-moisture probiotic foods.
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References
Barriga JAT, Cooper DG, Idziak ES, Cameron DR (1999) Components of the bioemulsifier from S. cerevisiae. Enzym Microb Technol 25(1–2):96–102. doi:10.1016/S0141-0229(99)00032-0
Caselli M, Cassol F, Calò G, Holton J, Zuliani G, Gasbarrini A (2013) Actual concept of “probiotics”: Is it more functional to science or business? World J Gastroenterol: WJG 19(10):1527–1540. doi:10.3748/wjg.v19.i10.1527
Champagne CP, Gardner NJ, Roy D (2005) Challenges in the addition of probiotic cultures to foods. Crit Rev Food Sci Nutr 45(1):61–84. doi:10.1080/10408690590900144
Conway PL (1996) Selection criteria for probiotic microorganisms. Asia Pac J Clin Nutr 5(1):10–14
Corcoran BM, Stanton C, Fitzgerald GF, Ross RP (2005) Survival of probiotic lactobacilli in acidic environments is enhanced in the presence of metabolizable sugars. Appl Environ Microbiol 71(6):3060–3067. doi:10.1128/aem.71.6.3060-3067.2005
Cotter PD, Hill C (2003) surviving the acid test: responses of Gram-positive bacteria to low pH. Microbiol Mol Biol Rev 67(3):429–453. doi:10.1128/MMBR.67.3.429-453.2003
Ganan M, Carrascosa AV, de Pascual-Teresa S, Martinez-Rodriguez AJ (2012) Effect of mannoproteins on the growth, gastrointestinal viability, and adherence to Caco-2 cells of lactic acid bacteria. J Food Sci 77(3):M176–M180. doi:10.1111/j.1750-3841.2011.02602.x
Ganesan B, Stuart MR, Weimer BC (2007) Carbohydrate starvation causes a metabolically active but nonculturable state in Lactococcus lactis. Appl Environ Microbiol 73(8):2498–2512. doi:10.1128/aem.01832-06
Hamdan IY, Deane DD, Kunsman JE (1971) Effect of potassium sorbate on yogurt cultures. J Milk Food Technol 34:307–311
Han JH, Floros JD (1998) Modeling the growth inhibition kinetics of baker's yeast by potassium sorbate using statistical approaches. J Food Sci 63(1):12–14. doi:10.1111/j.1365-2621.1998.tb15664.x
Hirayama S, Furukawa S, Ogihara H, Morinaga Y (2012) Yeast mannan structure necessary for co-aggregation with Lactobacillus plantarum ML11-11. Biochem Biophys Res Commun 419(4):652–655. doi:10.1016/j.bbrc.2012.02.068
Hutkins RW, Nannen NL (1993) pH homeostasis in lactic acid bacteria. J Dairy Sci 76(8):2354–2365. doi:10.3168/jds.S0022-0302(93)77573-6
Kim D-S, Thomas S, Fogler HS (2000) Effects of pH and trace minerals on long-term starvation of Leuconostoc mesenteroides. Appl Environ Microbiol 66(3):976–981
Klaenhammer TR, Kullen MJ (1999) Selection and design of probiotics. Int J Food Microbiol 50(1–2):45–57. doi:10.1016/S0168-1605(99)00076-8
Lahtinen SJ (2012) Probiotic viability - does it matter? Microb Ecol Health Dis 23:18567. doi:10.3402/mehd.v23i0.18567
Lee YK, Salminen S (2009) Handbook of probiotics and prebiotics, 2nd edn. Wiley, Hoboken
Lee PR, Ong YL, Yu B, Curran P, Liu SQ (2010) Profile of volatile compounds during papaya juice fermentation by a mixed culture of Saccharomyces cerevisiae and Williopsis saturnus. Food Microbiol 27(7):853–861. doi:10.1016/j.fm.2010.05.010
Liu SQ, Tsao M (2009) Enhancement of survival of probiotic and non-probiotic lactic acid bacteria by yeasts in fermented milk under non-refrigerated conditions. Int J Food Microbiol 135(1):34–38. doi:10.1016/j.ijfoodmicro.2009.07.017
Liu SQ, Tsao M (2010) Enhancing stability of lactic acid bacteria and probiotics by Williopsis saturnus var. saturnus in fermented milks. Nutr Food Sci 40(3):314–322. doi:10.1108/00346651011044014
Lourens-Hattingh A, Viljoen BC (2001) Growth and survival of a probiotic yeast in dairy products. Food Res Int 34(9):791–796. doi:10.1016/S0963-9969(01)00085-0
Özer D, Akin S, Özer B (2005) Effect of inulin and lactulose on survival of Lactobacillus Acidophilus LA-5 and Bifidobacterium Bifidum BB-02 in acidophilus-bifidus yoghurt. Food Sci Technol Intl 11(1):1924. doi:10.1177/1082013205051275
Pearse AGE (1980) Histochemistry, theoretical and applied vol 1. Preparative and optical technology, Churchhill Livingstone
Reid AA, Champagne CP, Gardner N, Fustier P, Vuillemard JC (2007) Survival in food systems of Lactobacillus rhamnosus R011 microentrapped in whey protein gel particles. J Food Sci 72(1):M031–M037. doi:10.1111/j.1750-3841.2006.00222.x
Ruiz L, Ruas-Madiedo P, Gueimonde M, de Los Reyes-Gavilan CG, Margolles A, Sanchez B (2011) How do bifidobacteria counteract environmental challenges? Mechanisms involved and physiological consequences. Genes Nutr 6(3):307–318. doi:10.1007/s12263-010-0207-5
Russo P, López P, Capozzi V, de Palencia PF, Dueñas MT, Spano G, Fiocco D (2012) Beta-glucans improve growth, viability and colonization of probiotic microorganisms. Int J Mol Sci 13(5):6026–6039. doi:10.3390/ijms13056026
Saarela M, Mogensen G, Fondén R, Mättö J, Mattila-Sandholm T (2000) Probiotic bacteria: safety, functional and technological properties. J Biotechnol 84(3):197–215. doi:10.1016/S0168-1656(00)00375-8
Sanders ME (2008) Probiotics: definition, sources, selection, and uses. Clin Infect Dis 46(Supplement 2):S58–S61. doi:10.1086/523341
Sashihara T, Sueki N, Ikegami S (2006) An analysis of the effectiveness of heat-killed lactic acid bacteria in alleviating allergic diseases. J Dairy Sci 89(8):2846–2855. doi:10.3168/jds.S0022-0302(06)72557-7
Stack HM, Kearney N, Stanton C, Fitzgerald GF, Ross RP (2010) Association of beta-glucan endogenous production with increased stress tolerance of intestinal lactobacilli. Appl Environ Microbiol 76(2):500–507. doi:10.1128/AEM.01524-09
Stuart MR, Chou LS, Weimer BC (1999) Influence of carbohydrate starvation and arginine on culturability and amino acid utilization of Lactococcus lactis subsp. lactis. Appl Environ Microbiol 65(2):665–673
Suharja AAS, Henriksson A, Liu S-Q (2014) Impact of Saccharomyces cerevisiae on viability of probiotic Lactobacillus rhamnosus in fermented milk under ambient conditions. J Food Process Preserv 38(1):326–337. doi:10.1111/j.1745-4549.2012.00780.x
Tamime AY, Saarela M, Søndergaard AK, Mistry VV, Shah NP (2007) Production and maintenance of viability of probiotic micro-organisms in dairy products. In: Tamime A (ed) Probiotic dairy products. Blackwell Science Ltd, Oxford, pp 39–72. doi:10.1002/9780470995785.ch3
van der Veen S, Abee T (2011) Mixed species biofilms of Listeria monocytogenes and Lactobacillus plantarum show enhanced resistance to benzalkonium chloride and peracetic acid. Int J Food Microbiol 144(3):421–431. doi:10.1016/j.ijfoodmicro.2010.10.029
Vasiljevic T, Shah NP (2008) Probiotics—From Metchnikoff to bioactives. Int Dairy J 18(7):714–728. doi:10.1016/j.idairyj.2008.03.004
Xie N, Zhou T, Li B (2012) Kefir yeasts enhance probiotic potentials of Lactobacillus paracasei H9: The positive effects of coaggregation between the two strains. Food Res Int 45(1):394–401. doi:10.1016/j.foodres.2011.10.045
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Lim, P.L., Toh, M. & Liu, S.Q. Saccharomyces cerevisiae EC-1118 enhances the survivability of probiotic Lactobacillus rhamnosus HN001 in an acidic environment. Appl Microbiol Biotechnol 99, 6803–6811 (2015). https://doi.org/10.1007/s00253-015-6560-y
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DOI: https://doi.org/10.1007/s00253-015-6560-y