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Technological characterization and survival of the exopolysaccharide-producing strain Lactobacillus delbrueckii subsp. lactis 193 and its bile-resistant derivative 193+ in simulated gastric and intestinal juices

Published online by Cambridge University Press:  21 July 2011

Patricia Burns
Affiliation:
Instituto de Productos Lácteos de Asturias-Consejo Superior de Investigaciones Científicas (IPLA-CSIC), Departamento de Microbiología y Bioquímica de Productos Lácteos. Carretera de Infiesto s/n, 33300 Villaviciosa, Asturias, Spain Instituto de Lactología Industrial (INLAIN, UNL-CONICET), Facultad de Ingeniería Química, Universidad Nacional del Litoral, 1° de Mayo 3250, Santa Fe (3000), Argentina
Gabriel Vinderola
Affiliation:
Instituto de Lactología Industrial (INLAIN, UNL-CONICET), Facultad de Ingeniería Química, Universidad Nacional del Litoral, 1° de Mayo 3250, Santa Fe (3000), Argentina
Jorge Reinheimer
Affiliation:
Instituto de Lactología Industrial (INLAIN, UNL-CONICET), Facultad de Ingeniería Química, Universidad Nacional del Litoral, 1° de Mayo 3250, Santa Fe (3000), Argentina
Isabel Cuesta
Affiliation:
Instituto de Productos Lácteos de Asturias-Consejo Superior de Investigaciones Científicas (IPLA-CSIC), Departamento de Microbiología y Bioquímica de Productos Lácteos. Carretera de Infiesto s/n, 33300 Villaviciosa, Asturias, Spain
Clara G de los Reyes-Gavilán*
Affiliation:
Instituto de Productos Lácteos de Asturias-Consejo Superior de Investigaciones Científicas (IPLA-CSIC), Departamento de Microbiología y Bioquímica de Productos Lácteos. Carretera de Infiesto s/n, 33300 Villaviciosa, Asturias, Spain
Patricia Ruas-Madiedo
Affiliation:
Instituto de Productos Lácteos de Asturias-Consejo Superior de Investigaciones Científicas (IPLA-CSIC), Departamento de Microbiología y Bioquímica de Productos Lácteos. Carretera de Infiesto s/n, 33300 Villaviciosa, Asturias, Spain
*
For correspondance; e-mail:greyes_gavilan@ipla.csic.es

Abstract

The capacity of lactic acid bacteria to produce exopolysaccharides (EPS) conferring microorganisms a ropy phenotype could be an interesting feature from a technological point of view. Progressive adaptation to bile salts might render some lactobacilli able to overcome physiological gut barriers but could also modify functional properties of the strain, including the production of EPS. In this work some technological properties and the survival ability in simulated gastrointestinal conditions of Lactobacillus delbrueckii subsp. lactis 193, and Lb. delbrueckii subsp. lactis 193+, a strain with stable bile-resistant phenotype derived thereof, were characterized in milk in order to know whether the acquisition of resistance to bile could modify some characteristics of the microorganism. Both strains were able to grow and acidify milk similarly; however the production of ethanol increased at the expense of the aroma compound acetaldehyde in milk fermented by the strain 193+, with respect to milk fermented by the strain 193. Both microorganisms produced a heteropolysaccharide composed of glucose and galactose, and were able to increase the viscosity of fermented milks. In spite of the higher production yield of EPS by the bile-resistant strain 193+, it displayed a lower ability to increase viscosity than Lb. delbrueckii subsp. lactis 193. Milk increased survival in simulated gastric juice; the presence of bile improved adhesion to the intestinal cell line HT29-MTX in both strains. However, the acquisition of a stable resistance phenotype did not improve survival in simulated gastric and intestinal conditions or the adhesion to the intestinal cell line HT29-MTX. Thus, Lb. delbrueckii subsp. lactis 193 presents suitable technological properties for the manufacture of fermented dairy products; the acquisition of a stable bile-resistant phenotype modified some properties of the microorganism. This suggests that the possible use of bile-resistant derivative strains should be carefully evaluated in each specific application considering the influence that the acquisition of a stable bile-resistant phenotype could have in survival ability in gastric and intestinal conditions and in technological properties.

Type
Research Article
Copyright
Copyright © Proprietors of Journal of Dairy Research 2011

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References

Axelsson, L 2004 Lactic Acid Bacteria: classification and physiology. In Lactic Acid Bacteria: Microbiological and Functional Aspects, Third Edition, pp 166 (Ed. Salminen, S, von Wright, A. & Ouwehand, A). New York, USA: Marcel Dekker IncGoogle Scholar
Beshkova, D, Simova, E, Frengova, G & Simov, Z 1998 Production of flavour compounds by yogurt starter cultures. Journal of Industrial Microbiology & Biotechnology 20 180186CrossRefGoogle Scholar
Bron, PA, Marco, M, Hoffer, SM, Van Mullekom, E, de Vos, WM & Kleerebezem, M 2004 Genetic characterization of the bile salt response in Lactobacillus plantarum and analysis of responsive promoters in vitro and in situ in the gastrointestinal tract. Journal of Bacteriology 186 78297835CrossRefGoogle ScholarPubMed
Burns, P, Sánchez, B, Vinderola, G, Ruas-Madiedo, P, Ruiz, L, Margolles, A, Reinheimer, & de los Reyes-Gavilán, CG 2010 Inside the adaptation process of Lactobacillus delbrueckii subsp. lactis to bile. International Journal of Food Microbiology 142 132141CrossRefGoogle ScholarPubMed
Burns, P, Vinderola, G, Binetti, A, Quiberoni, A, de los Reyes-Gavilán, CG & Reinheimer, JA 2008 Bile-resistant derivatives obtained from non-intestinal dairy lactobacilli. International Dairy Journal 18 377385CrossRefGoogle Scholar
Burns, P, Vinderola, G & Reinheimer, J 2011 Impact of bile salt adaptation of L. delbrueckii subsp. lactis 200 on its interaction capacity with the gut. Research in Microbiology (submitted for publication)CrossRefGoogle Scholar
Cenci, G, Rossi, J, Trotta, F & Caldini, G 2002 Lactic acid bacteria isolated from dairy products inhibit genotoxic effect of 4-nitroquinoline-1-oxide in SOS-chromotest. Systematic and Applied Microbiology 25 483490CrossRefGoogle ScholarPubMed
Ciucanu, I & Kerek, F 1984 A simple and rapid method for the permethylation of carbohydrates. Carbohydrate Research 131 209217CrossRefGoogle Scholar
Cogan, TM 1995 Flavor production by dairy starter cultures. Journal of Applied Bacteriology 79 S49S64Google Scholar
Cogan, TM, Beresford, TP, Steele, J, Broadbent, J, Shah, NP & Ustunol, Z 2007 Advances in starter cultures and cultured foods. Journal of Dairy Science 90 40054021CrossRefGoogle ScholarPubMed
Elli, M, Callegari, ML, Ferrari, S, Bessi, E, Cattivelli, D, Soldi, S, Morelli, L, Goupil Feuillerat, N & Antoine, JM 2006 Survival of yogurt bacteria in the human gut. Applied and Environmental Microbiology 72 51135117CrossRefGoogle ScholarPubMed
Gilliland, SE 1998 Fermented milks and probiotics: Applied Dairy Microbiology, pp 195212 (Ed. Marth, EH & Steel, JL). New York, USA: Marcel Dekker IncGoogle Scholar
Giraffa, G, de Vecchi, P & Rossetti, L 1998 Note: Identification of Lactobacillus delbrueckii subspecies bulgaricus and subspecies lactis dairy isolates by amplified rDNA restriction analysis. Journal of Applied Microbiology 85 918924CrossRefGoogle ScholarPubMed
Gómez-Zavaglia, A, Kociubinski, G, Perez, P, Disalvo, E & DeAntoni, G 2002 Effect of bile on the lipid composition and surface properties of bifidobacteria. Journal of Applied Microbiology 93 794799CrossRefGoogle ScholarPubMed
Gueimonde, M, Noriega, L, Margolles, A, de los Reyes-Gavilán, CG & Salminen, S 2005 Ability of Bifidobacterium strains with acquired resistance to bile to adhere to human intestinal mucus. International Journal of Food Microbiology 101 341346CrossRefGoogle ScholarPubMed
Guglielmotti, D, Briggiler Marcó, M, Vinderola, C, de los Reyes-Gavilán, CG, Reinheimer, J & Quiberoni, A 2007 Spontaneous Lactobacillus delbrueckii phage-resistant mutants with acquired bile tolerance. International Journal of Food Microbiology 119 236242CrossRefGoogle ScholarPubMed
Hassan, AN 2008 ADSA Foundation Scholar Award: Possibilities and challenges of exopolysaccharide-producing lactic cultures in dairy foods. Journal of Dairy Science 91 12821298CrossRefGoogle ScholarPubMed
Hebert, EM, Mamone, G, Picariello, G, Raya, RR, Savoy, G, Ferranti, P & Addeo, F 2008 Characterization of the pattern of alpha(s1)- and beta-casein breakdown and release of a bioactive peptide by a cell envelope proteinase from Lactobacillus delbrueckii subsp. lactis CRL 581. Applied and Environmental Microbiology 74 36823689CrossRefGoogle ScholarPubMed
Hellinga, C, Somesen, DJ & Koenraads, JPJM 1989 Viscosity of stirred yoghurt: modern techniques useful in analysing and improving routine measurements. Netherland Milk and Dairy Journal 40 217240Google Scholar
Lahtinen, SJ, Ouwehand, AC, Reinikainen, JP, Korpela, JM, Sandholm, J, & Salminen, SJ 2006 Intrinsic properties of so-called dormant probiotic bacteria, determined by flow cytometric viability assays. Applied and Environmental Microbiology 72 51325134CrossRefGoogle ScholarPubMed
Leal, JA, Jimenez-Barbero, J, Bernabé, M & Prieto, A 2008 Structural elucidation of a cell wall fungal polysaccharide isolated from Ustilaginoidea virens, a pathogenic fungus of Oriza sativa and Zea mays. Carbohydrate Research 343 29802984CrossRefGoogle ScholarPubMed
Lee, K, Lee, HG & Choi, YJ 2008 Proteomic analysis of the effect of bile salts on the intestinal and probiotic bacterium Lactobacillus reuteri. Journal of Biotechnology 137 1419CrossRefGoogle ScholarPubMed
Lesuffleur, T, Barbat, A, Dussaulx, E & Zweibaum, A 1990 Growth adaptation to methotrexate of HT-29 human colon-carcinoma cells is associated with their ability to differentiate into columnar and mucus-secreting cells. Cancer Research 50 63346343Google ScholarPubMed
Lick, S, Drescher, K & Heller, KJ 2001 Survival of Lactobacillus delbrueckii subsp. bulgaricus and Streptococcus thermophilus in the terminal ileum of fistulated Göttingen minipigs. Applied and Environmental Microbiology 67 41374143CrossRefGoogle ScholarPubMed
Lucey, JA & Singh, H 1998 Formation and physical properties of acid milk gels: a review. Food Research International 30 529542CrossRefGoogle Scholar
Marteau, P, Minekus, M, Havenaar, R & Huis In't Veld, JHJ 1997 Survival of lactic acid bacteria in a dynamic model of the stomach and small intestine: validation and the effects of bile. Journal of Dairy Science 80 10311037CrossRefGoogle Scholar
Mater, DDG, Bretigny, L, Firmesse, O, Flores, MJ, Mogenet, A, Bresson, JL & Corthier, G 2005 Streptococcus thermophilus and Lactobacillus delbrueckii subsp. bulgaricus survive gastrointestinal transit of healthy volunteers consuming yogurt. FEMS Microbiology Letters 250 185187CrossRefGoogle ScholarPubMed
Mozzi, F, Vaningelgem, F, Hébert, EM, van der Meulen, R, Moreno, MRF, de Valdez, GF & De Vuyst, L 2006 Diversity of heteropolysaccharides-producing lactic acid bacterium strains and their biopolymers. Applied and Environmental Microbiology 72 44314435CrossRefGoogle ScholarPubMed
Noriega, L, Gueimonde, M, Sánchez, B, Margolles, A & de los Reyes-Gavilán, CG 2004 Effect of the adaptation to high bile salts concentrations on glycosidic activity, survival at low pH and cross-resistance to bile salts in Bifidobacterium. International Journal of Food Microbiology 94 7986CrossRefGoogle Scholar
Pinto, SM, das Graças Clemente, M & Ronaldo de Abreu, L 2009 Behaviour of volatile compounds during the shelf life of yogurt. International Journal of Dairy Technology 62 215223CrossRefGoogle Scholar
Qian, M & Reineccius, G 2003 Potent aroma compounds in Parmigiano Reggiano cheese studied using a dynamic headspace (purge-trap) method. Flavour and Frangrance Journal 18 252259CrossRefGoogle Scholar
Ruas-Madiedo, P, Alting, AC & Zoon, P 2005 Effect of exopolysaccharides and proteolytic activity of Lactococcus lactis subsp. cremoris strains on the viscosity and structure of fermented milks. International Dairy Journal 15 155164CrossRefGoogle Scholar
Ruas-Madiedo, P, Gueimonde, M, Arigoni, F, de los Reyes-Gavilán, CG & Margolles, A 2009a Bile affects the synthesis of exopolysaccharides by Bifidobacterium animalis. Applied and Environmental Microbiology 75 12041207CrossRefGoogle ScholarPubMed
Ruas-Madiedo, P, Medrano, M, Salazar, N, de los Reyes-Gavilán, CG, Pérez, PF & Abraham, A 2010 Exopolysaccharides produced by Lactobacillus and Bifidobacterium strains abrogate in vitro the cytotoxic effect of bacterial toxins on eukaryotic cells. Journal of Applied Microbiology 109 20792086CrossRefGoogle ScholarPubMed
Ruas-Madiedo, P, Salazar, N & de los Reyes-Gavilán, CG 2009b Biosynthesis and biochemical analysis of exopolysaccharides produced by lactic acid bacteria. In Bacterial polysaccharides: current innovations and future trends, pp 279310 (Ed. Ullrich, M). Pittsburg (Pennsylvania), USA: Caister Academic PressGoogle Scholar
Ruas-Madiedo, P, Salazar, N & de los Reyes-Gavilán, CG 2009c Exopolysaccharides produced by lactic acid bacteria in food and probiotic applications. In Microbial Glycobiology: structures, relevance and applications, pp 887902 (Eds. Moran, A, Brennan, P, Holst, O, von Itzstein, M). San Diego, CA, USA: ElsevierGoogle Scholar
Ruas-Madiedo, P, Tuinier, R, Kanning, M & Zoon, P 2002 Role of exopolysaccharides produced by Lactococcus lactis subsp. cremoris on the viscosity of fermented milks. International Dairy Journal 12 689695CrossRefGoogle Scholar
Ruiz, L, Sánchez, B, Ruas-Madiedo, P, de los Reyes-Gavilán, CG & Margolles, A 2007 Cell envelope changes in Bifidobacterium animalis ssp.lactis as a response to bile. FEMS Microbiology Letters 274 316322CrossRefGoogle ScholarPubMed
Salazar, N, Prieto, A, Leal, JA, Mayo, B, Bada-Gancedo, JC, de los Reyes-Gavilán, CG & Ruas-Madiedo, P 2009 Production of exopolysaccharides by Lactobacillus and Bifidobacterium strains from human origin and metabolic activity of the producing bacteria in milk. Journal of Dairy Science 92 41584168CrossRefGoogle ScholarPubMed
Sánchez, B, de los Reyes-Gavilán, CG & Margolles, A 2006 The F1F0-ATPase of Bifidobacterium animalis is involved in bile tolerance. Environmental Microbiology 8 18251833CrossRefGoogle ScholarPubMed
Sánchez, B, Fernández-García, M, Margolles, A, de los Reyes-Gavilán, CG & Ruas-Madiedo, P 2010 Technological and probiotic selection criteria of a bile-adapted Bifidobacterium animalis subsp. lactis strain. International Dairy Journal 20 800805CrossRefGoogle Scholar
Sánchez, B, Ruíz, L, de los Reyes-Gavilán, CG & Margolles, A 2008 Proteomics of stress response in Bifidobacterium. Frontiers in Biosciences 13 69056919CrossRefGoogle ScholarPubMed
Sarkar, S 2010 Approaches for enhancing the viability of probiotics: a review. British Food Journal 112 329349CrossRefGoogle Scholar
Schillinger, U, Guigas, C & Holzapfel, WH 2005 In vitro adherence and other properties of lactobacilli used in probiotic yoghurt-like products. International Dairy Journal 15 12891297CrossRefGoogle Scholar
Shene, C & Bravo, S 2007 Whey fermentation by Lactobacillus delbrueckii subsp. bulgaricus for exopolysaccharide production in continuous culture. Enzyme and Microbial Technology 40 15781584CrossRefGoogle Scholar
Tannock, GW 2003 The intestinal microflora. In Gut flora: nutrition, immunity and health, pp 123 (Eds. Fuller, R & Perdigón, G). Oxford, UK: Backwell PressGoogle Scholar
van Marle, ME & Zoon, P 1995 Permeability and rheological properties of microbially and chemically acidified skim-milk gels. Netherlands Milk and Dairy Journal 49 4765Google Scholar
Vinderola, G & Reinheimer, J 2003 Lactic acid starter and probiotic bacteria: a comparative ‘in vitro’ study of probiotic characteristics and biological barrier resistance. Food Research International 36 895904CrossRefGoogle Scholar
Wall, R, Fitzgerald, G, Hussey, S, Ryan, T, Murphy, B, Ross, P & Stanton, C 2007 Genomic diversity of cultivable Lactobacillus populations residing in the neonatal and adult gastrointestinal tract. FEMS Microbiology Ecology 59 127137CrossRefGoogle ScholarPubMed