1887

Abstract

The effect of inclusion of various C18 fatty acids with 0–2 double bonds in either or configuration on GG survival was analysed in simulated gastric juice at pH 2.5. The incorporation of Tween 80 (1 g l) in the growth media enhanced subsequent survival of stationary-phase cultures up to 1000-fold following 90 min acid exposure compared with controls grown without Tween 80. There was a significant (<0.05) increase in bacterial content of oleic acid [C18 : 1 (9c), up to 55-fold] after growth of bacteria in MRS supplemented with Tween 80. The inclusion of various C18 fatty acids in the growth media revealed that only oleic and vaccenic acids [C18 : 1 (11t)] had protective effects on the survival of GG when exposed to the acidic environment. Comparative analysis with other lactobacilli indicated that all strains exhibited increased survival when grown in the presence of Tween 80. Further work with a neomycin-resistant mutant with 48 % of the FF-ATPase activity of the parent indicated that the Tween 80 effect was independent of the complex. The mechanisms behind the effect of fatty acid protection were investigated and proton permeability assays showed that cultures grown in the presence of Tween 80 had higher extracellular pH than controls. Furthermore, there was a significant reduction of oleic acid and a significant increase in stearic acid (C18 : 0) (<0.05) content of bacterial cells following exposure of Tween 80-supplemented cultures to simulated gastric juice. Overall, the data suggest that probiotic lactobacilli can use an exogenous oleic acid source to increase their acid survival and the underlying mechanism most likely involves the ability of increased membrane oleic acid to be reduced by H to stearic acid.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.28966-0
2007-01-01
2019-10-19
Loading full text...

Full text loading...

/deliver/fulltext/micro/153/1/291.html?itemId=/content/journal/micro/10.1099/mic.0.28966-0&mimeType=html&fmt=ahah

References

  1. Ananta, E., Birkeland, S.-E., Corcoran, B., Fitzgerald, G., Hinz, S., Klijn, A., Maettoe, J., Mercernier, A., Nilsson, U., Nyman, M. & other authors ( 2004; ). Processing effects on the nutritional advancement of probiotics and prebiotics. Microb Ecol Health Dis 16, 114–124.
    [Google Scholar]
  2. Bender, G. R., Sutton, S. V. & Marquis, R. E. ( 1986; ). Acid tolerance, proton permeabilities, and membrane ATPases of oral streptococci. Infect Immun 53, 331–338.
    [Google Scholar]
  3. Beumer, R. R., de Vries, J. & Rombouts, F. M. ( 1992; ). Campylobacter jejuni non-culturable coccoid cells. Int J Food Microbiol 15, 153–163.[CrossRef]
    [Google Scholar]
  4. Bolotin, A., Wincker, P., Mauger, S., Jaillon, O., Malarme, K., Weissenbach, J., Ehrlich, S. D. & Sorokin, A. ( 2001; ). The complete genome sequence of the lactic acid bacterium Lactococcus lactis ssp. lactis IL1403. Genome Res 11, 731–753.[CrossRef]
    [Google Scholar]
  5. Budin-Verneuil, A., Maguin, E., Auffray, Y., Ehrlich, S. D. & Pichereau, V. ( 2005; ). Transcriptional analysis of the cyclopropane fatty acid synthase gene of Lactococcus lactis MG1363 at low pH. FEMS Microbiol Lett 250, 189–194.[CrossRef]
    [Google Scholar]
  6. Chang, Y. Y. & Cronan, J. E., Jr ( 1999; ). Membrane cyclopropane fatty acid content is a major factor in acid resistance of Escherichia coli. Mol Microbiol 33, 249–259.[CrossRef]
    [Google Scholar]
  7. Charalampopoulos, D., Pandiella, S. S. & Webb, C. ( 2003; ). Evaluation of the effect of malt, wheat and barley extracts on the viability of potentially probiotic lactic acid bacteria under acidic conditions. Int J Food Microbiol 82, 133–141.[CrossRef]
    [Google Scholar]
  8. Coakley, M., Ross, R. P., Nordgren, M., Fitzgerald, G., Devery, R. & Stanton, C. ( 2003; ). Conjugated linoleic acid biosynthesis by human-derived Bifidobacterium species. J Appl Microbiol 94, 138–145.[CrossRef]
    [Google Scholar]
  9. Conway, P. L., Gorbach, S. L. & Goldin, B. R. ( 1987; ). Survival of lactic acid bacteria in the human stomach and adhesion to intestinal cells. J Dairy Sci 70, 1–12.[CrossRef]
    [Google Scholar]
  10. Corcoran, B. M., Ross, R. P., Fitzgerald, G. F. & Stanton, C. ( 2004; ). Comparative survival of probiotic lactobacilli spray-dried in the presence of prebiotic substances. J Appl Microbiol 96, 1024–1039.[CrossRef]
    [Google Scholar]
  11. Corcoran, B. M., Ross, R. P., Fitzgerald, G. F. & Stanton, C. ( 2005; ). Survival of probiotic lactobacilli in acidic environments is enhanced in the presence of metabolizable sugars. Appl Environ Microbiol 71, 3060–3067.[CrossRef]
    [Google Scholar]
  12. Cotter, P. D., Gahan, C. G. & Hill, C. ( 2001; ). A glutamate decarboxylase system protects Listeria monocytogenes in gastric fluid. Mol Microbiol 40, 465–475.[CrossRef]
    [Google Scholar]
  13. deMan, J. C., Rogosa, M. & Sharpe, M. E. ( 1960; ). A medium for the cultivation of lactobacilli. J Appl Bacteriol 23, 130–135.[CrossRef]
    [Google Scholar]
  14. Desmond, C., Ross, R. P., O'Callaghan, E., Fitzgerald, G. & Stanton, C. ( 2002; ). Improved survival of Lactobacillus paracasei NFBC 338 in spray-dried powders containing gum acacia. J Appl Microbiol 93, 1003–1011.[CrossRef]
    [Google Scholar]
  15. de Vrese, M., Winkler, P., Rautenberg, P., Harder, T., Noah, C., Laue, C., Ott, S., Hampe, J., Schreiber, S. & other authors ( 2005; ). Effect of Lactobacillus gasseri PA 16/8, Bifidobacterium longum SP 07/3, B. bifidum MF 20/5 on common cold episodes: a double blind, randomized, controlled trial. Clin Nutr 24, 481–491.[CrossRef]
    [Google Scholar]
  16. FAO/WHO ( 2001; ). Evaluation of health and nutritional properties of powder milk with live lactic acid bacteria. Report from FAO/WHO expert consultation 1–4 October.
  17. Fozo, E. M. & Quivey, R. G., Jr ( 2004a; ). The fabM gene product of Streptococcus mutans is responsible for the synthesis of monounsaturated fatty acids and is necessary for survival at low pH. J Bacteriol 186, 4152–4158.[CrossRef]
    [Google Scholar]
  18. Fozo, E. M. & Quivey, R. G., Jr ( 2004b; ). Shifts in the membrane fatty acid profile of Streptococcus mutans enhance survival in acidic environments. Appl Environ Microbiol 70, 929–936.[CrossRef]
    [Google Scholar]
  19. Fozo, E. M., Kajfasz, J. K. & Quivey, R. G., Jr ( 2004; ). Low pH-induced membrane fatty acid alterations in oral bacteria. FEMS Microbiol Lett 238, 291–295.[CrossRef]
    [Google Scholar]
  20. Gardiner, G., Stanton, C., Lynch, P. B., Collins, J. K., Fitzgerald, G. & Ross, R. P. ( 1999; ). Evaluation of cheddar cheese as a food carrier for delivery of a probiotic strain to the gastrointestinal tract. J Dairy Sci 82, 1379–1387.[CrossRef]
    [Google Scholar]
  21. Guandalini, S., Pensabene, L., Zikri, M. A., Dias, J. A., Casali, L. G., Hoekstra, H., Kolacek, S., Massar, K., Micetic-Turk, D. & other authors ( 2000; ). Lactobacillus GG administered in oral rehydration solution to children with acute diarrhoea: a multicenter European trial. J Pediatr Gastroenterol Nutr 30, 54–60.[CrossRef]
    [Google Scholar]
  22. Guerrini, S., Bastianini, A., Granchi, L. & Vincenzini, M. ( 2002; ). Effect of oleic acid on Oenococcus oeni strains and Malolactic fermentation in wine. Curr Microbiol 44, 5–9.[CrossRef]
    [Google Scholar]
  23. Guillot, A., Obis, D. & Mistou, M. Y. ( 2000; ). Fatty acid membrane composition and activation of glycine-betaine transport in Lactococcus lactis subjected to osmotic stress. Int J Food Microbiol 55, 47–51.[CrossRef]
    [Google Scholar]
  24. Holzapfel, W. H. & Schillinger, U. ( 2002; ). Introduction to pre- and probiotics. Food Res Int 35, 109–116.[CrossRef]
    [Google Scholar]
  25. Ishibashi, N. & Shimamura, S. ( 1993; ). Bifidobacteria: research and development in Japan. Food Technol 46, 126–135.
    [Google Scholar]
  26. Isolauri, E., Juntunen, M., Rautanen, T., Sillanaukee, P. & Koivula, T. ( 1991; ). A human Lactobacillus strain (Lactobacillus casei sp. strain GG) promotes recovery from acute diarrhea in children. Pediatrics 88, 90–97.
    [Google Scholar]
  27. Jacobsen, C. N., Rosenfeldt Nielsen, V., Hayford, A. E., Moller, P. L., Michaelsen, K. F., Paerregaard, A., Sandstrom, B., Tvede, M. & Jakobsen, M. ( 1999; ). Screening of probiotic activities of forty-seven strains of Lactobacillus spp. by in vitro techniques and evaluation of the colonization ability of five selected strains in humans. Appl Environ Microbiol 65, 4949–4956.
    [Google Scholar]
  28. Jacques, N. A., Hardy, L., Knox, K. W. & Wicken, A. J. ( 1980; ). Effect of Tween 80 on the morphology and physiology of Lactobacillus salivarius strain IV CL-37 grown in a chemostat under glucose limitation. J Gen Microbiol 119, 195–201.
    [Google Scholar]
  29. Jacques, N. A., Jacques, V. L., Wolf, A. C. & Wittenberger, C. L. ( 1985; ). Does an increase in membrane unsaturated fatty acids account for Tween 80 stimulation of glucosyltransferase secretion by Streptococcus salivarius? J Gen Microbiol 131, 67–72.
    [Google Scholar]
  30. Johnsson, T., Nikkila, P., Toivonen, L., Rosenqvist, H. & Laakso, S. ( 1995; ). Cellular fatty acid profiles of Lactobacillus and Lactococcus strains in relation to the oleic acid content of the cultivation medium. Appl Environ Microbiol 61, 4497–4499.
    [Google Scholar]
  31. Kalliomaki, M., Salminen, S., Arvilommi, H., Kero, P., Koskinen, P. & Isolauri, E. ( 2001; ). Probiotics in primary prevention of atopic disease: a randomised placebo-controlled trial. Lancet 357, 1076–1079.[CrossRef]
    [Google Scholar]
  32. Kankaanpää, P. E., Salminen, S. J., Isolauri, E. & Lee, Y. K. ( 2001; ). The influence of polyunsaturated fatty acids on probiotic growth and adhesion. FEMS Microbiol Lett 194, 149–153.[CrossRef]
    [Google Scholar]
  33. Klaenhammer, T. R., Barrangou, R., Buck, B. L., Azcarate-Peril, M. A. & Altermann, E. ( 2005; ). Genomic features of lactic acid bacteria effecting bioprocessing and health. FEMS Microbiol Rev 29, 393–409.[CrossRef]
    [Google Scholar]
  34. Kullen, M. J. & Klaenhammer, T. R. ( 1999; ). Identification of the pH-inducible, proton-translocating F1F0-ATPase (atpBEFHAGDC) operon of Lactobacillus acidophilus by differential display: gene structure, cloning and characterization. Mol Microbiol 33, 1152–1161.
    [Google Scholar]
  35. Lavermicocca, P., Valerio, F., Lonigro, S. L., De Angelis, M., Morelli, L., Callegari, M. L., Rizzello, C. G. & Visconti, A. ( 2005; ). Study of adhesion and survival of lactobacilli and bifidobacteria on table olives with the aim of formulating a new probiotic food. Appl Environ Microbiol 71, 4233–4240.[CrossRef]
    [Google Scholar]
  36. Ma, Y. & Marquis, R. E. ( 1997; ). Thermophysiology of Streptococcus mutans and related lactic-acid bacteria. Antonie Van Leeuwenhoek 72, 91–100.[CrossRef]
    [Google Scholar]
  37. Machado, M. C., Lopez, C. S., Heras, H. & Rivas, E. A. ( 2004; ). Osmotic response in Lactobacillus casei ATCC 393: biochemical and biophysical characteristics of membrane. Arch Biochem Biophys 422, 61–70.[CrossRef]
    [Google Scholar]
  38. O'Mahony, L., McCarthy, J., Kelly, P., Hurley, G., Luo, F., Chen, K., O'Sullivan, G. C., Kiely, B., Collins, J. K. & other authors ( 2005; ). Lactobacillus and Bifidobacterium in irritable bowel syndrome: symptom responses and relationship to cytokine profiles. Gastroenterology 128, 541–551.[CrossRef]
    [Google Scholar]
  39. O'Riordan, K., Andrews, D., Buckle, K. & Conway, P. ( 2001; ). Evaluation of microencapsulation of a Bifidobacterium strain with starch as an approach to prolonging viability during storage. J Appl Microbiol 91, 1059–1066.[CrossRef]
    [Google Scholar]
  40. Partanen, L., Marttinen, N. & Alatossava, T. ( 2001; ). Fats and fatty acids as growth factors for Lactobacillus delbrueckii. Syst Appl Microbiol 24, 500–506.[CrossRef]
    [Google Scholar]
  41. Raychowdhury, M. K., Goswami, R. & Chakrabarti, P. ( 1985; ). Effect of unsaturated fatty acids in growth inhibition of some penicillin-resistant and sensitive bacteria. J Appl Bacteriol 59, 183–188.[CrossRef]
    [Google Scholar]
  42. Saarela, M., Rantala, M., Hallamaa, K., Nohynek, L., Virkajarvi, I. & Matto, J. ( 2004; ). Stationary-phase acid and heat treatments for improvement of the viability of probiotic lactobacilli and bifidobacteria. J Appl Microbiol 96, 1205–1214.[CrossRef]
    [Google Scholar]
  43. Saxelin, M., Pessi, T. & Salminen, S. ( 1995; ). Fecal recovery following oral administration of Lactobacillus strain GG (ATCC 53103) in gelatine capsules to healthy volunteers. Int J Food Microbiol 25, 199–203.[CrossRef]
    [Google Scholar]
  44. Stanton, C., Lawless, F., Kjellmer, G., Harrington, D., Devery, R., Connolly, J. F. & Murphy, J. ( 1997; ). Dietary Influences on bovine milk cis-9, trans-11-conjugated linoleic acid content. J Food Sci 62, 1083–1086.[CrossRef]
    [Google Scholar]
  45. Suutari, M. & Laakso, S. ( 1992; ). Temperature adaptation in Lactobacillus fermentum: interconversions of oleic, vaccenic and dihydrosterulic acids. J Gen Microbiol 138, 445–450.[CrossRef]
    [Google Scholar]
  46. Veerkamp, J. H. ( 1971; ). Fatty acid composition of Bifidobacterium and Lactobacillus strains. J Bacteriol 108, 861–867.
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.28966-0
Loading
/content/journal/micro/10.1099/mic.0.28966-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error