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Molecular Characterization of Bile Salt Hydrolase from Bifidobacterium animalis subsp. lactis Bi30

  • Jarocki, Piotr (Department of Biotechnology, Human Nutrition and Food Commodities, University of Life Sciences in Lublin)
  • Received : 2011.03.16
  • Accepted : 2011.05.11
  • Published : 2011.08.28

Abstract

The present work describes the identification, purification, and characterization of bile salt hydrolase (BSH) from Bifidobacterium animalis subsp. lactis. The enzyme was purified to electrophoretic homogeneity by hydrophobic chromatography, ion-exchange chromatography and ultrafiltration. SDS-PAGE analysis of putative BSH and gel filtration revealed that the analyzed protein is presumably a tetramer composed of four monomers each of about 35 kDa. The purified enzyme was analyzed by liquid chromatography coupled to LTQ FT ICR mass spectrometry and unambiguously identified as a bile salt hydrolase from B. animalis. The isoelectric point of the studied protein was estimated to be around pH 4.9. The pH optimum of the purified BSH is between 4.7 to 6.5, and the temperature optimum is around 50oC. The BSH of B. animalis could deconjugate all tested bile salts, with clear preference for glycine-conjugated bile salts over taurine-conjugated forms. Genetic analysis of the bsh showed high similarity to the previously sequenced bsh gene from B. animalis and confirmed the usefulness of bile salt hydrolase as a genetic marker for B. animalis identification.

Keywords

References

  1. Arunachalam, K. D. 1999. Role of bifidobacteria in nutrition, medicine and technology. Nutr. Res. 19: 1559-1597. https://doi.org/10.1016/S0271-5317(99)00112-8
  2. Begley, M., C. Hill, and C. G. Gahan. 2006. Bile salt hydrolase activity in probiotics. Appl. Environ. Microbiol. 72: 1729-1738. https://doi.org/10.1128/AEM.72.3.1729-1738.2006
  3. Begley, M., C. Hill, and C. G. Gahan. 2006. Bile salt hydrolase activity in probiotics. Appl. Environ. Microbiol. 72: 1729-1738. https://doi.org/10.1128/AEM.72.3.1729-1738.2006
  4. Berr, F., G. A. Kullak-Ublick, G. Paumgartner, W. Munzing, and P. B. Hylemon. 1996. 7 Alpha-dehydroxylating bacteria enhance deoxycholic acid input and cholesterol saturation of bile in patients with gallstones. Gastroenterology 111: 1611-1620. https://doi.org/10.1016/S0016-5085(96)70024-0
  5. Bielecka, M., E. Biedrzycka, and A. Majkowska. 2002. Selection of probiotics and prebiotics for synbiotics and confirmation of their in vivo effectiveness. Food Res. Int. 35: 125-131. https://doi.org/10.1016/S0963-9969(01)00173-9
  6. Chiang, B. L., Y. H. Sheih, L. H. Wang, C. K. Liao, and H. S. Gill. 2000. Enhancing immunity by dietary consumption of a probiotic lactic acid bacterium (Bifidobacterium lactis HN019): Optimization and definition of cellular immune responses. Eur. J. Clin. Nutr. 54: 849-855. https://doi.org/10.1038/sj.ejcn.1601093
  7. Dashkevicz, M. P. and S. D. Feighner. 1989. Development of a differential medium for bile salt hydrolase-active Lactobacillus spp. Appl. Environ. Microbiol. 55: 11-16.
  8. Du Toit, M., C. M. Franz, L. M. Dicks, U. Schillinger, P. Harberer, B. Warlies, F. Ahrens, and W. H. Holzapfel. 1998. Characterization and selection of probiotic lactobacilli for a preliminary mini-pig feeding trial and their effect on serum cholesterol levels, feces pH, and feces moisture content. Int. J. Food Microbiol. 40: 93-104. https://doi.org/10.1016/S0168-1605(98)00024-5
  9. Felis, G. E. and F. Dellaglio. 2007. Taxonomy of lactobacilli and bifidobacteria. Curr. Issues Intest. Microbiol. 8: 44-61.
  10. Grill, J. P., C. Cayuela, J. M. Antoine, and F. Schneider. 2000. Isolation and characterization of a Lactobacillus amylovorus mutant depleted in conjugated bile salt hydrolase activity: Relation between activity and bile salt resistance. J. Appl. Microbiol. 89: 553-563. https://doi.org/10.1046/j.1365-2672.2000.01147.x
  11. Grill, J. P., F. Schneider, J. Crociani, and J. Ballongue. 1995. Purification and characterization of conjugated bile salt hydrolase from Bifidobacterium longum BB536. Appl. Environ. Microbiol. 61: 2577-2582.
  12. Ha, C. G., J. K. Cho, Y. G. Chai, Y. A. Ha, and S. H. Shin. 2006. Purification and characterization of bile salt hydrolase from Lactobacillus plantarum CK 102. J. Microbiol. Biotechnol. 16: 1047-1052.
  13. Jarocki, P., M. Podlesny, A. Wasko, A. Siuda, and Z. Targonski. 2010. Differentiation of 3 Lactobacillus rhamnosus strains: E/N, Oxy and Pen by SDS-PAGE and two-dimensional electrophoresis of surface-associated proteins. J. Microbiol. Biotechnol. 20: 558-562.
  14. Jiang, T., A. Mustapha, and D. A. Savaiano. 1996. Improvement of lactose digestion in humans by ingestion of unfermented milk containing Bifidobacterium longum. J. Dairy Sci. 79: 750-757. https://doi.org/10.3168/jds.S0022-0302(96)76422-6
  15. Johnson, J. L. 1994. Similarity analysis of rRNAs, pp. 683- 700. In P. Gerhardt, W. A. Wood, N. R. Krieg, and R. Murray (eds.). Methods for General and Molecular Bacteriology. American Society for Microbiology, Washington, DC, USA.
  16. Kim, G. B., S. H. Yi, and B. Lee. 2004. Purification and characterization of three different types of bile salt hydrolase from Bifidobacterium strains. J. Dairy Sci. 87: 258-266. https://doi.org/10.3168/jds.S0022-0302(04)73164-1
  17. Kim, G. B., C. M. Miyamoto, E. A. Meighen, and B. H. Lee. 2004. Cloning and characterization of the bile salt hydrolase genes (bsh) from Bifidobacterium bifidum strains. Appl. Environ. Microbiol. 70: 5603-5612. https://doi.org/10.1128/AEM.70.9.5603-5612.2004
  18. Kim, G. B. and B. H. Lee. 2005. Biochemical and molecular insights into bile salt hydrolase in the gastrointestinal microflora. Asian-Aust. J. Animal Sci. 18: 1505-1512. https://doi.org/10.5713/ajas.2005.1505
  19. Kim, G. B. and B. H. Lee. 2008. Genetic analysis of a bile salt hydrolase in Bifidobacterium animalis subsp. lactis KL61. J. Appl. Microbiol. 105: 778-790. https://doi.org/10.1111/j.1365-2672.2008.03825.x
  20. Kim, J. E., J. Y. Kim, K. W. Lee, and H. J. Lee. 2007. Cancer chemopreventive effects of lactic acid bacteria. J. Microbiol. Biotechnol. 17: 1227-1235.
  21. Leahy, S. C., D. G. Higgins, G. F. Fitzgerald, and D. van Sinderen. 2005. Getting better with bifidobacteria. J. Appl. Microbiol. 98: 1303-1315. https://doi.org/10.1111/j.1365-2672.2005.02600.x
  22. Liong, M. T. and N. P. Shah. 2005. Bile salt deconjugation and BSH activity of five bifidobacterial strains and their cholesterol co-precipitating properties. Food Res. Int. 38: 135-142. https://doi.org/10.1016/j.foodres.2004.08.003
  23. Liong, M. T. and N. P. Shah. 2005. Bile salt deconjugation ability, bile salt hydrolase activity and cholesterol co-precipitation ability of lactobacilli strains. Int. Dairy J. 15: 391-398. https://doi.org/10.1016/j.idairyj.2004.08.007
  24. Lundeen, S. G. and D. C. Savage. 1990. Characterization and purification of bile salt hydrolase from Lactobacillus sp. strain 100-100. J. Bacteriol. 172: 4171-4177. https://doi.org/10.1128/jb.172.8.4171-4177.1990
  25. Nagengast, F. M., M. J. Grobben, and I. P. van Munster. 1995. Role of bile acids in colorectal carcinogenesis. Eur. J. Cancer 31: 1067-1070. https://doi.org/10.1016/0959-8049(95)00216-6
  26. Noriega, L., I. Cuevas, A. Margolles, and C. G. de los Reyes- Gavilan. 2006. Deconjugation and bile salts hydrolase activity by Bifidobacterium strains with acquired resistance to bile. Int. Dairy. J. 16: 850-855. https://doi.org/10.1016/j.idairyj.2005.09.008
  27. Patel, A. K., R. R. Singhania, A. Pandey, and S. B. Chincholkar. 2010. Probiotic bile salt hydrolase: Current developments and perspectives. Appl. Biochem. Biotechnol. 162: 166-180. https://doi.org/10.1007/s12010-009-8738-1
  28. Picard, C., J. Fioramonti, A. Francois, T. Robinson, F. Neant, and C. Matuchansky. 2005. Review article: Bifidobacteria as probiotic agents - physiological effects and clinical benefits. Aliment. Pharmacol. Ther. 22: 495-512. https://doi.org/10.1111/j.1365-2036.2005.02615.x
  29. Pereira, D. I. and G. R. Gibson. 2002. Effects of consumption of probiotics and prebiotics on serum lipid levels in humans. Crit. Rev. Biochem. Mol. Biol. 37: 259-281. https://doi.org/10.1080/10409230290771519
  30. Tanaka, H., T. Doesburg, T. Iwasaki, and I. Mierau. 1999. Screening of lactic acid bacteria for bile salt hydrolase sactivity. J. Dairy Sci. 82: 2530-2535. https://doi.org/10.3168/jds.S0022-0302(99)75506-2
  31. Tanaka, H., H. Hashiba, J. Kok, and I. Mierau. 2000. Bile salt hydrolase of Bifidobacterium longum - biochemical and genetic characterization. Appl. Environ. Microbiol. 66: 2502-2512. https://doi.org/10.1128/AEM.66.6.2502-2512.2000
  32. Taranto, M. P., M. Medici, G. Perdigon, A. P. Ruiz Holgado, and G. F. Valdez. 1998. Evidence for hypocholesterolemic effect of Lactobacillus reuteri in hypercholesterolemic mice. J. Dairy Sci. 81: 2336-2340. https://doi.org/10.3168/jds.S0022-0302(98)70123-7
  33. Tlaskalova-Hogenova, H., R. Stepankova, T. Hudcovic, L. Tuckova, B. Cukrowska, R. Lodinova-Zadnikova, et al. 2004. Commensal bacteria (normal microflora), mucosal immunity and chronic inflammatory and autoimmune diseases. Immunol. Lett. 93: 97-108. https://doi.org/10.1016/j.imlet.2004.02.005
  34. Ventura, M., D. van Sinderen, G. F. Fitzgerald, and R. Zink. 2004. Insights into the taxonomy, genetics and physiology of bifidobacteria. Antonie Van Leeuwenhoek 86: 205-223. https://doi.org/10.1023/B:ANTO.0000047930.11029.ec

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