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Assessment of Bile Salt Effects on S-Layer Production, slp Gene Expression and, Some Physicochemical Properties of Lactobacillus acidophilus ATCC 4356

  • Khaleghi, M. (Department of Biology, Faculty of Sciences, Shahid Bahonar University of Kerman) ;
  • Kermanshahi, R. Kasra (Department of Biology, Faculty of Sciences, University of Isfahan) ;
  • Yaghoobi, M.M. (Department of Biotechnology, Research Institute of Environmental Sciences, International Center for Science, High Technology and Environmental Sciences) ;
  • Zarkesh-Esfahani, S.H. (Department of Biology, Faculty of Sciences, University of Isfahan) ;
  • Baghizadeh, A. (Department of Biotechnology, Research Institute of Environmental Sciences, International Center for Science, High Technology and Environmental Sciences)
  • Received : 2009.06.21
  • Accepted : 2009.12.06
  • Published : 2010.04.28

Abstract

In many conditions, bacterial surface properties are changed as a result of variation in the growth medium and conditions. This study examined the influence of bile salt concentrations (0-0.1%) on colony morphotype, hydrophobicity, $H_2O_2$ concentration, S-layer protein production, and slpA gene expression in Lactobacillus acidophilus ATCC 4356. It was observed that two types of colonies (R and S) were in the control group and the stress condition. When the bile level increased in the medium, the amount of S type was more than the R type. A stepwise increment in the bile concentration resulted in a stepwise decline in the maximum growth rate. The results showed that hydrophobicity was increased in 0.01%-0.02% bile, but it was decreased in 0.1% bile. Treatment by bile (0.01%-0.1%) profoundly decreased $H_2O_2$ formation. S-Layer protein and slpA gene expression were also altered by the stress condition. S-Protein expression was increased in the stress condition. The slpA gene expression increased in 0.01%-0.05% bile and it decreased in 0.1% bile. However, we found that different bile salt concentrations influenced the morphology and some surface properties of L. acidophilus ATCC 4356. These changes were very different in the 0.1% bile. It appears that the bacteria respond abruptly to 0.1% bile.

Keywords

References

  1. Altermann, E., B. L. Buck, R. Cano, and T. R. Klaenhammer. 2004. Identification and phenotypic characterization of the celldivision protein CdpA. Gene 342: 189-197. https://doi.org/10.1016/j.gene.2004.08.004
  2. Avall-Jaaskelainen, S. and A. Palva. 2005. Lactobacillus surface layers and their applications. FEMS Microbiol. Rev. 29: 511-529.
  3. Barnard, J. P. and M. W. Stinson. 1999. Influence of environmental conditions on hydrogen peroxide formation by Streptococcus gordonii. Infect. Immun. 67: 6558-6564.
  4. Ben-Jacob, E., I. Cohen, I. Golding, D. L. Gutnick, M. Tcherpakov, D. Helbing, and I. G. Ron. 2000. Bacterial cooperative organization under antibiotic stress. Physica 282 A: 247-282.
  5. Boot, H. J. and P. H. Pouwels. 1996. Expression, secretion and antigenic variation of bacterial S-layer proteins. Mol. Microbiol. 21: 1117-1123. https://doi.org/10.1046/j.1365-2958.1996.711442.x
  6. Boot, H. J., C. P. A. M. Kolen, F. J. Andreadaki, R. J. Leer, and P. H. Pouwels. 1996. The Lactobacillus acidophilus S-layer protein gene expression site comprises two consensus promoter sequences, one of which directs transcription of stable mRNA. J. Bacteriol. 178: 5388-5394.
  7. Boot, H. J., C. P. A. M. Kolen, J. M. van Noort, and P. H. Pouwels. 1993. S-Layer protein of Lactobacillus acidophilus ATCC 4356: Purification, expression in Escherichia coli, and nucleotide sequence of the corresponding genet J. Bacteriol. 175: 6089-6096.
  8. Boot, H. J., C. P. A. M. Kolen, and P. H. Pouwels. 1995. Identification, cloning, and nucleotide sequence of a silent S-layer protein gene of Lactobacillus acidophilus ATCC 4356 which has extensive similarity with the S-layer protein gene of this species. J. Bacteriol. 177: 7222-7230.
  9. Bradford, M. M. 1976. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of dye-binding. Anal. Biochem.72: 248-254. https://doi.org/10.1016/0003-2697(76)90527-3
  10. Bron, P. A., M. Marco, S. M. Hoffer, E. V. Mullekom, W. M. de Vos, and M. Kleerebezem. 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. J. Bacteriol. 186: 7829-7835. https://doi.org/10.1128/JB.186.23.7829-7835.2004
  11. De Angelis, M. and M. Gobbetti. 2004. Environmental stress responses in Lactobacillus: A review. Proteomics 4: 106-122. https://doi.org/10.1002/pmic.200300497
  12. De Roos, N. M. and M. B. Katan. 2000. Effects of probiotic bacteria on diarrhea, lipid metabolism, and carcinogenesis: A review of papers published between 1988 and 1998. Am. J. Clin. Nutr. 71: 405-411.
  13. Eschenbach, D. A., P. R. Davick, B. L. Williams, S. J. Klebanoff, K. Young-Smith, C. M. Critchlow, and K. K. Holmes. 1989. Prevalence of hydrogen peroxide-producing Lactobacillus species in normal women and women with bacterial vaginosis. J. Clin. Microbiol. 27: 251-256.
  14. Fitzsimons, N. A., A. D. L. Akermans, W. M. de Vos, and E. E. Vaughan. 2003. Bacterial gene expression detected in human faeces by reverse transcription-PCR. J. Microbiol. Methods 55: 133-140. https://doi.org/10.1016/S0167-7012(03)00121-0
  15. Frece, J., B. Kos, I. K. Svetec, Z. Zgaga, V. Mrsa, and J. Suskovic. 2005. Importance of S-layer proteins in probiotc activity of Lactobacillus acidophilus M92. J. Appl. Microbiol. 98: 285-292. https://doi.org/10.1111/j.1365-2672.2004.02473.x
  16. Goderska, K. and Z. Czarnecki. 2007. Characterization of selected strain from Lactobacillus acidophilus and Bifidobacterium bifidum. Afric. J. Microbiol. Res. 1: 65-78.
  17. Jagnow, J. and S. Clegg. 2003. Klebsiella pneumoniae MrkD-mediated biofilm formation on extracellular matrix- and collagen-coated surfaces. Microbiology 149: 2397-2405. https://doi.org/10.1099/mic.0.26434-0
  18. Jakava-Viljanen, M., S. Avall-Jaaskelainen, P. Messner, U. B. Sleytr, and A. Palva1. 2002. Isolation of three new surface layer protein genes (slp) from Lactobacillus brevis ATCC 14869 and characterization of the change in their expression under aerated and anaerobic conditions. J. Bacteriol. 184: 6786-6795. https://doi.org/10.1128/JB.184.24.6786-6795.2002
  19. Jan, G., P. Leverrier, V. Pichereau, and P. Boyaval. 2001. Changes in protein synthesis and morphology during acid adaptation of Propionibacterium freudenreichii. Appl. Environ. Microbiol. 67: 2029-2036. https://doi.org/10.1128/AEM.67.5.2029-2036.2001
  20. Kim, W. S., L. Perl, J. H. Park, J. E. Tandianus, and N. W. Dunn. 2001. Assessment of stress response of the probiotic Lactobacillus acidophilus. Curr. Microbiol. 43: 346-350. https://doi.org/10.1007/s002840010314
  21. Kirisits, M. J., L. Prost, M. Starkey, and M. R. Parsek. 2005. Characterization of colony morphology variants isolated from Pseudomonas aeruginosa biofilms. Appl. Environ. Microbiol. 71: 4809-4821. https://doi.org/10.1128/AEM.71.8.4809-4821.2005
  22. Klaenhammer, T. R. and E. G. Kleeman. 1981. Growth characteristics, bile sensitivity and freeze damage in colonial variants of Lactobacillus acidophilus. Appl. Environ. Microbiol. 41: 1461-1467.
  23. Kos, B., J. Suskovic, S. Vukovic, M. Simpraga, J. Frece. and S. Matosic. 2003. Adhesion and aggregation ability of probiotic strain Lactobacillus acidophilus M92. J. Appl. Microbiol. 94: 981-987. https://doi.org/10.1046/j.1365-2672.2003.01915.x
  24. Kosin, B. and S. K. Rakshit. 2006. Microbial and processing criteria for production of probiotics: A review. Food Technol. Biotechnol. 44: 371-379.
  25. Kristoffersen, S. M., S. Ravnum, N. J. Tourasse, O. A. Okstad, A. B. Kolsto, and W. Davies. 2007. Low concentrations of bile salts induce stress responses and reduce motility in Bacillus cereus ATCC 14570. J. Bacteriol. 189: 5302-5313. https://doi.org/10.1128/JB.00239-07
  26. Kubota, H., S. Senda, N. Nomura, H. Tokuda, and H. Uchiyama. 2008. Biofilm formation by lactic acid bacteria and resistance to environmental stress. J. Biosci. Bioeng. 106: 381-386. https://doi.org/10.1263/jbb.106.381
  27. Lorca, G. L. and G. F. de Valdez. 2001. A low-pH-inducible, stationary-phase acid tolerance response in Lactobacillus acidophilus CRL 639. Curr. Microbiol. 42: 21-25. https://doi.org/10.1007/s002840010172
  28. Marty-Teysset, C., F. De La Torre, and J. R. Garel. 2000. Increased production of hydrogen peroxide by Lactobacillus delbrueckii subsp. bulgaricus upon aeration: Involvement of an NADH oxidase in oxidative stress. Appl. Environ. Microbiol. 66: 262-267. https://doi.org/10.1128/AEM.66.1.262-267.2000
  29. Ocana, V. S., E. Bru, A. A. P. de Ruiz Holgado, and M. E. Nader-Macias. 1999. Surface characteristics of lactobacilli isolated from human vagina. J. Gen. Appl. Microbiol. 45: 203-212. https://doi.org/10.2323/jgam.45.203
  30. Ouwehand, A. C., A. Batsman, and S. Salminen. 2003. Probiotics for the skin: A new area of potential application. Lett. Appl. Microbiol. 36: 327-331. https://doi.org/10.1046/j.1472-765X.2003.01319.x
  31. Rabe, L. K. and S. L. Hillier. 2003. Optimization of media for detection of hydrogen peroxide production by Lactobacillus species. J. Clin. Microbiol. 41: 3260-3264. https://doi.org/10.1128/JCM.41.7.3260-3264.2003
  32. Sanders, M. E. and T. R. Klaenhammer. 2001. Invited review: The scientific basis of Lactobacillus acidophilus NCFM functionality as a probiotic. J. Dairy Sci. 84: 319-331. https://doi.org/10.3168/jds.S0022-0302(01)74481-5
  33. Sanders, J. W., G. Venema, and J. Kok. 1999. Environmental stress responses in Lactococcus lactis. FEMS Microbiol. Rev. 23: 483-501. https://doi.org/10.1111/j.1574-6976.1999.tb00409.x
  34. Sara, M. and U. B. Sleytr. 2000. S-Layer proteins. J. Bacteriol. 182: 859-868. https://doi.org/10.1128/JB.182.4.859-868.2000
  35. Schar-Zammaretti, P., M-L. Dillmann, N. D'Amico, M. Affolter, and J. Ubbink. 2005. Influence of fermentation medium composition on physicochemical surface properties of Lactobacillus acidophilus. Appl. Environ. Microbiol. 71: 8165-8173. https://doi.org/10.1128/AEM.71.12.8165-8173.2005
  36. Smit, E., F. Oling, R. Demel, B. Martiez, and P. H. Pouwels. 2001. The S-layer protein of Lactobacillus acidophilus ATCC 4356: Identification and characterization of domains responsible for S-protein assembly and cell wall binding. J. Mol. Biol. 305: 245-257. https://doi.org/10.1006/jmbi.2000.4258
  37. Sullivan, A. and C. E. Nord. 2002. Probiotics in human infections. J. Antimicrob. Chemother. 50: 625-627. https://doi.org/10.1093/jac/dkf194
  38. Trotha, R., T. H. W. Konig, and B. Konig. 2001. Rapid ribosequencing - an effective diagnostic tool for detecting microbial infection. Infection 29: 12-16. https://doi.org/10.1007/s15010-001-0064-7
  39. Ventura, M., I. Jankovic, D. C. Walker, R. D. Pridmore, and R. Zink. 2002. Identification and characterization of novel surface proteins in Lactobacillus johnsonii and Lactobacillus gasseri. Appl. Environ. Microbiol. 68: 6172-6181. https://doi.org/10.1128/AEM.68.12.6172-6181.2002
  40. Wankano, J. Y., S. Maenosono, A. Komoto, N. Eiha, and Y. Yamaguchi. 2003. Self-organized pattern formation of a bacteria colony modeled by a reaction diffusion system and nucleation theory. Phys. Rev. Lett. 90: 258102-258102.4. https://doi.org/10.1103/PhysRevLett.90.258102
  41. Welin, J., J. C. Wilkins, D. Beighton, and G. Svensater. 2004. Protein expression by Streptococcus mutans during initial stage of biofilm formation. J. Appl. Microbiol. 70: 3736-3741. https://doi.org/10.1128/AEM.70.6.3736-3741.2004

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