Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
권호 표지
DOI QR코드

DOI QR Code

Adhesive Properties, Extracellular Protein Production, and Metabolism in the Lactobacillus rhamnosus GG Strain when Grown in the Presence of Mucin

  • Received : 2009.11.05
  • Accepted : 2010.01.04
  • Published : 2010.06.28
Download PDF
⟨ Previous Next ⟩

Abstract

This paper examines the probiotic bacterium Lactobacillus rhamnosus GG, and how it reacts to the presence of mucin in its extracellular milieu. Parameters studied included cell clustering, adhesion to mucin, extracellular protein production, and formation of final metabolites. L. rhamnosus GG was found to grow efficiently in the presence of glucose, N-acetylglucosamine, or mucin (partially purified or purified) as sole carbon sources. However, it was unable to grow using other mucin constituents, such as fucose or glucuronic acid. Mucin induced noticeable changes in all the parameters studied when compared with growth using glucose, including in the formation of cell clusters, which were easily disorganized with trypsin. Mucin increased adhesion of the bacterium, and modulated the production of extracellular proteins. SDS-PAGE revealed that mucin was not degraded during L. rhamnosus GG growth, suggesting that this bacterium is able to partially use the glucidic moiety of glycoprotein. This study goes some way towards developing an understanding of the metabolic and physiological changes that L. rhamnosus GG undergoes within the human gastrointestinal tract.

Keywords

References

  1. Alander, M., R. Satokari, R. Korpela, M. Saxelin, T. Vilpponen-Salmela, T. Mattila-Sandholm, and A. von Wright. 1999. Persistence of colonization of human colonic mucosa by a probiotic strain, Lactobacillus rhamnosus GG, after oral consumption. Appl. Environ. Microbiol. 65: 351-354.
  2. Basu, S., M. Chatterjee, S. Ganguly, and P. K. Chandra. 2007. Efficacy of Lactobacillus rhamnosus GG in acute watery diarrhoea of Indian children: A randomised controlled trial. J. Paediatr. Child Health 43: 837-842. https://doi.org/10.1111/j.1440-1754.2007.01201.x
  3. Boekhorst, J., Q. Helmer, M. Kleerebezem, and R. J. Siezen. 2006. Comparative analysis of proteins with a mucus-binding domain found exclusively in lactic acid bacteria. Microbiology 152: 273-280. https://doi.org/10.1099/mic.0.28415-0
  4. Brockhausen, I. 2006. Mucin-type O-glycans in human colon and breast cancer: Glycodynamics and functions. EMBO Rep. 7: 599-604. https://doi.org/10.1038/sj.embor.7400705
  5. Desai, A. R., N. P. Shah, and I. B. Powell. 2006. Discrimination of dairy industry isolates of the Lactobacillus casei group. J. Dairy Sci. 89: 3345-3351. https://doi.org/10.3168/jds.S0022-0302(06)72371-2
  6. Goldin, B. R., S. L. Gorbach, M. Saxelin, S. Barakat, L. Gualtieri, and S. Salminen. 1992. Survival of Lactobacillus species (strain GG) in human gastrointestinal tract. Dig. Dis. Sci. 37: 121-128. https://doi.org/10.1007/BF01308354
  7. Gosselink, M. P., W. R. Schouten, van L. M. Lieshout, W. C. Hop, J. D. Laman, and J. G. Ruseler-van Embden. 2004. Delay of the first onset of pouchitis by oral intake of the probiotic strain Lactobacillus rhamnosus GG. Dis. Colon Rectum 47: 876-884. https://doi.org/10.1007/s10350-004-0525-z
  8. Jeffery, C. J. 2003. Moonlighting proteins: Old proteins learning new tricks. Trends Genet. 19: 415-417. https://doi.org/10.1016/S0168-9525(03)00167-7
  9. Jonsson, H., E. Strom, and S. Roos. 2001. Addition of mucin to the growth medium triggers mucus-binding activity in different strains of Lactobacillus reuteri in vitro. FEMS Microbiol. Lett. 204: 19-22. https://doi.org/10.1111/j.1574-6968.2001.tb10855.x
  10. Kalliomaki, M., S. Salminen, T. Poussa, H. Arvilommi, and E. Isolauri. 2003. Probiotics and prevention of atopic disease: 4-Year follow-up of a randomised placebo-controlled trial. Lancet 361: 1869-1871. https://doi.org/10.1016/S0140-6736(03)13490-3
  11. Kawada, M., C. C. Chen, A. Arihiro, K. Nagatani, T. Watanabe, and E. Mizoguchi. 2008. Chitinase 3-like-1 enhances bacterial adhesion to colonic epithelial cells through the interaction with bacterial chitin-binding protein. Lab. Invest. 88: 883-895. https://doi.org/10.1038/labinvest.2008.47
  12. Lebeer, S., T. L. Verhoeven, V. M. Perea, J. Vanderleyden, and S. C. De Keersmaecker. 2007. Impact of environmental and genetic factors on biofilm formation by the probiotic strain Lactobacillus rhamnosus GG. Appl. Environ. Microbiol. 73: 6768-6775. https://doi.org/10.1128/AEM.01393-07
  13. Messner, P., G. Allmaier, C. Schaffer, T. Wugeditsch, S. Lortal, H. Konig, R. Niemetz, and M. Dorner. 1997. Biochemistry of S-layers. FEMS Microbiol. Rev. 20: 25-46. https://doi.org/10.1016/S0168-6445(97)00041-7
  14. Pappin, D. J. 2003. Peptide mass fingerprinting using MALDI-TOF mass spectrometry. Methods Mol. Biol. 211: 211-219.
  15. Ruas-Madiedo, P., M. Gueimonde, F. Arigoni, C. G. de los Reyes-Gavilán, and A. Margolles. 2009. Bile affects the synthesis of exopolysaccharides by Bifidobacterium animalis. Appl. Environ. Microbiol. 75: 1204-1207. https://doi.org/10.1128/AEM.00908-08
  16. Ruseler-van Embden, J. G., L. M. van Lieshout, M. J. Gosselink, and P. Marteau. 1995. Inability of Lactobacillus casei strain GG, L. acidophilus, and Bifidobacterium bifidum to degrade intestinal mucus glycoproteins. Scand. J. Gastroenterol 30: 675-680. https://doi.org/10.3109/00365529509096312
  17. Salminen, S. 1996. Functional dairy foods with Lactobacillus strain GG. Nutr. Rev. 54: S99-S101.
  18. Sanchez, B., P. Bressollier, S. Chaignepain, J. M. Schmitter, and M. C. Urdaci. 2009. Identification of surface-associated proteins in the probiotic bacterium Lactobacillus rhamnosus GG. Int. Dairy J. 19: 85-88. https://doi.org/10.1016/j.idairyj.2008.09.005
  19. SAnchez, B., P. Bressollier, and M. C. Urdaci. 2008. Exported proteins in probiotic bacteria: Adhesion to intestinal surfaces, host immunomodulation and molecular cross-talking with the host. Fems Immunol. Med. Microbiol. 54: 1-17. https://doi.org/10.1111/j.1574-695X.2008.00454.x
  20. Sanchez, B., S. Chaignepain, J. M. Schmitter, and M. C. Urdaci. 2009. A method for the identification of proteins secreted by lactic acid bacteria grown in complex media. FEMS Microbiol. Lett. 295: 226-229. https://doi.org/10.1111/j.1574-6968.2009.01599.x
  21. Sanchez, B., M. C. Champomier-Verges, B. Stuer-Lauridsen, P. Ruas-Madiedo, P. Anglade, F. Baraige, et al. 2007. Adaptation and response of Bifidobacterium animalis subsp. lactis to bile: A proteomic and physiological approach. Appl. Environ. Microbiol. 73: 6757-6767. https://doi.org/10.1128/AEM.00637-07
  22. Seth, A., F. Yan, D. B. Polk, and R. K. Rao. 2008. Probiotics ameliorate the hydrogen peroxide-induced epithelial barrier disruption by a PKC- and MAP kinase-dependent mechanism. Am. J. Physiol. Gastrointest. Liver Physiol. 294: G1060-G1069. https://doi.org/10.1152/ajpgi.00202.2007
  23. Tallon, R., S. Arias, P. Bressollier, and M. C. Urdaci. 2007 Strain- and matrix-dependent adhesion of Lactobacillus plantarum is mediated by proteinaceous bacterial compounds. J. Appl. Microbiol. 102: 442-451.
  24. Tuomola, E. M., A. C. Ouwehand, and S. J. Salminen. 1999. The effect of probiotic bacteria on the adhesion of pathogens to human intestinal mucus. FEMS Immunol. Med. Microbiol. 26: 137-142. https://doi.org/10.1111/j.1574-695X.1999.tb01381.x
  25. Velez, M. P., De S. C. Keersmaecker, and J. Vanderleyden. 2007. Adherence factors of Lactobacillus in the human gastrointestinal tract. FEMS Microbiol. Lett. 276: 140-148. https://doi.org/10.1111/j.1574-6968.2007.00908.x
  26. Yan, F., H. Cao, T. L. Cover, R. Whitehead, M. K. Washington, and D. B. Polk. 2007. Soluble proteins produced by probiotic bacteria regulate intestinal epithelial cell survival and growth. Gastroenterology 132: 562-575. https://doi.org/10.1053/j.gastro.2006.11.022
  27. Zhou, J. S., P. K. Gopal, and H. S. Gill. 2001. Potential probiotic lactic acid bacteria Lactobacillus rhamnosus (HN001), Lactobacillus acidophilus (HN017) and Bifidobacterium lactis (HN019) do not degrade gastric mucin in vitro. Int. J. Food Microbiol. 63: 81-90. https://doi.org/10.1016/S0168-1605(00)00398-6

Cited by

  1. An endo-β-N-acetylglucosaminidase from Enterococcus faecalisV583 responsible for the hydrolysis of high-mannose and hybrid-type N-linked glycans vol.325, pp.2, 2011, https://doi.org/10.1111/j.1574-6968.2011.02419.x
  2. Carbohydrate-active enzymes from pigmented Bacilli : a genomic approach to assess carbohydrate utilization and degradation vol.11, pp.None, 2010, https://doi.org/10.1186/1471-2180-11-198
  3. Strain‐Dependent Proliferation in Response to Human Gastric Mucin and Adhesion Properties of Helicobacter pylori are not Affected by Co‐isolated Lactobacillus sp. vol.16, pp.1, 2010, https://doi.org/10.1111/j.1523-5378.2010.00810.x
  4. Lactobacillaceae and Cell Adhesion: Genomic and Functional Screening vol.7, pp.5, 2010, https://doi.org/10.1371/journal.pone.0038034
  5. Evaluation of Bacillus subtilis strains as probiotics and their potential as a food ingredient vol.3, pp.2, 2010, https://doi.org/10.3920/bm2012.0002
  6. In vitro evaluation of the mucin‐adhesion ability and probiotic potential of Lactobacillus mucosae LM1 vol.117, pp.2, 2010, https://doi.org/10.1111/jam.12539
  7. An l-Fucose Operon in the Probiotic Lactobacillus rhamnosus GG Is Involved in Adaptation to Gastrointestinal Conditions vol.81, pp.11, 2015, https://doi.org/10.1128/aem.00260-15
  8. The Variable Regions of Lactobacillus rhamnosus Genomes Reveal the Dynamic Evolution of Metabolic and Host-Adaptation Repertoires vol.8, pp.6, 2016, https://doi.org/10.1093/gbe/evw123
  9. Draft genome sequence of Lactobacillus plantarum strains E2C2 and E2C5 isolated from human stool culture vol.12, pp.None, 2010, https://doi.org/10.1186/s40793-017-0222-x
  10. Utilization of Host-Derived Glycans by Intestinal Lactobacillus and Bifidobacterium Species vol.9, pp.None, 2018, https://doi.org/10.3389/fmicb.2018.01917
  11. Characterization and probiotic properties of Lactobacilli from human breast milk vol.9, pp.11, 2010, https://doi.org/10.1007/s13205-019-1926-y
  12. Precision modification of the human gut microbiota targeting surface-associated proteins vol.11, pp.1, 2010, https://doi.org/10.1038/s41598-020-80187-3