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Research article

Food Microbiology and Biotechnology

Proteomic Analysis of Proteins Increased or Reduced by Ethanol of Lactobacillus plantarum ST4 Isolated from Makgeolli, Traditional Korean Rice Wine

Seung Gyu Lee 1, Kang Wook Lee 1, Tae Heung Park 1, Ji Yeong Park 1, Nam Soo Han 2 and Jeong Hwan Kim 1, 3*

1Division of Applied Life Science (BK21), Graduate school, Gyeongsang National University, Jinju 660-701, Korea, 2Department of Food Science and Technology, BK21 Education and Research Center for Advanced Bio-Agriculture Technology, Chungbuk National University, Cheongju 361-763, Korea, 3Institute of Agriculture and Life Science, Gyeongsang National University, Jinju 660-701, Korea

Received: September 7, 2011; Accepted: November 28, 2011

J. Microbiol. Biotechnol. 2012; 22(4): 516-525

Published April 28, 2012 https://doi.org/10.4014/jmb.1109.09012

Copyright © The Korean Society for Microbiology and Biotechnology.

Abstract

LAB were isolated from makgeolli locally produced around Jinju, Gyeongnam, S. Korea during spring of 2011. Randomly selected 11 isolates from MRS agar plates were identified first by API CHL 50 kits and then 16S rRNA gene sequencing. All 11 isolates were identified as Lactobacillus plantarum. Among them, ST4 grew in MRS broth with ethanol up to 10%, showing the highest alcohol resistance. L. plantarum ST4 was moderately resistant against acid and bile salts. When cellular proteins of L. plantarum ST4 under ethanol stress were analyzed by two-dimensional gel electrophoresis (2DE), the intensities of 6 spots increased, whereas 22 spots decreased at least 2-fold. Those 28 spots were identified by peptide mass fingerprinting (PMF). FusA2 (elongation factor G) increased 18.8-fold (6% ethanol) compared with control. Other proteins were AtpD (ATP synthase subunit beta), DnaK, GroEL, Tuf (elongation factor Tu), and Npr2 (NADH peroxidase), respectively. Among the 22 proteins decreased in intensities, lactate dehydrogenases (LdhD and LdhL1) were included.

Keywords

Makgeolli, LAB, Lactobacillus plantarum, ethanol stress

References

  1. Arnau, J., K. I. Sorensen, K. Appel, F. K. Vogensen, and K. Hammer. 1996. Analysis of heat shock gene expression in Lactococcus lactis MG1363. Microbiology 142: 1685-1691.
    Pubmed CrossRef
  2. Broadbent, J. R., R. L. Larsen, V. Deibel, and J. L. Steele. 2010. Physiological and transcriptional response of Lactobacillus casei ATCC 334 to acid stress. J. Bacteriol. 192: 2445-2458.
    Pubmed PMC CrossRef
  3. Bron, P. A., D. Molenaar, W. M. de Vos, and M. Kleerebezem. 2006. DNA micro-array based identification of bile-responsive genes in Lactobacillus plantarum. J. Appl. Microbiol. 100: 728-738.
    Pubmed CrossRef
  4. Caldas, T. D., A. El. Yaagoubi, and G. Richarme. 1998. Chaperone properties of bacterial elongation factor EF-Tu. J. Biol. Chem. 273: 11478-11482.
    Pubmed CrossRef
  5. Cho, M. J., B. S. Jeon, J. W. Park, T. S. Jung, J. Y. Song, W. K. Lee, et al. 2002. Identifying the major proteome components of Helicobacter pylori strain 26695. Electrophoresis 23: 1161-1173.
    CrossRef
  6. De Angelis, M., R. Di Cagno, C. Huet, C. Crecchio, P. F. Fox, and M. Gobbetti. 2004. Heat shock response in Lactobacillus plantarum. Appl. Environ. Microbiol. 70: 1336-1346.
    Pubmed PMC CrossRef
  7. Desmond, C., G. F. Fitzgerald, C. Stanton, and R. P. Ross. 2004. Improved stress tolerance of GroESL-overproducing Lactococcus lactis and probiotic Lactobacillus paracasei NFBC 338. Appl. Environ. Microbiol. 70: 5929-5936.
    Pubmed PMC CrossRef
  8. Ding, W. K. and N. P. Shah. 2007. Acid, bile, and heat tolerance of free and microencapsulated probiotic bacteria. J. Food Sci. 72: M446-M450.
    Pubmed CrossRef
  9. G-Alegria, E., I. López, J. I. Ruiz, J. Sáenz, E. Fernández, M. Zarazaga, M. Dizy, C. Torres, and F. Ruiz-Larrea. 2004. High tolerance of wild Lactobacillus plantarum and Oenococcus oeni strains to lyophilization and stress environmental conditions of acid pH and ethanol. FEMS Microbiol. Lett. 230: 53-61.
    CrossRef
  10. Hong, Y., Y. B. Kim, S. O. Park, and E. H. Choi. 1997. Microflora and physicochemical characteristics of nuruk and main mashes during fermentation of a traditional Andong-soju. Food Sci. Biotechnol. 6: 297-303.
  11. Jin, J., S. Y. Kim, Q. Jin, H. J. Eom, and N. S. Han. 2008. Diversity analysis of lactic acid bacteria in takju, Korean rice wine. J. Microbiol. Biotechnol. 18: 1678-1682.
    Pubmed
  12. Kim, H. R., Y. H. Kwon, S. J. Jo, J.-H. Kim, and B.-H. Ahn. 2009. Characterization and volatile flavor components in glutinous rice wines prepared with different yeasts of nuruks. J. Food Sci. Technol. 41: 296-301 (in Korean)
  13. Kim, H. R., J.-H. Kim, D.-H. Bae, and B.-H. Ahn. 2010. Characterization of yakju brewed from glutinous rice and wildtype yeast strains isolated from nuruks. J. Microbiol. Biotechnol. 20: 1702-1710.
    Pubmed
  14. Kim, H. S., J. S. Hyun, J. Kim, H. P. Ha, and T. S. Yu. 1998. Enzymological characteristics and identification of useful fungi isolated from traditional Korean nuruk. Korean J. Appl. Microbiol. Biotechnol. 26: 456-464 (in Korean)
  15. 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.
    Pubmed CrossRef
  16. Koebmann, B. J., D. Nilsson, O. P. Kuipers, and P. R. Jensen. 2000. The membrane-bound H(+)-ATPase complex is essential for growth of Lactococcus lactis. J. Bacteriol. 182: 4738-4743.
    Pubmed PMC CrossRef
  17. Lee, J. W. and J. Y. Shim. 2010. Quality characteristics of makgeolli during freezing storage. Food Eng. Prog. 14: 328334 (in Korean).
  18. Lee, Y. K. and S. Salminen. 1995. The coming of age of probiotics. Trends Food Sci. Technol. 6: 241-245.
    Pubmed CrossRef
  19. Le Marrec, C., E. Bon, and A. Lonvaud-Funel. 2007. Tolerance to high osmolality of the lactic acid bacterium Oenococcus oeni and identification of potential osmoprotectants. Int. J. Food Microbiol. 15: 335-342.
    Pubmed CrossRef
  20. Liu, S.-Q. 2002. A review malolactic fermentation in wine beyond deacidification. J. Appl. Microbiol. 92: 589-602.
    Pubmed CrossRef
  21. O’Connell, K. L. and J. T. Stults. 1997. Identification of mouse liver proteins on two-dimensional electrophoresis gel by matrixassisted laser desorption/ionization mass spectrometry of in situ enzymatic digests. Electrophoresis 18: 349-359.
    Pubmed CrossRef
  22. Park, J. C., M. Ok, J. Y. Cha, and Y. S. Cho. 2003. Isolation and identification of the high-glutathione producing Saccharomyces cerevisiae FF-8 from Korean traditional rice wine and optimal producing conditions. J. Korean Soc. Agric. Chem. Biotech. 46:348-352 (in Korean)
  23. Pieterse, B., R. J. Leer, F. H. Schuren, and M. J. van der Werf. 2005. Unravelling the multiple effects of lactic acid stress on Lactobacillus plantarum by transcription profiling. Microbiology 151: 3881-3894.
    Pubmed CrossRef
  24. Plumed-Ferrer, C., K. M. Koistinen, T. L. Tolonen, S. J. Lehesranta, S. O. Karenlampi, E. M. Kimattila, V. Joutsjoki, V. Virtanen, and A. von Wright. 2008. Comparative study of sugar fermentation and protein expression patterns of two Lactobacillus plantarum strains grown in three different media. Appl. Environ. Microbiol. 74: 5349-5358.
    Pubmed PMC CrossRef
  25. Salotra, P., D. K. Singh, K. P. Seal, N. Krishna, H. Jaffe, and R. Bhatnagar. 1995. Expression of DnaK and GroEL homologs in Leuconostoc mesenteroides in response to heat shock, cold shock or chemical stress. FEMS Microbiol Lett. 15: 57-62.
    Pubmed CrossRef
  26. Sanchez, B., M. C. Champomier-Verges, P. Anglade, F. Baraige, C. G. D. Reyes-Gavilan, A. Margolles, and M. Zagorec. 2005. Proteomic analysis of global changes in protein expression during bile salt exposure of Bifidobacterium longum NCIMB 8809. J. Bacteriol. 187: 5799-5808.
    Pubmed PMC CrossRef
  27. Seo, D. H., J. H. Jung, H. Y. Kim, Y. R. Kim, S. J. Ha, Y. C. Kim, and C. S. Park. 2007. Identification of lactic acid bacteria involved in traditional Korean rice wine fermentation. Food Sci. Biotechnol. 16: 994-998.
  28. Seo, M. J. and S. R. Ryu. 2002. Screening and characteristics of ethanol tolerant strain Saccharomyces cerevisiae SE211. Korean J. Appl. Microbiol. Biotechnol. 30: 216-222 (in Korean)
  29. Shin, Y. D. and D. H. Cho. 1970. A study on the microflora changes during takju brewing. Kor. J. Microbiol. 8: 53-64 (in Korean)
  30. Sico, M. A., M. G. Bonomo, A. D’Adamo, S. Bochicchio, and G. Salzano. 2009. Fingerprinting analysis of Oenococcus oeni strains under stress conditions. FEMS Microbiol. Lett. 296: 11-17.
    Pubmed CrossRef
  31. Stark, H., V. M. Rodnina, H. J. Wieden, F. Zemlin, W. Wintermeyer, and M. van Heel. 2002. Ribosome interactions of aminoacyl-tRNA and elongation factor Tu in the codonrecognition complex. Nat. Struct. Biol. 9: 849-854.
    Pubmed
  32. Wickner, S., J. Hoskins, and K. McKenney. 1991. Function of DnaJ and DnaK as chaperones in origin-specific DNA binding by RepA. Nature 350: 165-167.
    Pubmed CrossRef
  33. Wilkins, J. C., K. A. Homer, and D. Beighton. 2002. Analysis of Streptococcus mutans proteins modulated by culture under acidic conditions. Appl. Environ. Microbiol. 68: 2382-2390.
    Pubmed PMC CrossRef

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Article

Research article

J. Microbiol. Biotechnol. 2012; 22(4): 516-525

Published online April 28, 2012 https://doi.org/10.4014/jmb.1109.09012

Copyright © The Korean Society for Microbiology and Biotechnology.

Proteomic Analysis of Proteins Increased or Reduced by Ethanol of Lactobacillus plantarum ST4 Isolated from Makgeolli, Traditional Korean Rice Wine

Seung Gyu Lee 1, Kang Wook Lee 1, Tae Heung Park 1, Ji Yeong Park 1, Nam Soo Han 2 and Jeong Hwan Kim 1, 3*

1Division of Applied Life Science (BK21), Graduate school, Gyeongsang National University, Jinju 660-701, Korea, 2Department of Food Science and Technology, BK21 Education and Research Center for Advanced Bio-Agriculture Technology, Chungbuk National University, Cheongju 361-763, Korea, 3Institute of Agriculture and Life Science, Gyeongsang National University, Jinju 660-701, Korea

Received: September 7, 2011; Accepted: November 28, 2011

Abstract

LAB were isolated from makgeolli locally produced
around Jinju, Gyeongnam, S. Korea during spring of
2011. Randomly selected 11 isolates from MRS agar plates
were identified first by API CHL 50 kits and then 16S
rRNA gene sequencing. All 11 isolates were identified as
Lactobacillus plantarum. Among them, ST4 grew in MRS
broth with ethanol up to 10%, showing the highest alcohol
resistance. L. plantarum ST4 was moderately resistant
against acid and bile salts. When cellular proteins of L.
plantarum ST4 under ethanol stress were analyzed by
two-dimensional gel electrophoresis (2DE), the intensities
of 6 spots increased, whereas 22 spots decreased at least
2-fold. Those 28 spots were identified by peptide mass
fingerprinting (PMF). FusA2 (elongation factor G) increased
18.8-fold (6% ethanol) compared with control. Other proteins
were AtpD (ATP synthase subunit beta), DnaK, GroEL,
Tuf (elongation factor Tu), and Npr2 (NADH peroxidase),
respectively. Among the 22 proteins decreased in intensities,
lactate dehydrogenases (LdhD and LdhL1) were included.

Keywords: Makgeolli, LAB, Lactobacillus plantarum, ethanol stress

References

  1. Arnau, J., K. I. Sorensen, K. Appel, F. K. Vogensen, and K. Hammer. 1996. Analysis of heat shock gene expression in Lactococcus lactis MG1363. Microbiology 142: 1685-1691.
    Pubmed CrossRef
  2. Broadbent, J. R., R. L. Larsen, V. Deibel, and J. L. Steele. 2010. Physiological and transcriptional response of Lactobacillus casei ATCC 334 to acid stress. J. Bacteriol. 192: 2445-2458.
    Pubmed KoreaMed CrossRef
  3. Bron, P. A., D. Molenaar, W. M. de Vos, and M. Kleerebezem. 2006. DNA micro-array based identification of bile-responsive genes in Lactobacillus plantarum. J. Appl. Microbiol. 100: 728-738.
    Pubmed CrossRef
  4. Caldas, T. D., A. El. Yaagoubi, and G. Richarme. 1998. Chaperone properties of bacterial elongation factor EF-Tu. J. Biol. Chem. 273: 11478-11482.
    Pubmed CrossRef
  5. Cho, M. J., B. S. Jeon, J. W. Park, T. S. Jung, J. Y. Song, W. K. Lee, et al. 2002. Identifying the major proteome components of Helicobacter pylori strain 26695. Electrophoresis 23: 1161-1173.
    CrossRef
  6. De Angelis, M., R. Di Cagno, C. Huet, C. Crecchio, P. F. Fox, and M. Gobbetti. 2004. Heat shock response in Lactobacillus plantarum. Appl. Environ. Microbiol. 70: 1336-1346.
    Pubmed KoreaMed CrossRef
  7. Desmond, C., G. F. Fitzgerald, C. Stanton, and R. P. Ross. 2004. Improved stress tolerance of GroESL-overproducing Lactococcus lactis and probiotic Lactobacillus paracasei NFBC 338. Appl. Environ. Microbiol. 70: 5929-5936.
    Pubmed KoreaMed CrossRef
  8. Ding, W. K. and N. P. Shah. 2007. Acid, bile, and heat tolerance of free and microencapsulated probiotic bacteria. J. Food Sci. 72: M446-M450.
    Pubmed CrossRef
  9. G-Alegria, E., I. López, J. I. Ruiz, J. Sáenz, E. Fernández, M. Zarazaga, M. Dizy, C. Torres, and F. Ruiz-Larrea. 2004. High tolerance of wild Lactobacillus plantarum and Oenococcus oeni strains to lyophilization and stress environmental conditions of acid pH and ethanol. FEMS Microbiol. Lett. 230: 53-61.
    CrossRef
  10. Hong, Y., Y. B. Kim, S. O. Park, and E. H. Choi. 1997. Microflora and physicochemical characteristics of nuruk and main mashes during fermentation of a traditional Andong-soju. Food Sci. Biotechnol. 6: 297-303.
  11. Jin, J., S. Y. Kim, Q. Jin, H. J. Eom, and N. S. Han. 2008. Diversity analysis of lactic acid bacteria in takju, Korean rice wine. J. Microbiol. Biotechnol. 18: 1678-1682.
    Pubmed
  12. Kim, H. R., Y. H. Kwon, S. J. Jo, J.-H. Kim, and B.-H. Ahn. 2009. Characterization and volatile flavor components in glutinous rice wines prepared with different yeasts of nuruks. J. Food Sci. Technol. 41: 296-301 (in Korean)
  13. Kim, H. R., J.-H. Kim, D.-H. Bae, and B.-H. Ahn. 2010. Characterization of yakju brewed from glutinous rice and wildtype yeast strains isolated from nuruks. J. Microbiol. Biotechnol. 20: 1702-1710.
    Pubmed
  14. Kim, H. S., J. S. Hyun, J. Kim, H. P. Ha, and T. S. Yu. 1998. Enzymological characteristics and identification of useful fungi isolated from traditional Korean nuruk. Korean J. Appl. Microbiol. Biotechnol. 26: 456-464 (in Korean)
  15. 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.
    Pubmed CrossRef
  16. Koebmann, B. J., D. Nilsson, O. P. Kuipers, and P. R. Jensen. 2000. The membrane-bound H(+)-ATPase complex is essential for growth of Lactococcus lactis. J. Bacteriol. 182: 4738-4743.
    Pubmed KoreaMed CrossRef
  17. Lee, J. W. and J. Y. Shim. 2010. Quality characteristics of makgeolli during freezing storage. Food Eng. Prog. 14: 328334 (in Korean).
  18. Lee, Y. K. and S. Salminen. 1995. The coming of age of probiotics. Trends Food Sci. Technol. 6: 241-245.
    Pubmed CrossRef
  19. Le Marrec, C., E. Bon, and A. Lonvaud-Funel. 2007. Tolerance to high osmolality of the lactic acid bacterium Oenococcus oeni and identification of potential osmoprotectants. Int. J. Food Microbiol. 15: 335-342.
    Pubmed CrossRef
  20. Liu, S.-Q. 2002. A review malolactic fermentation in wine beyond deacidification. J. Appl. Microbiol. 92: 589-602.
    Pubmed CrossRef
  21. O’Connell, K. L. and J. T. Stults. 1997. Identification of mouse liver proteins on two-dimensional electrophoresis gel by matrixassisted laser desorption/ionization mass spectrometry of in situ enzymatic digests. Electrophoresis 18: 349-359.
    Pubmed CrossRef
  22. Park, J. C., M. Ok, J. Y. Cha, and Y. S. Cho. 2003. Isolation and identification of the high-glutathione producing Saccharomyces cerevisiae FF-8 from Korean traditional rice wine and optimal producing conditions. J. Korean Soc. Agric. Chem. Biotech. 46:348-352 (in Korean)
  23. Pieterse, B., R. J. Leer, F. H. Schuren, and M. J. van der Werf. 2005. Unravelling the multiple effects of lactic acid stress on Lactobacillus plantarum by transcription profiling. Microbiology 151: 3881-3894.
    Pubmed CrossRef
  24. Plumed-Ferrer, C., K. M. Koistinen, T. L. Tolonen, S. J. Lehesranta, S. O. Karenlampi, E. M. Kimattila, V. Joutsjoki, V. Virtanen, and A. von Wright. 2008. Comparative study of sugar fermentation and protein expression patterns of two Lactobacillus plantarum strains grown in three different media. Appl. Environ. Microbiol. 74: 5349-5358.
    Pubmed KoreaMed CrossRef
  25. Salotra, P., D. K. Singh, K. P. Seal, N. Krishna, H. Jaffe, and R. Bhatnagar. 1995. Expression of DnaK and GroEL homologs in Leuconostoc mesenteroides in response to heat shock, cold shock or chemical stress. FEMS Microbiol Lett. 15: 57-62.
    Pubmed CrossRef
  26. Sanchez, B., M. C. Champomier-Verges, P. Anglade, F. Baraige, C. G. D. Reyes-Gavilan, A. Margolles, and M. Zagorec. 2005. Proteomic analysis of global changes in protein expression during bile salt exposure of Bifidobacterium longum NCIMB 8809. J. Bacteriol. 187: 5799-5808.
    Pubmed KoreaMed CrossRef
  27. Seo, D. H., J. H. Jung, H. Y. Kim, Y. R. Kim, S. J. Ha, Y. C. Kim, and C. S. Park. 2007. Identification of lactic acid bacteria involved in traditional Korean rice wine fermentation. Food Sci. Biotechnol. 16: 994-998.
  28. Seo, M. J. and S. R. Ryu. 2002. Screening and characteristics of ethanol tolerant strain Saccharomyces cerevisiae SE211. Korean J. Appl. Microbiol. Biotechnol. 30: 216-222 (in Korean)
  29. Shin, Y. D. and D. H. Cho. 1970. A study on the microflora changes during takju brewing. Kor. J. Microbiol. 8: 53-64 (in Korean)
  30. Sico, M. A., M. G. Bonomo, A. D’Adamo, S. Bochicchio, and G. Salzano. 2009. Fingerprinting analysis of Oenococcus oeni strains under stress conditions. FEMS Microbiol. Lett. 296: 11-17.
    Pubmed CrossRef
  31. Stark, H., V. M. Rodnina, H. J. Wieden, F. Zemlin, W. Wintermeyer, and M. van Heel. 2002. Ribosome interactions of aminoacyl-tRNA and elongation factor Tu in the codonrecognition complex. Nat. Struct. Biol. 9: 849-854.
    Pubmed
  32. Wickner, S., J. Hoskins, and K. McKenney. 1991. Function of DnaJ and DnaK as chaperones in origin-specific DNA binding by RepA. Nature 350: 165-167.
    Pubmed CrossRef
  33. Wilkins, J. C., K. A. Homer, and D. Beighton. 2002. Analysis of Streptococcus mutans proteins modulated by culture under acidic conditions. Appl. Environ. Microbiol. 68: 2382-2390.
    Pubmed KoreaMed CrossRef