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References

  1. Altschul SF, Madded TL, Schaffer AA, Zhang J, Zhang Z, Miller W. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search program. Nucleic Acids Res. 25: 3389-3402.
    Pubmed PMC CrossRef
  2. Bae JW, Rhee SK, Park JR, Chung WH, Nam YD, Lee I, et al. 2005. Development and evaluation of genome-probing microarrays for monitoring lactic acid bacteria. Appl. Environ. Microbiol. 71: 8825-8835.
    Pubmed PMC CrossRef
  3. Breslin PA, Beuchamp GK. 1997. Salt enhances flavor by suppressing bitterness. Nature 387: 563.
    Pubmed CrossRef
  4. Cheigh HS, Park KY. 1994. Biochemical, microbiological, and nutritional aspects of kimchi (Korean fermented vegetable products). Crit. Rev. Food Sci. Nutr. 34: 175-203.
    Pubmed CrossRef
  5. Cho EJ, Lee SM, Rhee SH, Park KY. 1998. Studies on the standardization of Chinese cabbage kimchi. Korean J. Food Sci. Technol. 30: 324-332.
  6. Choi HJ, Cheigh CI, Kim SB, Lee JC, Lee DW, Choi SW, Park JM, Pyun YR. 2002. Weissella kimchii sp. nov., a novel lactic acid bacterium from kimchi. Int. J. Syst. Evol. Microbiol. 52: 507-511.
    Pubmed CrossRef
  7. Choi NY, Chun JK. 1996. Development of a microcontrollerbased process controller for on-line monitoring of kimchi fermentation. Foods Biotechnol. 5: 198-200.
  8. Choi SM, Jun YS, Park KY, Cheigh HS. 1991. Changes in the contents of moisture, reducing sugar, microorganisms, NO2 and NO3 during salting in various varieties of Chinese cabbage for kimchi fermentation. Res. Bull. Coll. Home Econ. Pusan Natl. Univ. 17: 25-30.
  9. Franz CM, Von Holy A. 1996. Thermotolerance of meat spoilage lactic acid bacteria and their inactivation in vacuum-packaged Vienna sausages. Int. J. Food Microbiol. 29:59-73.
    CrossRef
  10. Hong Y, Yang HS, Chang HC, Kim HY. 2013. Comparison of bacterial community changes in fermenting kimchi at two different temperatures using a denaturing gradient gel electrophoresis analysis. J. Microbiol. Biotechnol. 23: 76-84.
    Pubmed CrossRef
  11. Jo JS. 2002. Kimchi preservation, pp. 307-347. In: Studies on Kimchi. Yurim Munhwasa Publishing Co., Seoul.
    Pubmed
  12. Jung HJ, Hong Y, Yang HS, Chang HC, Kim HY. 2012. Distribution of lactic acid bacteria in garlic (Allium sativum) and green onion (Allium fistulosum) using SDS-PAGE whole cell protein pattern comparison and 16S rRNA gene sequence analysis. Food Sci. Biotechnol. 21: 1457-1462.
    CrossRef
  13. Kim BJ, Lee HJ, Park SY, Kim JH, Han HU. 2000. Identification and characterization of Leuconostoc gelidum isolated from kimchi, a fermented cabbage product. J. Microbiol. 38: 132-136.
  14. Kim ES, Chun HC, Kim BK, Rhee KC. 1997. Garlic and cancer prevention. J. Food Sci. Nutr. 2: 180-190.
  15. Kim J, Chun J, Han HU. 2000. Leuconostoc kimchii sp. nov., a new species from kimchi. Int. J. Syst. Evol. Microbiol. 50:1915-1919.
    Pubmed CrossRef
  16. Kim J F, J eong H, Lee JS, Choi SH, Ha M, Hur CG, et al. 2008. Complete genome sequence of Leuconostoc citreum KM20. J. Bacteriol. 190: 3093-3094.
    Pubmed PMC CrossRef
  17. Kim M, Chun J. 2005. Bacterial community structure in kimchi, a Korean fermented vegetable food, as revealed by 16S rRNA gene analysis. Int. J. Food Microbiol. 103: 9-96.
    Pubmed CrossRef
  18. Kim TW, Lee JH, Kim SE, Park MH, Chang HC, Kim HY. 2010. Analysis of microbial communities in doenjang, a Korean fermented soybean paste, using nested PCRdenaturing gradient gel electrophoresis. Int. J. Food Microbiol. 131: 265-271.
    Pubmed CrossRef
  19. Kim TW, Lee JY, Song HS, Park JH, Ji GE, Kim HY. 2004. Isolation and identification of Weissella kimchii from green onion by cell protein pattern analysis. J. Microbiol. Biotechnol. 14: 105-109.
  20. Korea Food and Drug Administration. 2008. Korean Food Standard Codex: Korea Foods Industry Association, Para 5-23-1. KFDA, Korea.
  21. Lawless H, Heymann H. 1998. Sensory Evaluation of Food:Principles and Practices, pp. 254-258. Chapman & Hall, New York.
  22. Lee CW, Ko CY, Ha DM. 1992. Microfloral changes of the lactic acid bacteria during kimchi fermentation and identification of the isolates. Korean J. Appl. Microbiol. Biotechnol. 20: 102-109.
  23. Lee JS, Heo GY, Jun WL, Oh YJ, Park JA, Park YH, et al. 2005. Analysis of kimchi microflora using denaturing gradient gel electrophoresis. Int. J. Food Microbiol. 102: 143-150.
    Pubmed CrossRef
  24. Lee M, Cho KH, Han ES, Lee JH. 2010. Bacterial diversity in the initial fermentation stage of Korean and Chinese kimchi. Korean J. Microbiol. Biotechnol. 38: 207-215.
  25. Lee YH, Yang IW. 1970. Studies on the packaging and preservation of kimchi. J. Korean Agric. Chem. Soc. 13: 207-218.
  26. Leroy F, De Vuyst L. 1999. The presence of salt and a curing agent reduces bacteriocin production by Lactobacillus sakei CTC 494, a potential starter culture for sausage fermentation. Appl. Environ. Microbiol. 65: 5350-5356.
    Pubmed PMC
  27. Lim CR, Park HK, Han HU. 1989. Reevaluation of isolation and identification of gram-positive bacteria in kimchi. Korean J. Microbiol. 27: 404-414.
  28. Magnusson J, Jonsson H, Schnurer J, Roos S. 2010. Weissella soli sp. nov., a lactic acid bacterium isolated from soil. Int. J. Syst. Evol. Microbiol. 52: 831-834.
  29. McCarron JL, Keefe GP, McKenna SL, Dohoo IR, Poole DE. 2009. Laboratory evaluation of 3M Petrifilms and University of Minnesota bi-plates as potential on-farm tests for clinical mastitis. J. Dairy Sci. 92: 2297-2305.
    Pubmed CrossRef
  30. Mheen TI. 1998. Kimchi fermentation and characteristics of the related lactic acid bacteria. Korea Inst. Sci. Technol. Inform. 1: 1-34.
  31. Mheen TI. 1998. Kimchi, pp. 454-480. In Mheen TI (eds.). Microorganisms and Industry. Hanlimwon Publishing Co., Seoul.
  32. Mheen TI, Kwon TW. 1984. Effect of temperature and salt concentrations on kimchi fermentation. Korean J. Food Sci. Technol. 16: 443-450.
  33. Muyzer G, Smalia K. 1998. Application of denaturing gradient gel electrophoresis DGGE and temperature gradient gel electrophoresis TGGE in microbial ecology. Antonie Van Leeuwenhoek 73: 127-141.
    Pubmed CrossRef
  34. Park HR, Jeong GO, Lee SL, Kim JY, Kang SA, Park KY, Ryou HJ. 2009. Workers intake too much salt from dishes of eating out and food service cafeterias; direct chemical analysis of sodium content. Nutr. Res. Pract. 3: 328-333.
    Pubmed PMC CrossRef
  35. Park JA, Heo GY, Lee JS, Oh YJ, Kim BY, Mheen TI. 2003. Change of microbial communities in kimchi fermentation at low temperature. Korean J. Microbiol. 39: 45-50.
  36. Park JM, Shin JH, Lee DW, Song JC, Suh HJ, Chang UJ, Kim JM. 2010. Identification of the lactic acid bacteria in kimchi according to initial and over-ripened fermentation using PCR and 16S rRNA gene sequence analysis. Food Sci. Biotechnol. 19: 541-546.
    CrossRef
  37. Peryam DR, Kroll BJ. 1998. The 9-point hedonic scale, pp. 2-7. Peryam & Kroll Research Corporation, USA.
  38. Rhee HS. 1972. Study in kimchi making. The concentration of salt solution and the soaking time of Chinese cabbage to prepare kimchi. Korean J. Food Nutr. 10: 35-43.
  39. Shaw BG, Harding CD. 1989. Leuconostoc gelidum sp. nov. and Leuconostoc carnosum sp. nov. from chill-stored meats. Int. J. Syst. Bacteriol. 39: 217-223.
    CrossRef
  40. Shin DH, Kim MS, Han JS, Lim DK, Park WS. 1996. Changes of chemical composition and microflora in commercial kimchi. Korean J. Food Sci. Technol. 28: 137-145.
  41. Shin MS, Han SK, Ryu JS, Kim KS, Lee WK. 2008. Isolation and partial characterization of a bacteriocin produced by Pediococcus pentosaceus K23-2 isolated from kimchi. J. Appl. Microbiol. 105: 331-339.
    Pubmed CrossRef
  42. So MH, Lee YS, Kim HS, Cho EJ, Yea MJ. 1996. An influence of salt concentrations on growth rates of lactic acid bacteria isolated from kimchi. Korean J. Food Nutr. 9:341-347.
  43. Son SM, Park YS, Lim HJ, Kim SB, Jeong YS. 2007. Sodium intakes of Korean adults with 24-hour urine analysis and dish frequency questionnaire and comparison of sodium intakes according to the regional area and dish group. Korean J. Community Nutr. 12: 545-558.
  44. Song ES, Jeon YS, Cheigh HS. 1997. Antioxidative effect of different kinds of kimchi on the lipid oxidation of cooked meat. J. Korean Soc. Food Sci. Nutr. 26: 993-997.
  45. Water J, Tannock GW, Tilsala-Timisjarvi A, Rodtong S, Loach DM, Munro K, Alatossava T. 2000. Detection and identification of gastrointestinal Lactobacillus species by using denaturing gradient gel electrophoresis and species specific PCR primer. Appl. Environ. Microbiol. 66: 297-303.
    CrossRef

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Article

Research article

J. Microbiol. Biotechnol. 2015; 25(12): 2049-2057

Published online December 28, 2015 https://doi.org/10.4014/jmb.1506.06058

Copyright © The Korean Society for Microbiology and Biotechnology.

Effect of Low Salt Concentrations on Microbial Changes During Kimchi Fermentation Monitored by PCR-DGGE and Their Sensory Acceptance

Lenny S. F. Ahmadsah 1, Sung-Gi Min 1, Seon-Kyeong Han 1, Yeun Hong 1 and Hae-Yeong Kim 1*

Institute of Life Sciences & Resources and Department of Food Science and Biotechnology, Kyung Hee University, Yongin 446-701, Republic of Korea

Received: June 29, 2015; Accepted: September 5, 2015

Abstract

Various salt concentrations (1.0%, 1.3%, 1.6%, 1.9%, and 2.1% labeled as sample A, B, C, D, and
E, respectively) were investigated for microbial diversity, identification of Lactic Acid Bacteria
(LAB) in salted kimchi cabbage, prepared under laboratory conditions. These samples were
stored at 4°C for 5 weeks in proper aluminum-metalized pouch packaging with calcium
hydroxide gas absorber. A culture-independent method known as polymerase chain reaction –
denaturing gradient gel electrophoresis was carried out to identify LAB distributions among
various salt concentration samples that had identified 2 Weissella (W. confusa and W. soli), 1
Lactobacillus (Lb. sakei), and 3 Leuconostoc (Lc. mesenteroides, Lc. lactis, and Lc. gelidum) in the
overall kimchi samples. The pH, titratable acidity, viable cell counts, and coliform counts were
not affected by salt variations. In order to assess sensory acceptance, the conducted sensory
evaluation using a 9-point hedonic scale had revealed that samples with 1.3% salt
concentration (lower than the manufacturer’s regular salt concentration) was more preferred,
indicating that the use of 1.3% salt concentration was acceptable in normal kimchi fermentation
for its quality and safety. Despite similarities in pH, titratable acidity, viable cell counts,
coliform counts, and LAB distributions among the various salt concentrations of kimchi
samples, the sample with 1.3% salt concentration was shown to be the most preferred,
indicating that this salt concentration was suitable in kimchi production in order to reduce salt
intake through kimchi consumptions.

Keywords: low salt, kimchi, lactic acid bacteria, PCR-DGGE, sensory evaluation

References

  1. Altschul SF, Madded TL, Schaffer AA, Zhang J, Zhang Z, Miller W. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search program. Nucleic Acids Res. 25: 3389-3402.
    Pubmed KoreaMed CrossRef
  2. Bae JW, Rhee SK, Park JR, Chung WH, Nam YD, Lee I, et al. 2005. Development and evaluation of genome-probing microarrays for monitoring lactic acid bacteria. Appl. Environ. Microbiol. 71: 8825-8835.
    Pubmed KoreaMed CrossRef
  3. Breslin PA, Beuchamp GK. 1997. Salt enhances flavor by suppressing bitterness. Nature 387: 563.
    Pubmed CrossRef
  4. Cheigh HS, Park KY. 1994. Biochemical, microbiological, and nutritional aspects of kimchi (Korean fermented vegetable products). Crit. Rev. Food Sci. Nutr. 34: 175-203.
    Pubmed CrossRef
  5. Cho EJ, Lee SM, Rhee SH, Park KY. 1998. Studies on the standardization of Chinese cabbage kimchi. Korean J. Food Sci. Technol. 30: 324-332.
  6. Choi HJ, Cheigh CI, Kim SB, Lee JC, Lee DW, Choi SW, Park JM, Pyun YR. 2002. Weissella kimchii sp. nov., a novel lactic acid bacterium from kimchi. Int. J. Syst. Evol. Microbiol. 52: 507-511.
    Pubmed CrossRef
  7. Choi NY, Chun JK. 1996. Development of a microcontrollerbased process controller for on-line monitoring of kimchi fermentation. Foods Biotechnol. 5: 198-200.
  8. Choi SM, Jun YS, Park KY, Cheigh HS. 1991. Changes in the contents of moisture, reducing sugar, microorganisms, NO2 and NO3 during salting in various varieties of Chinese cabbage for kimchi fermentation. Res. Bull. Coll. Home Econ. Pusan Natl. Univ. 17: 25-30.
  9. Franz CM, Von Holy A. 1996. Thermotolerance of meat spoilage lactic acid bacteria and their inactivation in vacuum-packaged Vienna sausages. Int. J. Food Microbiol. 29:59-73.
    CrossRef
  10. Hong Y, Yang HS, Chang HC, Kim HY. 2013. Comparison of bacterial community changes in fermenting kimchi at two different temperatures using a denaturing gradient gel electrophoresis analysis. J. Microbiol. Biotechnol. 23: 76-84.
    Pubmed CrossRef
  11. Jo JS. 2002. Kimchi preservation, pp. 307-347. In: Studies on Kimchi. Yurim Munhwasa Publishing Co., Seoul.
    Pubmed
  12. Jung HJ, Hong Y, Yang HS, Chang HC, Kim HY. 2012. Distribution of lactic acid bacteria in garlic (Allium sativum) and green onion (Allium fistulosum) using SDS-PAGE whole cell protein pattern comparison and 16S rRNA gene sequence analysis. Food Sci. Biotechnol. 21: 1457-1462.
    CrossRef
  13. Kim BJ, Lee HJ, Park SY, Kim JH, Han HU. 2000. Identification and characterization of Leuconostoc gelidum isolated from kimchi, a fermented cabbage product. J. Microbiol. 38: 132-136.
  14. Kim ES, Chun HC, Kim BK, Rhee KC. 1997. Garlic and cancer prevention. J. Food Sci. Nutr. 2: 180-190.
  15. Kim J, Chun J, Han HU. 2000. Leuconostoc kimchii sp. nov., a new species from kimchi. Int. J. Syst. Evol. Microbiol. 50:1915-1919.
    Pubmed CrossRef
  16. Kim J F, J eong H, Lee JS, Choi SH, Ha M, Hur CG, et al. 2008. Complete genome sequence of Leuconostoc citreum KM20. J. Bacteriol. 190: 3093-3094.
    Pubmed KoreaMed CrossRef
  17. Kim M, Chun J. 2005. Bacterial community structure in kimchi, a Korean fermented vegetable food, as revealed by 16S rRNA gene analysis. Int. J. Food Microbiol. 103: 9-96.
    Pubmed CrossRef
  18. Kim TW, Lee JH, Kim SE, Park MH, Chang HC, Kim HY. 2010. Analysis of microbial communities in doenjang, a Korean fermented soybean paste, using nested PCRdenaturing gradient gel electrophoresis. Int. J. Food Microbiol. 131: 265-271.
    Pubmed CrossRef
  19. Kim TW, Lee JY, Song HS, Park JH, Ji GE, Kim HY. 2004. Isolation and identification of Weissella kimchii from green onion by cell protein pattern analysis. J. Microbiol. Biotechnol. 14: 105-109.
  20. Korea Food and Drug Administration. 2008. Korean Food Standard Codex: Korea Foods Industry Association, Para 5-23-1. KFDA, Korea.
  21. Lawless H, Heymann H. 1998. Sensory Evaluation of Food:Principles and Practices, pp. 254-258. Chapman & Hall, New York.
  22. Lee CW, Ko CY, Ha DM. 1992. Microfloral changes of the lactic acid bacteria during kimchi fermentation and identification of the isolates. Korean J. Appl. Microbiol. Biotechnol. 20: 102-109.
  23. Lee JS, Heo GY, Jun WL, Oh YJ, Park JA, Park YH, et al. 2005. Analysis of kimchi microflora using denaturing gradient gel electrophoresis. Int. J. Food Microbiol. 102: 143-150.
    Pubmed CrossRef
  24. Lee M, Cho KH, Han ES, Lee JH. 2010. Bacterial diversity in the initial fermentation stage of Korean and Chinese kimchi. Korean J. Microbiol. Biotechnol. 38: 207-215.
  25. Lee YH, Yang IW. 1970. Studies on the packaging and preservation of kimchi. J. Korean Agric. Chem. Soc. 13: 207-218.
  26. Leroy F, De Vuyst L. 1999. The presence of salt and a curing agent reduces bacteriocin production by Lactobacillus sakei CTC 494, a potential starter culture for sausage fermentation. Appl. Environ. Microbiol. 65: 5350-5356.
    Pubmed KoreaMed
  27. Lim CR, Park HK, Han HU. 1989. Reevaluation of isolation and identification of gram-positive bacteria in kimchi. Korean J. Microbiol. 27: 404-414.
  28. Magnusson J, Jonsson H, Schnurer J, Roos S. 2010. Weissella soli sp. nov., a lactic acid bacterium isolated from soil. Int. J. Syst. Evol. Microbiol. 52: 831-834.
  29. McCarron JL, Keefe GP, McKenna SL, Dohoo IR, Poole DE. 2009. Laboratory evaluation of 3M Petrifilms and University of Minnesota bi-plates as potential on-farm tests for clinical mastitis. J. Dairy Sci. 92: 2297-2305.
    Pubmed CrossRef
  30. Mheen TI. 1998. Kimchi fermentation and characteristics of the related lactic acid bacteria. Korea Inst. Sci. Technol. Inform. 1: 1-34.
  31. Mheen TI. 1998. Kimchi, pp. 454-480. In Mheen TI (eds.). Microorganisms and Industry. Hanlimwon Publishing Co., Seoul.
  32. Mheen TI, Kwon TW. 1984. Effect of temperature and salt concentrations on kimchi fermentation. Korean J. Food Sci. Technol. 16: 443-450.
  33. Muyzer G, Smalia K. 1998. Application of denaturing gradient gel electrophoresis DGGE and temperature gradient gel electrophoresis TGGE in microbial ecology. Antonie Van Leeuwenhoek 73: 127-141.
    Pubmed CrossRef
  34. Park HR, Jeong GO, Lee SL, Kim JY, Kang SA, Park KY, Ryou HJ. 2009. Workers intake too much salt from dishes of eating out and food service cafeterias; direct chemical analysis of sodium content. Nutr. Res. Pract. 3: 328-333.
    Pubmed KoreaMed CrossRef
  35. Park JA, Heo GY, Lee JS, Oh YJ, Kim BY, Mheen TI. 2003. Change of microbial communities in kimchi fermentation at low temperature. Korean J. Microbiol. 39: 45-50.
  36. Park JM, Shin JH, Lee DW, Song JC, Suh HJ, Chang UJ, Kim JM. 2010. Identification of the lactic acid bacteria in kimchi according to initial and over-ripened fermentation using PCR and 16S rRNA gene sequence analysis. Food Sci. Biotechnol. 19: 541-546.
    CrossRef
  37. Peryam DR, Kroll BJ. 1998. The 9-point hedonic scale, pp. 2-7. Peryam & Kroll Research Corporation, USA.
  38. Rhee HS. 1972. Study in kimchi making. The concentration of salt solution and the soaking time of Chinese cabbage to prepare kimchi. Korean J. Food Nutr. 10: 35-43.
  39. Shaw BG, Harding CD. 1989. Leuconostoc gelidum sp. nov. and Leuconostoc carnosum sp. nov. from chill-stored meats. Int. J. Syst. Bacteriol. 39: 217-223.
    CrossRef
  40. Shin DH, Kim MS, Han JS, Lim DK, Park WS. 1996. Changes of chemical composition and microflora in commercial kimchi. Korean J. Food Sci. Technol. 28: 137-145.
  41. Shin MS, Han SK, Ryu JS, Kim KS, Lee WK. 2008. Isolation and partial characterization of a bacteriocin produced by Pediococcus pentosaceus K23-2 isolated from kimchi. J. Appl. Microbiol. 105: 331-339.
    Pubmed CrossRef
  42. So MH, Lee YS, Kim HS, Cho EJ, Yea MJ. 1996. An influence of salt concentrations on growth rates of lactic acid bacteria isolated from kimchi. Korean J. Food Nutr. 9:341-347.
  43. Son SM, Park YS, Lim HJ, Kim SB, Jeong YS. 2007. Sodium intakes of Korean adults with 24-hour urine analysis and dish frequency questionnaire and comparison of sodium intakes according to the regional area and dish group. Korean J. Community Nutr. 12: 545-558.
  44. Song ES, Jeon YS, Cheigh HS. 1997. Antioxidative effect of different kinds of kimchi on the lipid oxidation of cooked meat. J. Korean Soc. Food Sci. Nutr. 26: 993-997.
  45. Water J, Tannock GW, Tilsala-Timisjarvi A, Rodtong S, Loach DM, Munro K, Alatossava T. 2000. Detection and identification of gastrointestinal Lactobacillus species by using denaturing gradient gel electrophoresis and species specific PCR primer. Appl. Environ. Microbiol. 66: 297-303.
    CrossRef