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Isolation, identification, and probiotic characteristics of Bacillus strains affecting the biogenic amine content in fermented soybean paste

발효 된장의 바이오제닉 아민 함량에 영향을 미치는 바실러스균의 분리 동정 및 프로바이오틱 특성

Lim, Eun-Seo
임은서

  • Received : 2019.02.11
  • Accepted : 2019.03.27
  • Published : 2019.06.30

Abstract

The primary objective of this study was to determine the content of biogenic amines in Korean traditional fermented soybean pastes (doenjang) and to isolate potential probiotic Bacillus sp. with the ability to inhibit biogenic amines accumulation. There were significant differences in the bacterial cell counts, pH value, titratable acidity, salinity, and biogenic amine content between the samples. Among Bacillus strains isolated from doenjang, Bacillus (B.) licheniformis DB102, B. subtilis DB203, B. stearothermophilus DB206, Bacillus sp. DB209, Bacillus sp. DB310, B. coagulans DB311, B. cereus DB313, B. amyloliquefaciens DB714, Bacillus sp. DB917, B. cereus DB 915, B. subtilis DB1020, and Bacillus sp. DB1022 were found to be able to produce biogenic amines. On the other hand, biogenic amine-degrading strains were identified as Bacillus sp. DB403, Bacillus sp. DB407, B. subtilis DB517, B. licheniformis DB612, and B. subtilis DB821. In particular, Bacillus sp. DB407 and B. subtilis DB821 showed probiotic properties including tolerance to artificial digestive juices, adherence to intestinal epithelial cells, resistance to antibiotics, and antibacterial activity against biogenic amine-producing strains. In conclusion, the two probiotic Bacillus strains may be considered as the suitable starter for manufacture of fermented soybean foods with low biogenic amines content.

Keywords

Bacillus;biogenic amine;probiotic

References

  1. Al Bulushi I, Poole S, Deeth HC, and Dykes GA. 2009. Biogenic amines in fish: roles in intoxication, spoilage, and nitrosamine formation. A review. Crit. Rev. Food Sci. Nutr. 49, 369-377.
  2. Alander M, Korpela R, Saxelin M, Vilpponen-Salmela T, Matilla-Sandholm T, and Wright A. 1997. Recovery of Lactobacillus rhamnosus GG from human colonic biopsies. Lett. Appl. Microbiol. 24, 361-364. https://doi.org/10.1046/j.1472-765X.1997.00140.x
  3. Argyri AA, Nisiotou AA, Malauchos A, Panagou EZ, and Tassou CC. 2014. Performance of two potential probiotic Lactobacillus strains from the olive microbiota as starters in the fermentation of heat shocked green olives. Int. J. Food Microbiol. 171, 68-76. https://doi.org/10.1016/j.ijfoodmicro.2013.11.003
  4. Brink B, Damink C, Joosten HMLJ, and Huis In't Veld JHJ. 1990. Occurrence and formation of biologically active amines in foods. Int. J. Food Microbiol. 11, 73-84. https://doi.org/10.1016/0168-1605(90)90040-C
  5. Cho TY, Han GH, Bahn KN, Son YW, Jan MR, Lee CH, Kim SH, Kim DB, and Kim SB. 2006. Evaluation of biogenic amines in Korean commercial fermented foods. Korean J. Food Sci. Technol. 38, 730-737.
  6. Choi JY, Hong SW, and Chung KS. 2012. Selection of biogenic amine-reducing microorganisms from a traditional Korean-style fermented food, Cheonggukjang. Korean J. Food Sci. Technol. 44, 196-201. https://doi.org/10.9721/KJFST.2012.44.2.196
  7. Dapkevicius MLNE, Nout MJR, Rombouts FM, Houben JH, and Wymenga W. 2000. Biogenic amine formation and degradation by potential fish silage starter microorganisms. Int. J. Food Microbiol. 191, 53-59.
  8. Eerola S, Roig-Sagues AX, and Hirvi TK. 1998. Biogenic amines in Finnish dry sausages. J. Food Saf. 18, 127-138. https://doi.org/10.1111/j.1745-4565.1998.tb00208.x
  9. Elshaghabee FMF, Rokana N, Gulhane RD, Sharma C, and Panwar H. 2017. Bacillus as potential probiotics: Status, concerns, and future perspectives. Front. Microbiol. 8, 1-15.
  10. Fuller R. 1991. Probiotics in human medicine. Gut 32, 439-442. https://doi.org/10.1136/gut.32.4.439
  11. Gardini F, Ozogul Y, Suzzi G, Tabanelli G, and Ozogul F. 2016. Technological factors affecting biogenic amine content in foods: A review. Front. Microbiol. 7, 1-18.
  12. Guan RF, Liu ZF, Zhang JJ, Wei YX, Wahab S, Liu DH, and Ye XQ. 2013. Investigation of biogenic amines in sufu(furu): A Chinese traditional fermented soybean food product. Food Cont. 31, 345-352. https://doi.org/10.1016/j.foodcont.2012.10.033
  13. Han GH, Cho TY, Yoo MS, Kim CS, Kim JM, Kim HA, Kim MO, Kim SC, Lee SA, Ko YS, et al. 2007. Biogenic amines formation and content in fermented soybean paste (Cheonggukjang). Korean J. Food Sci. Technol. 39, 541-545.
  14. Hanifi A, Culpepper T, Mai V, Anand A, Ford AL, and Ukhanova M. 2015. Evaluation of Bacillus subtilis R0179 on gastrointestinal viability and general wellness: A randomized, double-blind, placebo-controlled trial in healthy adults. Benef. Microbes 6, 19-27.
  15. Hernandez-Jover T, Izquierdo-Pulido M, Vechiana-Nogues MT, Marine-Font A, and Vidal-Carou MC. 1997. Biogenic amines and polyamine contents in meat and meat products. J. Ag. Food Chem. 45, 2098-2102.
  16. Herrero-Fresno A, Martinez N, Sanhez-Llana E, Diaz M, Ferrandez M, Martin MC, Ladero V, and Alvarez MA. 2012. Lactobacillus casei strains isolated from cheese reduce biogenic amines accumulation in an experimental model. Int. J. Food Microbiol. 157, 297-304. https://doi.org/10.1016/j.ijfoodmicro.2012.06.002
  17. Holo H, Nilssen O, and Nes IF. 1991. Lactococcin A. a new bacteriocin from Lactococcus lactis subsp. cremoris: isolation and characterization of the protein and its gene. J. Bacteriol. 173, 3879-3887. https://doi.org/10.1128/jb.173.12.3879-3887.1991
  18. Jena PK, Trivedi D, Thakore K, Chaudhary H, Giri SS, and Seshadri S. 2013.Isolation and characterization of probiotic properties of lactobacilli isolated from rat fecal microbiota. Microbiol. Immunol. 57, 407-416. https://doi.org/10.1111/1348-0421.12054
  19. Jeon HH, Jung JY, Chun BH, Kim MD, Baek SY, Moon JY, Yeo SH, and Jeon CO. 2016. Screening and characterization of potential Bacillus starter cultures for fermenting low-salt soybean paste (doenjang). J. Microbiol. Biotechnol. 26, 666-674.
  20. Kalac P and Krausova P. 2005. A review of dietary polyamines: Formation, implications for growth and health and occurrence in foods. Food Chem. 77, 349-351.
  21. Kim JH, Ahn HJ, Kim DH, Jo C, Yook HS, Park HJ, and Byun MW. 2003a. Irradiation effects on biogenic amines in Korean fermented soybean paste during fermentation. J. Food Sci. 68, 80-84. https://doi.org/10.1111/j.1365-2621.2003.tb14118.x
  22. Kim YS, Cho SH, Jeong DY, and Uhm TB. 2012. Isolation of biogenic amines-degrading strains of Bacillus subtilis and Bacillus amyloliquefaciens from traditionally fermented soybean products. Korean J. Microbiol. 48, 220-224. https://doi.org/10.7845/kjm.2012.042
  23. Kim KM, Kim MJ, Kim DH, Park YS, and Kang JS. 2009. Characterization of Bacillus polyfermenticus KJS-2 as a probiotic. J. Microbiol. Biotechnol. 19, 1013-1018. https://doi.org/10.4014/jmb.0903.113
  24. Kim M, Oh HS, Park SC, and Chun J. 2014. Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. Int. J. Syst. Evol. Microbiol. 64, 346-351. https://doi.org/10.1099/ijs.0.059774-0
  25. Kim JH, Park HJ, Kim MJ, Ahn HJ, and Byun MW. 2003b. Survey of biogenic amine contents in commercial soy sauce. Korean J. Food Sci. Technol. 35, 325-328.
  26. Lee HT, Kim JH, and Lee SS. 2009. Analysis of microbiological contamination and biogenic amines content in traditional and commercial doenjang. J. Fd. Hyg. Safety 24, 102-109.
  27. Lee SK, Lee JJ, Jin YI, Jeong JC, Chang YH, Lee YS, Jeong YH, and Kim MS. 2017. Probiotic characteristics of Bacillus strains isolated from Korean traditional soy sauce. LWT-Food Sci. Technol. 79, 518-524. https://doi.org/10.1016/j.lwt.2016.08.040
  28. Lee YC, Lin CS, Liu FL, Huang TC, and Tsai YH. 2015. Degradation of histamine by Bacillus polymyxa isolated from salted fish products. J. Food Drug Anal. 23, 836-844. https://doi.org/10.1016/j.jfda.2015.02.003
  29. Lehane L and Olley J. 2000. Histamine fish poisoning revisited. Int. J. Food Microbiol. 58, 1-37. https://doi.org/10.1016/S0168-1605(00)00296-8
  30. Li L, Wen X, Wen Z, Chen S, Wang L, and Wei X. 2018. Evaluation of the biogenic amines formation and degradation abilities of Lactobacillus curvatus from Chinese bacon. Front. Microbiol. 9, 1-9. https://doi.org/10.3389/fmicb.2018.00001
  31. Mah JH. 2015. Fermented soybean foods: Significance of biogenic amines. Austin J. Nutri. Food Sci. 3, 1058-1060.
  32. Manhar AK, Saikia D, Bashir Y, Mech RK, Nath D, and Konwar BK. 2015. In vitro evaluation of celluloytic Bacillus amyloliquefaciens AMS1 isolated from traditional fermented soybean (Churpi) as an animal probiotic. Res. Veterinary Sci. 99, 149-156. https://doi.org/10.1016/j.rvsc.2015.01.008
  33. Moon JY, Kwon SW, Hong SB, Seok SJ, Kim JS, and Kim SJ. 2015. Characteristics and functional analysis of Bacillus strains from the fermented soybean products, Cheonggukjang. Korean J. Microbiol. 51, 300-307. https://doi.org/10.7845/kjm.2015.5044
  34. Olmos J and Paniagua-Michel J. 2014. Bacillus subtilis a potential probiotic bacterium to formulate functional feeds for aquaculture. J. Microb. Biochem. Technol. 6, 7-10.
  35. Otero MC, Ocana VS, and Macias ENM. 2004. Bacterial surface characteristics applied to selection of probiotic microorganisms. Methods Mol. Biol. 268, 435-440.
  36. Patel AK, Ahire JJ, Pawar SP, Chaudhari BL, and Chincholkar SB. 2009. Comparative accounts of probiotic characteristics of Bacillus spp. isolated from food wastes. Food Res. Int. 42, 505-510. https://doi.org/10.1016/j.foodres.2009.01.013
  37. Pedersen K and Tannock GW. 1989. Colonization of the porcine gastrointestinal tract by lactobacilli. Appl. Environ. Microbiol. 55, 279-283.
  38. Ryu MS, Yang HJ, Kim JW, Jeong SJ, Jeong SY, Eom JS, and Jeong DY. 2017. Potential probiotics activity of Bacillus spp. from traditional soybean pastes and fermentation characteristics of Cheonggukjang. Korean J. Food Preserv. 24, 1168-1179.
  39. Savitha K, Srinivas M, and Dhanalakshmi K. 2016. Isolation and characterization of bacteriocin from Bacillus cereus MTCC 1307. Int. J. Appl. Pure Sci. Agric. 2, 200-208.
  40. Seker E. 2010. Identification of Candida species isolated from bovine mastitic milk and their in vitro hemolytic activity in Western Turkey. Mycopathologia 169, 303-380. https://doi.org/10.1007/s11046-009-9255-z
  41. Shalaby AR. 1996. Significance of biogenic amines to food safety and human health. Food Res. Int. 29, 675-690. https://doi.org/10.1016/S0963-9969(96)00066-X
  42. Shim JM, Lee KW, Yao Z, Kim HJ, and Kim JH. 2016.Properties of doenjang (soybean paste) prepared with different types of salts. J. Microbiol. Biotechnol. 26, 1533-1541. https://doi.org/10.4014/jmb.1605.05019
  43. Shin DH and Jeong DY. 2015. Korean traditional fermented soybean products: Jang. J. Ethnic Food 2, 2-7. https://doi.org/10.1016/j.jef.2015.02.002
  44. Shukla S, Park HK, Kim JK, and Kim MH. 2010. Determination of biogenic amines in Korean traditional fermented soybean paste (Doenjang). Food Chem. Toxicol. 48, 1191-1195. https://doi.org/10.1016/j.fct.2010.01.034
  45. Suva MA, Sureja VP, and Kheni DB. 2018. Novel insight on probiotic Bacillus subtilis: Mechanism of action and clinical applications. J. Curr. Res. Sci. Med. 2, 65-72.
  46. Tabanelli G, Montanari C, Bargossi E, Lanciotti R, Gatto V, Felis G, Torriani S, and Gardini F. 2014. Control of tyramine and histamine accumulation by lactic acid bacteria using bacteriocin forming lactococci. Int. J. Food Microbiol. 190, 14-23. https://doi.org/10.1016/j.ijfoodmicro.2014.08.023
  47. Wang T and Su J. 2016. Bacillus subtilis from soybean food shows antimicrobial activity for multidrug-resistant Acinetobacter baumannii by affecting the adeS gene. J. Microbiol. Biotechnol. 26, 2043-2050. https://doi.org/10.4014/jmb.1607.07006
  48. Wunderlichova L, Bunkova L, Koutny M, Jancova P, and Bunka F. 2014. Formation, degradation, and detoxification of putrescine by foodborne bacteria: a review. Comp. Rev. Food Sci. Food Safety 13, 1012-1030. https://doi.org/10.1111/1541-4337.12099
  49. Zhang Q, Lin S, and Nie X. 2013. Reduction of biogenic amine accumulation in silver carp sausage by an amine-negative Lactobacillus plantarum. Food Control 32, 496-500.