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http://dx.doi.org/10.7845/kjm.2018.8058

Antibacterial activity of lactic acid bacteria against biogenic amine-producing Bacillus spp. isolated from traditional fermented soybean paste  

Lim, Eun-Seo (Department of Food Science & Nutrition, Tongmyong University)
Publication Information
Korean Journal of Microbiology / v.54, no.4, 2018 , pp. 398-409 More about this Journal
Abstract
In the present study, biogenic amine-forming Bacillus spp. and bacteriocin-producing lactic acid bacteria (LAB) isolated from Doenjang were generally identified through 16S rRNA gene sequencing, and the physicochemical and microbiological characteristics of cheonggukjang prepared using the isolated strains were investigated. Biogenic amine-producing bacteria from the samples were identified as Bacillus licheniformis DB102, B. subtilis DB203, B. stearothermophilus DB206, B. pumilus DB209, B. subtilis DB310, B. coagulans DB311, B. cereus DB313, B. amyloliquefaciens DB714, B. amylolique-faciens DB915, B. licheniformis DB917, B. cereus DB1019, B. subtilis DB1020, B. megaterium DB1022. The bacteriocin-producing LAB showed antibacterial effect against biogenic amine-producing Bacillus spp. were identified as Lactobacillus plantarum DLA205, L. brevis DLA501, L. fermentum DLA509, L. acidophilus DLA703, and Enterococcus faecalis DLA804. The bacteriocin produced by the LAB significantly decreased the viable numbers and the amine production ability of the biogenic amine-forming Bacillus spp. in a concentration dependent manner. Therefore, the pH, ammonia nitrogen and biogenic amine content of cheonggukjang prepared by mixed culture of the LAB and Bacillus spp. were significantly decreased compared to the control group.
Keywords
Bacillus; bacteriocin; biogenic amine; lactic acid bacteria;
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1 Abdulla AA. 2014. Antimicrobial activity of Lactobacillus acidophilus that carry the bacteriocin gene. Int. J. Curr. Microbiol. App. Sci. 3, 269-276.
2 And HC and Hoover DG. 2003. Bacteriocins and their food applications. Compr. Rev. Food Sci. Food Saf. 2, 82-100.
3 Bai X, Byun Y, and Mah JH. 2013. Formation and destruction of biogenic amines in Chunjang (a black soybean paste) and Jajang (a black soybean sauce). Food Chem. 141, 1026-1031.   DOI
4 Beasley SS and Saris PEJ. 2004. Nisin-producing Lactococcus lactis strains isolated from human milk. J. Appl. Environ. Microbiol. 70, 5051-5053.   DOI
5 Bover-Cid S and Holzapfel WH. 1999. Improved screening procedure for biogenic amine production by lactic acid bacteria. Int. J. Food Microbiol. 53, 33-41.   DOI
6 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.   DOI
7 Byun BY, Lee AJ, and Mah JH. 2012. Occurrence of biogenic amines in Miso, Japanese traditional fermented soybean paste. J. Food Sci. 77, T216-T223.   DOI
8 Chang M and Chang HC. 2012. Development of a screening method for biogenic amine producing Bacillus spp. Int. J. Food Microbiol. 153, 269-274.   DOI
9 Cho TY, Han GH, Bahn KN, Son YW, Jang MR, and Lee CH. 2006. Evaluation of biogenic amines in Korean commercial fermented foods. Korean J. Food Sci. Technol. 38, 730-737.
10 Eerola S, Hinkkanen R, Lindfors E, and Hirvi T. 1993. Liquid chromatographic determination of biogenic amines in dry sausages. J. Assoc. Off. Anal. Chem. Int. 75, 575-577.
11 Gandevia HA, Rana ND, and Desai BA. 2017. Screening, production and antibacterial activity of bacteriocin from Lactobacillus sp. BMR Microbiol. 3, 1-8.
12 Ghanbari M, Jami M, Domig KJ, and Kneifel W. 2013. Seafood biopreservation by lactic acid bacteria-a review. LWT-Food Sci. Technol. 54, 315-324.   DOI
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 Hassaine O, Zadi-Karam H, and Karam NE. 2009. Evaluation of biogenic amines formation by proteolytic enterococci strains isolated from raw dromedary milks from Southern Algeria. J. Food Saf. 29, 381-393.   DOI
15 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.   DOI
16 Ibe A, Nishima T, and Kasai N. 1992. Bacteriological properties of and amine-production conditions for tyramine- and histamineproducing bacterial strains isolated from soybean paste (miso) starting materials. Jap. J. Toxicol. Environ. Health 38, 403-409.   DOI
17 Ladero V, Calles-Enriquez M, Fernandez M, and Alvarez MA. 2010. Toxicological effects of dietary biogenic amines. Curr. Nutr. Food Sci. 6, 145-156.   DOI
18 Joosten HMLJ and Nunez M. 1996. Prevention of histamine formation in cheese by bacteriocin-producing lactic acid bacteria. Appl. Environ. Microbiol. 62, 1178-1181.
19 Ju KE and Oh NS. 2009. Effect of the mixed culture of Bacillus subtilis and Lactobacillus plantarum on the quality of Chenonggukjang. Korean J. Food Sci. Technol. 41, 399-404.
20 Kashket ER. 1987. Bioenergetics of lactic acid bacteria: cytoplasmic pH and osmotolerance. FEMS Microbiol. Rev. 46, 233-244.   DOI
21 Lee GY, Kim SI, Jung MG, Seong JH, Lee YG, Kim HS, Chung HS, Lee BW, and Kim DS. 2014. Characteristics of Chungkookjang that enhance the flavor and GABA content in a mixed culture of Bacillus subtilis MC31 and Lactobacillus sakei 383. J. Life Sci. 24, 1102-1109.   DOI
22 Lee YC, Kung HF, Huang YL, Wu CH, Huang YR, and Tsai YH. 2016. Reduction of biogenic amines during miso fermentation by Lactobacillus plantarum as a starter culture. J. Food Prot. 79, 1556-1561.   DOI
23 Lee SY, Park NY, Kim JY, and Choi HS. 2012. Quality characteristics of rice-doenjang during fermentation by differently shaped meju and adding starter. Korean J. Food Nutr. 25, 505-512.   DOI
24 Leuschner RG, Heidel M, and Hammes WP. 1998. Histamine and tyramine degradation by food fermenting microorganisms. Int. J. Food Microbiol. 39, 1-10.   DOI
25 Lim ES. 2016. Microbiological and chemical properties of sourdough fermented with probiotic lactic acid bacteria. Korean J. Microbiol. 52, 84-97.   DOI
26 Mah JH, Ahn JB, Park JH, Sung HC, and Hwang HJ. 2003. Characterization of biogenic amine-producing microorganisms isolated from Myeolchi-Jeot, Korean salted and fermented anchovy. J. Microbiol. Biotechnol. 13, 692-699.
27 Lim ES. 2017. Incubation conditions affecting biogenic amines degradation of probiotic lactic acid bacteria. Korean J. Microbiol. 53, 273-285.
28 Lim ES and Lee NG. 2016. Control of histamine-forming bacteria by probiotic lactic acid bacteria isolated from fish intestine. Korean J. Microbiol. 52, 352-364.   DOI
29 Linares DM, Martin M, Ladero V, Alveraz MA, and Fernandez M. 2011. Biogenic amines in dairy products. Crit. Rev. Food Sci. Nutr. 51, 691-703.   DOI
30 Mah JH and Hwang HJ. 2009. Effect of food additives on biogenic amine formation in Myeolchi-jeot, a salted and fermented anchovy (Engraulis japonicas). Food Chem. 114, 168-173.   DOI
31 McCabe-Sellers BJ, Staggs CG, and Bogle ML. 2006. Tyramine in foods and monoamine oxidase inhibitor drugs: A crossroad where medicine, nutrition, pharmacy, and food industry converge. J. Food Compos. Anal. 19, S58-S65.   DOI
32 Moon JS, Cho SK, Choi HY, Kim JE, Kim SY, Cho KJ, and Han NS. 2010. Isolation and characterization of biogenic amine producing bacteria in fermented soybean pastes. J. Microbiol. 48, 257-261.   DOI
33 Naila A, Flint S, Fletcher G, Bremer P, and Meerdink G. 2010. Control of biogenic amines in food-existing and emerging approaches. J. Food Sci. 75, R139-R150.   DOI
34 Nout MJR, Ruiker MMW, Bouwmeester HM, and Beljaars PR. 1993. Effect of processing conditions on the formation of biogenic amines and ethyl carbamate in soybean tempe. J. Food Saf. 33, 293-303.
35 Seok YR, Kim YH, Kim S, Woo HS, Kim TW, Lee SH, and Choi C. 1994. Change of protein and amino acid composition during cheonggukjang fermentation using Bacillus licheniformis CN-115. J. Korean Soc. Appl. Biol. Chem. 37, 65-71.
36 Ozogul F, Toy N, Ozogul Y, and Hamed I. 2017. Function of cell-free supernatants of Leuconostoc, Lactococcus, Streptococcus, Pediococcus strains on histamine formation by foodborne pathogens in histidine decarboxylase broth. J. Food Process Preserv. 41, e13208.   DOI
37 Park YJ and Joo WH. 2017. Inhibition of biogenic amine production by Bacillus sp. BCNU 9171 isolated from Doenjang. Microbiol. Biotechnol. Lett. 45, 299-304.   DOI
38 Santos MH. 1996. Biogenic amines: their importance in foods. Int. J. Food Microbiol. 29, 213-231.   DOI
39 Sgouras D, Maragkoudakis P, Petraki K, Martine-Gonzalez B, Erioutou E, Michopoulas S, Kalantzopoulos G, Tsakalidou E, and Mentis A. 2004. In vitro and in vivo inhibition of Helicobacter pylori by Lactobacillus casei strains Shirota. Appl. Environ. Microbiol. 70, 518-526.   DOI
40 Shakila RJ, Vasundhara TS, and Rao DV. 1996. Inhibitory effect of spices on in vitro histamine production and histidine decarboxylase activity of Morganella morganii and on the biogenic amine formation in mackerel stored at 30 degrees C. Z. Lebensm. Unters. Forsch. 203, 71-76.   DOI
41 Shalaby AR. 1996. Significance of biogenic amines to food safety and human health. Food Res. Int. 29, 675-690.   DOI
42 Shon MY, Kwon SH, Sung CK, Park SK, and Choi SD. 2001. Changes in chemical components of Chungkugjang prepared with small black bean. Korean J. Life Sci. 11, 284-290.
43 Zaman MZ, Bakar FA, Jinap S, and Bakar J. 2011. Novel starter cultures to inhibit biogenic amines accumulation during fish sauce fermentation. Int. J. Food Microbiol. 145, 84-91.   DOI
44 Straub BW, Kicherer M, Schilcher SM, and Hammes WP. 1995. The formation of biogenic amines by fermentation organisms. Z. Lebensm. Unters. Forsch. 201, 79-82.   DOI
45 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.   DOI
46 Veskovic Moracanin S, Dukic DA, and Memisi NR. 2014. Bacteriocins produced by lactic acid bacteria-a review. APTEFF 45, 271-283.