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http://dx.doi.org/10.7845/kjm.2016.6041

Control of histamine-forming bacteria by probiotic lactic acid bacteria isolated from fish intestine  

Lim, Eun-Seo (Department of Food Science & Nutrition, Tongmyong University)
Lee, Nahm-Gull (Department of Food Science & Nutrition, Tongmyong University)
Publication Information
Korean Journal of Microbiology / v.52, no.3, 2016 , pp. 352-364 More about this Journal
Abstract
In this study, we examined in vitro the potential probiotic properties of lactic acid bacteria (LAB) obtained from the fish intestine and their ability to degrade histamine through the production of diamine oxidase (DAO) enzymes and bacteriocin. Among 97 LAB strains isolated from the intestine of croaker, flatfish, pollack, and rockfish, CIL08, CIL16, FIL20, FIL31, PIL45, PIL49, PIL52, and RIL60 isolates exhibited excellent survival rates under simulated gastrointestinal tract conditions, high adhesion ability to HT-29 epithelial cells, and resistance to the antibiotics such as amoxicillin, ampicillin, erythromycin, penicillin G, streptomycin, tetracycline, or vancomycin. In addition, these strains did not produce histamine in decarboxylating broth containing histidine. In particular, 4 strains (CIL08, FIL20, PIL52, and RIL60) that may produce DAO were significantly able to degrade histamine. The bacteriocins produced by FIL20, FIL31, and PIL52 LAB inhibited the growth and histamine production of Enterococcus aerogenes CIH05, Serratia marcescens CIH09, Enterococcus faecalis FIH11, Pediococcus halophilus FIH15, Lactobacillus sakei PIH16, Enterococcus faecium PIH19, Leuconostoc mesenteroides RIH25, or Aeromonas hydrophilia RIH28. Histamine-producing strains isolated from fish intestine were found to reduce histamine accumulation during co-culture with CIL08, FIL20, PIL52, and RIL60 LAB showing histamine degradation or bacteriocin production ability. The probiotic strains preventing histamine formation were identified as Pediococcus pentosaceus CIL08, Lactobacillus plantarum FIL20, Lactobacillus paracasei FIL31, Lactobacillus sakei PIL52, and Leuconostoc mesenteroides RIL60 with high similarity based on 16S rRNA gene sequencing.
Keywords
bacteriocin; histamine; lactic acid bacteria; probiotic;
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1 Yongjin, H., Wenshui, X., and Xiaoyong, L. 2007. Changes in biogenic amines in fermented silver carp sausages inoculated with mixed starter cultures. Food Chem. 104, 188-195.   DOI
2 Zaman, M.Z., Bakar, F.A., Selamat, J., and Bakar, J. 2010. Occurrence of biogenic amines and amines degrading bacteria in fish sauce. Czech. J. Food Sci. 28, 440-449.   DOI
3 Zaman, M.Z., Bakar, F.A., 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
4 Migaw, S., Ghrairi, T., Belguesmia, Y., Choiset, Y., Berjeaud, J.M., Chobert, J.M., Hani, K., and Haertle, T. 2014. Diverstiy of bacteriocinogenic lactic acid bacteria isolated from Mediterranean fish viscera. World J. Microbiol. Biotechnol. 30, 1207-1217.   DOI
5 Morii, H., Cann, D.C., and Taylor, L.Y. 1988. Histamine formation by luminous bacteria in mackerel stored at low temperatures. B. Jpn. Soc. Sci. Fish. 54, 299-305.   DOI
6 Murooka, Y., Doi, N., and Harada, T. 1979. Distribution of membrane bound monoamine oxidase in bacteria. Appl. Environ. Microbiol. 38, 565-569.
7 Musikasang, H., Sohsomboon, N., Tani, A., and Maneerat, S. 2012. Bacteriocin-producing lactic acid bacteria as a probiotic potential from Thai indigenous chickens. Czech J. Anim. Sci. 57, 137-149.   DOI
8 Chahad, O.B., Bour, M.E., Calo-Mata, P., Boudabous, A., and Barros-Velazquez, J. 2012. Discovery of novel biopreservation agents with inhibitory effects on growth of food-borne pathogens and their application to seafood products. Res. Microbiol. 163, 44-54.   DOI
9 Nirunya, B., Suphitchaya, C., and Tipparat, H. 2008. Screening of lactic acid bacteria from gastrointestinal tracts of marine fish for their potential use as probiotics. Songklanakarin J. Sci. Technol. 30, 141-147.
10 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
11 Nugrahani, A., Anik, H., and Hariati, M. 2016. Characterization of bacteriocin Lactobacillus casei on histamine-forming bacteria. J. Life Sci. Biomed. 6, 15-21.
12 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.
13 Chen, H.C., Kung, H.F., Chen, W.C., Lin W.F., Hwang, D.F., Lee Y.C., and Tsai, Y.H. 2008. Determination of histamine and histamine-forming bacteria in tuna dumpling implicated in a food-borne poisoning. Food Chem. 106, 612-618.   DOI
14 Cho, G.S., Do, H.K., Bae, C.Y., Cho, G.S., Whang, C.W., and Shin, H.K. 2006. Candidate of probiotic bacteria isolated from several jeotgals: Korean traditional fermented seafoods. J. Food Sci. Nutr. 11, 140-145.
15 Dapkevicius, M.L.N.E., Nout, M.J.R., Rombouts, F.M., Houben, J.H., and Wymenga, W. 2000. Biogenic amine formation and degradation by potential fish silage starter microorganisms. Int. J. Food Microbiol. 57, 107-114.   DOI
16 Garcia-Ruiz, A., Gonzalez-Rompinelli, E.M., Bartolome, B., and Moreno-Arribas, M.V. 2011. Potential of wine-associated lactic acid bacteria to degrade biogenic amines. Int. J. Food Microbiol. 148, 115-120.   DOI
17 Ghanbari, M., Jami, M., Domig, K.J., and Kneifel, W. 2009. Seafood biopreservation by lactic acid bacteria-A review. LWT-Food Sci. Technol. 54, 315-324.
18 Ghanbari, M., Rezaei, M., Jami, M., and Nazari, R.M. 2013. Isolation and characterization of Lactobacillus species from intestinal contents of beluga (Huso huso) and Persian sturgeon (Acipenser persicus). Iran. J. Vet. Res. 10, 152-157.
19 Ozogul, F. 2011. Effects of specific lactic acid bacteria species on biogenic amine production by foodborne pathogen. Int. J. Food Sci. Technol. 46, 478-484.   DOI
20 Osmanagaoglu, O., Kiran, F., and Ataoglu, H. 2010. Evaluation of in vitro probiotic potential of Pediococcus pentosaceus OZF isolated from human breast milk. Probiotics Antimicrob. Proteins 2, 162-174.   DOI
21 Priyadarshani, W.M.D. and Rakshit, S.K. 2011. Screening selected strains of probiotic lactic acid bacteria for their ability to produce biogenic amines (histamine and tyramine). Int. J. Food Sci. Technol. 46, 2062-2069.   DOI
22 Santos, M.H.S. 1996. Biogenic amines: their importance in foods. Int. J. Food Microbiol. 29, 213-231.   DOI
23 Shakila, R.J., Vasundhara, T.S., and Rao, D.V. 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
24 Shalaby, A.R. 1996. Significance of biogenic amines to food safety and human health. Food Res. Int. 29, 675-690.   DOI
25 Joosten, H.M. and Nunez, M. 1996. Prevention of histamine formation in cheese by bacteriocin-producing lactic acid bacteria. Appl. Environ. Microbiol. 62, 1178-1181.
26 Grimoud, J., Durand, H., Courtin, C., Monsan, P., Ouarne, F., Theodorou, V., and Roques, C. 2010. In vitro screening of probiotic lactic acid bacteria and prebiotic glucooligosaccharides to select effective synbiotics. Anaerobe 16, 493-500.   DOI
27 Straub, B.W., Kicherer, M., Schilcher, S.M., and Hammes, W.P. 1995. The formation of biogenic amines by fermentation organisms. Z. Lebensm. Unters. Forsch. 201, 79-82.   DOI
28 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
29 Gomez-Sala, B., Munoz-Atienza, E., Sanchez, J., Basanta, A., Herranz, C., Hernandez, P.E., and Cintas, L.M. 2015. Bacteriocin production by lactic acid bacteria isolated from fish, seafood and fish products. Eur. Food Res. Technol. 241, 341-356.   DOI
30 Holo, H., Nilssen, O., and Nes, I.F. 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
31 Kim, M.W. and Kim, Y.M. 2006. Isolation and identification of histamine degrading bacteria from Kwamegi. Kor. J. Life Sci. 16, 120-125.   DOI
32 Kim, M.K., Mah, J.H., and Hwang, H.J. 2009. Biogenic amine formation and bacteria contribution in fish, squid and shellfish. Food Chem. 116, 87-95.   DOI
33 Klaenhammer, T.R. 1993. Genetics of bacteriocins produced by lactic acid bacteria. FEMS Microbiol. Rev. 12, 39-86.   DOI
34 Leuschner, R.G., Heidel, M., and Hammes, W.P. 1998. Histamine and tyramine degradation by food fermenting microorganisms. Int. J. Food Microbiol. 39, 1-10.   DOI
35 Kongkiattikajorn, J. 2015. Potential of starter culture to reduce biogenic amines accumulation in som-fug, a Thai traditional fermented fish sausage. J. Ethn. Foods 2, 186-194.   DOI
36 Lakshamanan, R., Shakila, R.J., and Jeyasekaran, G. 2002. Survival of amine-forming bacteria during the ice storage of fish and shrimp. Food Microbiol. 19, 617-625.   DOI
37 Lee, Y.C., Lin, C.S., Liu, F.L., Huang, T.C., and Tsai, Y.H. 2015. Degradation of histamine by Bacillus polymyxa isolated from salted fish products. J. Food Drug Anal. 23, 836-844.   DOI
38 Linares, D.M., Martin, M.C., Ladero, V., Alvarez, M.A., and Fernandez, M. 2011. Biogenic amines in dairy products. Crit. Rev. Food Sci. 51, 691-703.   DOI
39 Ten Brink, B., Damink, C., Joosten, H.M.L., and Veld, J.H.J. 1990. Occurrence and formation of biologically active amines in foods. Int. J. Food Microbiol. 11, 73-84.   DOI
40 Tajabadi, N., Mardan, M., Saari, N., Mustafa, S., Bahreini, R., and Manap, M.Y.A. 2013. Identification of Lactobacillus plantarum, Lactobacillus pentosus and Lactobacillus fermentum from honey stomach of honeybee. Braz. J. Microbiol. 44, 717-722.   DOI
41 Thiruneelakandan, G., Sesuraj, V.J., Babu, V., Senthikumar, V., Kathiresan, K., Sivakami, R., and Anthoni, S.A. 2013. Efficacy of preserving sea foods using marine Lactobacillus. Sci. Technol. Arts Res. J. 2, 10-13.   DOI
42 Bover-Cid, S. and Holzapfel, W.H. 1999. Improved screening procedure for biogenic amine production by lactic acid bacteria. Int. J. Food Microbiol. 52, 33-41.
43 Mah, J.H., Ahn, J.B., Park, J.H., Sung, H.C., and Hwang, H.J. 2003. Characterization of biogenic amine-producing microorganisms isolated from Myeolchi-Jeot, Korean salted and fermented anchovy. J. Microbiol. Biotechnol. 13, 692-699.
44 Mah, J.H. and Hwang, H.J. 2009. Inhibition of biogenic amine formation in a salted and fermented anchovy by Staphylococcus xylosus as a protective culture. Food Control 114, 168-173.
45 Maijala, R.L., Erola, S.H., Aho, M.A., and Hirn, J.A. 1993. The effect of GDL-induced pH decrease on the formation of biogenic amines in meat. J. Food Prot. 50, 125-129.
46 Todorov, S.D., Furtado, D.N., Saad, S.M.I., Tome, E., and Franco, B.D.G.M. 2011. Potential beneficial properties of bacteriocinproducing lactic acid bacteria isolated from smoked salmon. J. Appl. Microbiol. 110, 971-986.   DOI
47 Visciano, P., Schirone, M., Tofalo, R., and Suzzi, G. 2012. Biogenic amines in raw and processed seafood. Front. Microbiol. 3, 1-10.
48 Middlebrooks, B.L., Toom, P.M., Douglas, W.L., Harrison, R.E., and Mcdowell, S. 1988. Effects of storage time and temperature on the microflora and amine development in Spanish mackerel (Scoberomorus maculatus). J. Food Sci. 53, 1024-1029.   DOI
49 Balcazar, J.L., Vendrell, D., De Blas, I., and Ruiz-Zarzuela, I. 2008. Characterization of probiotic properties of lactic acid bacteria from intestinal microbiota of fish. Aquacuture 278, 188-191.   DOI
50 Allameh, S.K., Daud, H., Yusoff, F.M., Saad, C.R., and Ideris, A. 2012. Isolation, identification and characterization of Leuconostoc mesenteroides as a new probiotic from intestine of snakehead fish (Channa Striatus). Afr. J. Biotechnol. 11, 3810-3816.
51 Bajpai, V.K., Han, J.H., Nam, G.J., Majumder, R., Park, C.S., Lim, J.H., Paek, W.K., Rather, I.A., and Park, Y.H. 2016. Characterization and pharmacological potential of Lactobacillus sakei 111 isolated from fresh water fish Zacco koreanus. DARU J. Pharm. Sci. 24, 1-12.   DOI