FERMENTE SUCUKTAN İZOLE EDİLEN MUNDTİSİN KS ÜRETİCİSİ ENTEROCOCCUS MUNDTII YB6.30 SUŞUNUN TEKNOLOJİK ÖZELLİKLERİ VE GÜVENLİK DEĞERLENDİRMESİ

Year 2019, , 866 - 880, 17.08.2019

Melike Kasap , Yasin Tuncer

https://doi.org/10.15237/gida.GD19090

Abstract

Bu çalışmada, mundtisin KS üreticisi Enterococcus mundtii YB6.30 suşunun
teknolojik özellikleri ve güvenlik değerlendirmesinin fenotipik ve genotipik
yöntemler ile araştırılması amaçlanmıştır. E.
mundtii YB6.30 suşunun de Man, Rogosa and Sharpe broth ortamında,
yapılandırılmış yağsız süt ortamına göre daha hızlı asit üretim özelliği
gösterdiği belirlenmiştir. E. mundtii
YB6.30 suşunun proteolitik aktivite gösterdiği ve nitratı redükte ettiği fakat
lipolitik aktivite göstermediği tespit edilmiştir. YB6.30 suşu denemelerde
kullanılan antibiyotiklerin tamamına duyarlı bulunmuştur. Fenotipik testler
sonucu YB6.30 suşunun hemolitik aktivite ve jelatinaz aktivitesi göstermediği
belirlenmiştir. Polimeraz zincir reaksiyonu (PZR) ile YB6.30 suşunun virülens
faktör içermediği tespit edilmiştir. YB6.30 suşu histidin, lisin ve ornitini
dekarboksile edemez iken, tirozinden tiramin ürettiği belirlenmiştir. PZR
denemeleri sonucu YB6.30 suşunda yalnız tirozin dekarboksilaz (tdc) geni varlığı tespit edilmiştir. Bu
çalışmanın sonuçları mundtisin KS üreticisi E.
mundtii YB6.30 suşunun gıda endüstrisinde starter kültür olarak
kullanımının güvenli olduğunu göstermiştir.

Keywords

Enterococcus mundtii, sucuk, mundtisin KS, teknolojik özellikler, güvenlik değerlendirmesi

Supporting Institution

Süleyman Demirel Üniversitesi Bilimsel Araştırma Projeleri Yönetim Birimi

Project Number

FYL-2018-5765

Thanks

Bu çalışmayı FYL-2018-5765 nolu proje ile maddi olarak destekleyen Süleyman Demirel Üniversitesi Bilimsel Araştırma Projeleri Yönetim Birimi’ne teşekkür ederiz.

TECHNOLOGICAL PROPERTIES AND SAFETY EVALUATION OF MUNDTICIN KS PRODUCER ENTEROCOCCUS MUNDTII YB6.30 STRAIN ISOLATED FROM FERMENTED SUCUK

Abstract

In this study, investigation of
technological properties and safety evaluation of mundticin KS producer Enterococcus mundtii YB6.30 by
phenotypic and genotypic methods were aimed. E. mundtii YB6.30 strain has been determined to show a faster acid
production properties in de Man, Rogosa and Sharpe broth than reconstituted
skim milk. E. mundtii YB6.30 strain
showed proteolytic activity and reduced nitrate but not showed lipolytic
activity. The YB6.30 strain was found to be sensitive to all antibiotics used
in this study. As a result of phenotypic tests, YB6.30 strain did not show
hemolytic and gelatinase activities. The YB6.30 strain was not found to contain
virulence factor genes using polymerase chain reaction (PCR). The YB6.30 strain
was found to produce tyramine from tyrosine while it did not decarboxylate
histidine, lysine and ornithine. As a result of PCR experiment, only tyrosine
decarboxylase gene (tdc) was detected
in YB6.30 strain. The results of this study showed that mundticin KS producer E. mundtii YB6.30 strain was safe to use
as a starter culture in the food industry.

Keywords

Enterococcus mundtii, sucuk, mundticin KS, technological properties, safety evaluation

Project Number

FYL-2018-5765

References

• Ahn, H.J., Kim, J.H., Jo, C., Lee, J.W., Yook, H.S., Byun, M.W. (2004). Combined effects of gamma irradiation and a modified atmospheric packaging on the physicochemical characteristics of sausage. Radiat Phys Chem, 71(1-2), 53-56.
• Ambadoyiannis, G., Hatzikamari, M., Litopoulou-Tzanetaki, E., Tzanetakis, N. (2004). Probiotic and technological properties of enterococci isolates from infants and cheese. Food Biotechnol, 18 (3), 307-325.
• Ammor, M.S., Mayo, B. (2007). Selection criteria for lactic acid bacteria to be used as functional starter cultures in dry sausage production: an update. Meat Science, 76(1), 138-146.
• Anagnostopoulos, D., Bozoudi, D., Tsaltas, D. (2018). Enterococci isolated from cypriot green table olives as a new source of technological and probiotic properties. Fermentation, 4(2), 48.
• Aspri, M., Bozoudi, D., Tsaltas, D., Hill, C., Papademas, P. (2016). Raw donkey milk as a source of Enterococcus diversity: assessment of their technological properties and safety characteristics. Food Control, 73, 81-90.
• Avcı, M., Özden Tuncer, B. (2017). Safety evaluation of enterocin producer Enterococcus sp. strains isolated from traditional Turkish cheeses. Pol J Microbiol, 2, 223-233.
• Ayad, E.H.E., Nashat, S., El-Sadek, N., Metwaly, H., El-Soda, M. (2004). Selection of wild lactic acid bacteria isolated from traditional Egyptian dairy products according to production and technological criteria. Food Microbiol, 21(6), 715-725.
• Banwo, K., Sanni, A., Tan, H. (2013). Technological properties and probiotic potential of Enterococcus faecium strains isolated from cow milk. J Appl Microbiol, 114(1), 229-241.
• Barbieri, F., Montanari, C., Gardini, F., Tabanelli, F. (2019). Biogenic amine production by lactic acid bacteria: a review. Foods, 8, 17. doi:10.3390/foods8010017
• Ben Belgacem, Z., Abriouel, H., Omar, N.B., Lucas, R., Martínez-Canamero, M., Gálvez, A., Manai, M. (2010). Antimicrobial activity, safety aspects and some technological properties of bacteriocinogenic Enterococcus faecium from artisanal Tunisian fermented meat. Food Control, 21(4), 462-470.
• Bover-Cid, S., Holzapfel, W.H. (1999). Improved screening procedure for biogenic amine production by lactic acid bacteria. Int J Food Microbiol, 53(1), 33-41.
• Bradley, R.L., Arnold, E., Barbano, D.M., Semerad, R.G., Smith, D.E., Vines, B.K. (1992). Chemical and physical methods. In: Standart Methods for The Examination of Dairy Products. Marshall, T. (ed), American Public Healt Association, Washington Dc, pp. 433-531.
• Camargo, I.L.B.C., Gilmore, M.S., Darini, A.L.C. (2006). Multilocus sequence typing and analysis of putative virulence factors in vancomycin-resistant and vancomycin-sensitive Enterococcus faecium isolates from Brazil. Clin Microbiol Infect, 12(11), 1123-1130.
• Cancilla, M.R., Powell, I.B., Hillier, A.J., Davidson, B.E. (1992). Rapid genomic fingerprinting of Lactococcus lactis strains by arbitrarily primed polymerase chain reaction with 32P and fluorescent labels. Appl Environ Microbiol, 58(5), 1772-1775.
• Čanigová, M., Ducková, V., Lavová, M., Bezeková, J., Kročko, M. (2016). Selected technological properties and antibiotic resistance of enterococci isolated from milk. Potravinarstvo, Potr. S. J. F. Sci., 10(1), 518-523.
• Cariolato, D., Andrighetto, C., Lombardi, A. (2008). Occurrence of virulence factors and antibiotic resistances in Enterococcus faecalis and Enterococcus faecium collected from dairy and human samples in North Italy. Food Control, 19(9), 886-892.
• Chajęcka-Wierzchowska, W., Zandernowska, A., Łaniewska-Trokenheim, Ł. (2017). Virulence factors of Enterococcus spp. presented in food. LWT-Food Sci Technol, 75, 670-676.
• Clinical and Laboratory Standards Institute, (CLSI 2016). Performance Standards for Antimicrobial Susceptibility Testing; Twenty-Fifth Informational Supplement M100-S26 CLSI, Wayne, PA.
• Cogan, B.T.M., Barbosa, M., Beuvier, E., BianchiSalvadori, B., Cocconcelli, P.S., Fernandes, I., Gomez, J., Gomez, R., Kalantzopoulos, G., Ledda, A., Medina, M., Rea, M.C., Rodriguez, E. (1997). Characterization of the lactic acid bacteria in artisanal dairy products. J Dairy Res, 64, 409-421. de Las Rivas, B., Marcobal, A., Carrascosa, A.V., Munoz, R. (2006). PCR detection of foodborne bacteria producing the biogenic amines histamine, tyramine, putrescine and cadaverine. J Food Protect, 69(10), 2509-2514.
• Durlu-Ozkaya, F., Xanthopoulos, V., Tunail, N., Litopoulou-Tzanetaki, E. (2001). Technologically important properties of lactic acid bacteria isolates from beyaz cheese made from raw ewes’ milk. J Appl Microbiol, 91(5), 861-870.
• Dworniczek, E., Kuzko, K., Mróz, E., Wojciech, Ł., Adamski, R., Sobieszczańska, B., Seniuk, A. (2003). Virulence factors and in vitro adherence of Enterococcus strains to urinary datheters. Folia Microbiol, 48(5), 671-678.
• Eaton, T.J., Gasson, M.J. (2001). Molecular screening of Enterococcus virulence determinants and potential for genetic ort he between food and medical isolates. Appl Environ Microbiol, 67(4), 1628-1635.
• Essid, I., Ben Ismail, H., Bel Hadj Ahmed, S., Ghedamsi, R., Hassouna, M. (2007). Characterization and technological properties of Staphylococcus xylosus strains isolated from a Tunisian traditional salted meat. Meat Sci. 77(2), 204-212.
• Foulquié Moreno, M., Sarantinopoulos, P., Tsakalidou, E., De Vuyst, L. (2006). The role and application of enterococci in food and health. Int J Food Microbiol, 106(1), 1-24.
• Franz, C.M.A.P., Holzapfel, W.H., Stiles, M.E. (1999). Enterococci at the crossroads of food safety?. Int J Food Microbiol, 47(1-2), 1-24.
• Franz, C.M.A.P., Muscholl-Silberhorn, A.B., Yousif, N.M.K., Vancanneyt, M., Swings, J., Holzapfel, W. (2001). Incidence of virulence factors and antibiotic resistance among enterococci isolated from food. Appl Environ Microbiol, 67(9), 4385-4389.
• García-Solache, M., Rice, L. B. (2019). The Enterococcus: a model of adaptability to its environment. Clin Microbial Rev, 32:e00058-18.
• Giraffa, G. (1995). Enterococcal bacteriocins: their potential as anti-listeria factors in dairy technology. Food Microbiol, 12, 291-299.
• Giraffa, G. (2003). Functionality of enterococci in dairy products. Int J Food Microbiol, 88(2-3), 215-222.
• Gomes, B.C., Esteves, C.T., Palazzo, I.C.V., Darini, A.L.C., Felis, G.E., Sechi, L.A., Franco, B.D.G.M., De Martinis, E.C.P. (2008). Prevalence and characterization of Enterococcus spp. isolated from Brazilian foods. Food Microbiol, 25(5), 668-675.
• Gök Charyyev, M., Özden Tuncer, B., Akpınar Kankaya, D., Tuncer, Y. (2019). Bacteriocinogenic properties and safety evaluation of Enterococcus faecium YT52 isolated from boza, a traditional cereal based fermented beverage. J Verbrauch Lebensm, 14 (1), 41-53.
• Inoğlu, Z.N., Tuncer, Y. (2013). Safety assessment of Enterococcus faecium and Enterococcus faecalis strains isolated from Turkish tulum cheese. J Food Safety, 33(3), 369-377.
• Jaouani, I., Abbassi, M.S., Ribeiro, S.C., Khemiri, M., Mansouri, R., Messadi, L., Silva, C.C.G. (2015). Safety and technological properties of bacteriocinogenic enterococci isolates from Tunisia. J Appl Microbiol, 119(4), 1089-1100.
• Kalhotka, L., Manga, I., Přichystalová, J., Hůlová, M,. Vyletělová, M., Šustová K. (2012). Decarboxylase activity test of the genus Ente¬rococcus isolated from goat milk and cheese. Acta Vet Brno, 81(2), 145-151.
• Kanematsu, E., Deguchi, T., Yasuda, M., Kawamura, T., Nishino, Y., Kawada, Y. (1998). Alterations in the GyrA subunit of DNA gyrase and the ParC subunit of DNA topoisomerase IV associated with quinolone resistance in Enterococcus faecalis. Antimicrob Agents Chemother, 42(2), 433-435.
• Klare, I., Werner, G., Witte, W. (2001). Enterococci. Habitats, infections, virulence factors, resistances to antibiotics, transfer of resistance determinants. Contrib Microbiol, 8, 108- 122.
• Kucerová, K., Svobodová, H., Tůma, Š., Ondrácková, I., Plocková, M. (2009). Production of biogenic amines by enterococci. Czech J Food Sci, 27(2), 50-55.
• Landeta, G., Curiel, J.A., Carrascosa, A.V., Muñoz, R., de Las Rivas, B. (2013). Technological and safety properties of lactic acid bacteria isolated from Spanish dry-cured sausages. Meat Sci. 95(2), 272-280.
• Lee, K. (2005). A media design program for lactic acid production coupled with extraction by electrodialysis. Bioresour Technol, 96(13), 1505-1510.
• Liu, D.C., Wu, S.W., Tan, F.J. (2010). Effects of addition of anka rice on the qualities of low-nitrite Chinese sausages. Food Chem, 118(2), 245-250.
• Manavalan. J., Kannaiyan, K., Velatyutham, A., Vadivel, S., Kuthalaramalingam, S. (2015). Phenotypic speciation of enterococci with special reference to prevalence, virulence and antimicrobial resistance. Int J Res Med Sci, 3(10), 2623-2629.
• Martín, B., Garriga, M., Hugas, M., Bover-Cid, S., Veciana-Nogués, M.T., Aymerich, T. (2006). Molecular, technological and safety characterization of Gram-positive catalase-positive cocci from slightly fermented sausages. Int J Food Microbiol, 107(2), 148-158.
• Miralles, M.C., Flores, J., Perez-Martinez, G. (1996). Biochemical test ort he selection of Staphylococcus strains as potential meat starter cultures. Food Microbiol, 13(3), 227-236.
• Morandi, S., Brasca, M., Andrighetto, C., Lombardi, A., Lodi, R. (2006). Technological and molecular characterisation of enterococci isolated from North–West Italian dairy products. Intl Dairy J, 16(8), 867-875.
• Mundy, L.M., Sahm, D.F., Gilmore, M. (2000). Relationship between enterococcal virulence and antimicrobial resistance. Clin Microbiol Rev, 13(4), 513-522.
• Ogier, J.C., Serror, P. (2008). Safety assesment of dairy microorganisms: The Enterococcus genus. Int J Food Microbiol, 126(3), 291-301.
• Oladipo, C.I., Sanni, A., Chakraborty, W., Chakraborty, S., Jana, S., Rudra, D.S., Gacchui, R., Swarnakar, S. (2015). Technological properties of strains of Enterococcus gallinarum isolated from selected Nigerian traditional fermented foods. Malays J Microbiol, 11(1), 1-13.
• Özden Tuncer, B., Ay, Z., Tuncer, Y. (2013). Occurrence of enterocin genes, virulence factors, and antibiotic resistance in 3 bacteriocin-producer Enterococcus faecium strains isolated from Turkish tulum cheese. Turk J Biol, 37(4), 443-449.
• Özkalp, B., Özden, B., Tuncer, Y., Şanlibaba, P., Akçelik, M. (2007). Technological characterization of wild-type Lactococcus lactis strains isolated from raw milk and traditional fermented milk products in Turkey. Le Lait, 87(6), 521-534.
• Reviriego, C., Eaton, T., Martín, R., Jiménez, E., Fernández, L., Gasson, M.J., Rodríguez, J.M. (2005). Screening of virulence determinants in Enterococcus faecium strains isolated from breast milk. J Hum Lact, 21(2), 131-137.
• Reyes, K., Zervos, M., John, J. (2017). Enterococcal infections in adults. In: Antimicrobial Drug Resistance. Mayers, D.L., Sobel, J.D., Ouellette, M., Kaye, K.S., Marchaim, D. (eds), Clinical and Epidemiological Aspects, Volume 2, Springer International Publishing, Berlin, pp. 811-818.
• Ribeiro, S.C., Coelho, M.C., Todorov, S.D., Franco, B.D.G.M., Dapkevicius, M.L.E., Silva, C.C.G. (2014). Technological properties of bacteriocin producing lactic acid bacteria isolated from Pico cheese an artisanal cow’s milk cheese. J Appl Microbiol, 116(3), 573-585.
• Sarantinopoulos, P., Andrighetto, C., Georgalaki, M.D., Rea, M.C., Lombardi, A., Cogan, T. M., Kalantzopoulos, G., Tsakalidou, E. (2001). Biochemical properties of enterococci relevant to their technological performance. Int Dairy J, 11(8), 621-647.
• Serio, A., Chaves-López, C., Paparella, A., Suzzi, G. (2010). Evaluation of metabolic activities of enterococci isolated from Pecorino Abruzzese cheese. Int Dairy J, 20(7), 459-464.
• Singh, K.V., Qin, X., Weinstock, G.M., Murray, B.E. (1998). Generation and testing of mutants of Enterococcus faecalis in ort peritonitis model. J Infect Dis, 178(5), 1416-1420.
• Trivedi, K., Cupakova, S., Karpiskova, R. (2011). Virulence factors and antibiotic resistance in enterococci isolated from food-stuffs. Vet Med-Czech, 56 (7), 352-357.
• Tuncer, M., Özden Tuncer, B., Tuncer, Y. (2014). Çiğ sütten izole edilen enterosin B üreticisi Enterococcus faecalis MYE58 suşunun güvenlik değerlendirmesi. Gıda, 39(5), 275-282.
• Tuncer, Y. (2009). Some technological properties of phenotypically identified enterococci strains isolated from Turkish tulum cheese. Afr J Biotechnol, 8(24), 7008-7016.
• Valenzuela, A.S., Ben Omar, N., Abriouel, H., López, R.L., Veljovic, K., Cañamero, M.M., Topisirovic, M.K.T., Gálvez, A. (2009). Virulence factors, antibiotic resistance, and bacteriocins in enterococci from artisan foods of animal origin. Food Control, 20(4), 381-385.
• Vankerckhoven, V., Autgaerden, T.V., Vael, C., Lammens, C., Chapelle, S., Rossi, R., Jabes, D., Goossens, H. (2004). Development of a multiplex PCR ort he detection of asa1, gelE, cylA, esp, and hyl genes in enterococci and survey for virulence determinants among European hospital isolates of Enterococcus faecium. J Clin Microbiol, 42(10), 4473-4479.
• Yogurtcu, N.N., Tuncer, Y. (2013). Antibiotic susceptibility patterns of Enterococcus strains isolated from Turkish tulum cheese. Int J Dairy Technol, 66, 236-242.
• Yüceer, Ö., Özden Tuncer, B. (2015). Determination of antibiotic resistance and biogenic amine production of lactic acid bacteria isolated from fermented Turkish sausage (Sucuk). J Food Safety, 35(2), 276-285.
• Zommiti, M., Cambronel, M., Maillot, O., Barreau, M., Sebei, K., Feuilloley, M., Ferchichi, M., Connil, N. (2018). Evaluation of probiotic properties and safety of Enterococcus faecium isolated from artisanal Tunisian meat “Dried Ossban. Front Microbiol, 9, 1685.