Enterococcus faecium in artisanal ripening cheese: technological and safety aspects
DOI:
https://doi.org/10.33448/rsd-v9i11.9452Keywords:
Drug sensitivity; Antagonistic activity; Fermentation.Abstract
The aims of this work were to identify and characterize for some important technological properties of the E. faecium throughout the ripening process of cheese. The study involved evaluating the technological potential of six isolates of E. faecium (EFM55, EFM67, EFM9A, EFM16A, EFM19A and EFM44) from artisanal cheeses as their probiotic characteristics and technological perspective. Concerning the antimicrobial sensibility, 71% of the E. faecium tested were sensitive to all antimicrobials. No other medicine inhibited the active of E. faecium, with the exception of dipyrone for the EFM19A and EFM9A strains. The isolates showed good antagonistic activity against gram-negative, as EFM9A, EFM55 and EFM67 strais with better activity. The highest fermentation was observed in 42 ºC, showed the pH variation of 4.15 to 5.15, after 48 hours of fermentation. All isolates showed pH reduction at 20 ºC. However, all isolates produced higher titratable acidity at a temperature of 42ºC. The isolates EFM55 and EFM9A has had probiotic actived, biochemical and susceptibility parameters desirables, aim it’s technological potential in the production of dairy products.
References
Acuña, L., Picariello, G., Sesma, F., Morero, R. D., & Bellomio, A. (2012). A new hybrid bacteriocin, Ent35-MccV, displays antimicrobial activity against pathogenic Gram-positive and Gram-negative bacteria. FEBS Open Bio, 2, 12–19. https://doi.org/10 .1016/j.fob.2012.01.002
Anderson, A. C., Andisha, H., Hellwig, E., Jonas, D., Vach, K., & Al-Ahmad, A. (2018). Antibiotic resistance genes and antibiotic susceptibility of oral enterococcus faecalis isolates compared to isolates from hospitalized patients and food. In Advances in Experimental Medicine and Biology (Vol. 1057, pp. 47–62). https://doi.org/10.1007/5584_2017_53
Andrighetto, C., Knijff, E., Lombardi, A., Torriani, S., Vancanneyt, M., Kersters, K., Swings, J., & Dellaglio, F. (2001). Phenotypic and genetic diversity of enterococci isolated from Italian cheeses. Journal of Dairy Research, 68(2), 303–316. https://doi.org/10.1017/S0022029901004800
AOAC – Association of Official Analytical Chemists. (2003). Official methods of analysis of the Association of Official. Analytical Chemistry. 17. ed. Washington: AOAC, v. 1 e 2
Badarinath, V., & Halami, P. M. (2011). Purification of new β-galactosidase from enterococcus faecium mtcc 5153 with transgalactosylation activity. Food Biotechnology, 25(3), 225–239. https://doi.org/10.1080/08905436.2011.590766
Ben Braïek, O., Ghomrassi, H., Cremonesi, P., Morandi, S., Fleury, Y., Le Chevalier, P., Hani, K., Bel Hadj, O., & Ghrairi, T. (2017). Isolation and characterisation of an enterocin P-producing Enterococcus lactis strain from a fresh shrimp (Penaeus vannamei). Antonie van Leeuwenhoek, International Journal of General and Molecular Microbiology, 110(6), 771–786. https://doi.org/10.1007/s10482-017-0847-1
De Vuyst, L., & Leroy, F. (2007). Bacteriocins from lactic acid bacteria: Production, purification, and food applications. Journal of Molecular Microbiology and Biotechnology, 13(4), 194–199. https://doi.org/10.1159/000104752
Dunne, C., O’Mahony, L., Murphy, L., Thornton, G., Morrissey, D., O’Halloran, S., Feeney, M., Flynn, S., Fitzgerald, G., Daly, C., Kiely, B., O’Sullivan, G. C., Shanahan, F., & Collins, J. K. (2001). In vitro selection criteria for probiotic bacteria of human origin: Correlation with in vivo findings. American Journal of Clinical Nutrition, 73(2 SUPPL.), 386S-392S. https://doi.org/10.1093/ajcn/73.2.386s
El-Garhi, H. E. M., El-Aidie, S. A. M., Rashid, N. A., & Hayee, Z. A. (2018). Quality improvement of spreadable processed cheese made from ultrafiltered milk retentates using commercial starter cultures. Food Science and Technology International, 24(6), 465–475. https://doi.org/10.1177/1082013218766979
El-Ghaish, S., Dalgalarrondo, M., Choiset, Y., Sitohy, M., Ivanova, I., Haertlé, T., & Chobert, J. M. (2010). Screening of strains of Lactococci isolated from Egyptian dairy products for their proteolytic activity. Food Chemistry, 120(3), 758–764. https://doi.org/10.1016/j.foodchem.2009.11.007
Elmoslih, A., Zanzan, M., Aissa, R., Hamadi, F., Baddi, G., Aoumar, A., & Achemchem, F. (2017). Isolation and Characterization of Bacteriocinogenic Enterococcal and Lactococcal Strains from South of Morocco Dairy Product. Biotechnology Journal International, 18(4), 1–16. https://doi.org/10.9734/bji/2017/32919
Fernández, M., Hudson, J. A., Korpela, R., & De Los Reyes-Gavilán, C. G. (2015). Impact on human health of microorganisms present in fermented dairy products: An overview. BioMed Research International, 2015(ID 412714), 13 p. https://doi.org/10.1155/2015/412714
Foulquié Moreno, M. R., Sarantinopoulos, P., Tsakalidou, E., & De Vuyst, L. (2006). The role and application of enterococci in food and health. International Journal of Food Microbiology, 106(1), 1–24. https://doi.org/10.1016/j.ijfoodmicro.2005.06.026
Franz, C. M. A. P., Muscholl-Silberhorn, A. B., Yousif, N. M. K., Vancanneyt, M., Swings, J., & Holzapfel, W. H. (2001). Incidence of Virulence Factors and Antibiotic Resistance among Enterococci Isolated from Food. Applied and Environmental Microbiology, 67(9), 4385–4389. https://doi.org/10.1128/AEM.67.9.4385-4389.2001
Furlaneto Maia, L., Giazzi, A., Brandalize, C., Katsuda, M. S., Rocha, K. R., Terra, M. R., & Furlaneto, M. C. (2017). Isolation and characterization of potential probiotic enterococci strains from soft cheese flora. African Journal of Microbiology Research, 11(12), 482–487. https://doi.org/10.5897/ajmr2017.8429
García, M. T., Martínez Cañamero, M., Lucas, R., Omar, N. Ben, Pérez Pulido, R., & Gálvez, A. (2004). Inhibition of Listeria monocytogenes by enterocin EJ97 produced by Enterococcus faecalis EJ97. International Journal of Food Microbiology, 90(2), 161–170. https://doi.org/10.1016/S0168-1605(03)00051-5
Giraffa, G. (2002). Enterococci from foods. FEMS Microbiology Reviews, 26(2), 163–171. https://doi.org/10.1016/S0168-6445(02)00094-3
Giraffa, G. (2003). Functionality of enterococci in dairy products. International Journal of Food Microbiology, 88(2–3), 215–222. https://doi.org/10.1016/S0168-1605(03)00183-1
Hankin, L., & Anagnostakis, S. L. (1975). The Use of Solid Media for Detection of Enzyme Production by Fungi. Mycologia, 67(3), 597. https://doi.org/10.2307/3758395
İspirli, H., Demirbaş, F., & Dertli, E. (2017). Characterization of functional properties of Enterococcus spp. isolated from Turkish white cheese. LWT - Food Science and Technology, 75, 358–365. https://doi.org/10.1016/j.lwt.2016.09.010
Moreno, M. R. F., Rea, M. C., Cogan, T. M., & De Vuyst, L. (2003). The role and application of enterococci in food and health. International Journal of Food Microbiology, 106(1), 1–24.
Nami, Y., Bakhshayesh, R. V., Jalaly, H. M., Lotfi, H., Eslami, S., & Hejazi, M. A. (2019). Probiotic properties of enterococcus isolated from artisanal dairy products. Frontiers in Microbiology, 10(FEB), 13 p. https://doi.org/10.3389/fmicb.2019.00300
Nguyen, Y., & Sperandio, V. (2012). Enterohemorrhagic E. coli (EHEC) pathogenesis. Frontiers in Cellular and Infection Microbiology, 2(July), 90. https://doi.org/10.3389/fcimb.2012.00090
Nueno-Palop, C., & Narbad, A. (2011). Probiotic assessment of Enterococcus faecalis CP58 isolated from human gut. International Journal of Food Microbiology, 145(2–3), 390–394. https://doi.org/10.1016/j.ijfoodmicro.2010.12.029
Ogaki, M. B., Rocha, K. R., Terra, M. R., Furlaneto, M. C., & Furlaneto-Maia, L. (2016). Screening of the enterocin-encoding genes and antimicrobial activityin Enterococcus species. Journal of Microbiology and Biotechnology, 26(6), 1026–1034. https://doi.org/10.4014/jmb.1509.09020
Ogier, J. C., & Serror, P. (2008). Safety assessment of dairy microorganisms: The Enterococcus genus. International Journal of Food Microbiology, 126(3), 291–301. https://doi.org/10.1016/j.ijfoodmicro.2007.08.017
Öncül, N., & Yıldırım, Z. (2019). Inhibitory effect of bacteriocins against Escherichia coli O157:H7. Food Science and Technology International, 25(6), 504–514. https://doi.org/10.1177/1082013219840462
Ozturkoglu-Budak, S., Wiebenga, A., Bron, P. A., & de Vries, R. P. (2016). Protease and lipase activities of fungal and bacterial strains derived from an artisanal raw ewe’s milk cheese. International Journal of Food Microbiology, 237(21), 17–27. https://doi.org/10.1016/j.ijfoodmicro.2016.08.007
Perin, L. M., Miranda, R. O., Camargo, A. C., Colombo, M., Carvalho, A. F., & Nero, L. A. (2013). Antimicrobial activity of the nisin Z producer Lactococcus lactis subsp. lactis lc08 against listeria monocytogenes in skim milk. Arquivo Brasileiro de Medicina Veterinaria e Zootecnia, 65(5), 1554–1560. https://doi.org/10.1590/S0102-09352013000500037
Psoni, L., Kotzamanides, C., Andrighetto, C., Lombardi, A., Tzanetakis, N., & Litopoulou-Tzanetaki, E. (2006). Genotypic and phenotypic heterogeneity in Enterococcus isolates from Batzos, a raw goat milk cheese. International Journal of Food Microbiology, 109(1–2), 109–120. https://doi.org/10.1016/j.ijfoodmicro.2006.01.027
Rocha, K. R., Perini, H. F., de Souza, C. M., Schueler, J., Tosoni, N. F., Furlaneto, M. C., & Furlaneto-Maia, L. (2019). Inhibitory effect of bacteriocins from enterococci on developing and preformed biofilms of Listeria monocytogenes, Listeria ivanovii and Listeria innocua. World Journal of Microbiology and Biotechnology, 35(7), 1–11. https://doi.org/10.1007/s11274-019-2675-0
Todorov, S. D., Furtado, D. N., Saad, S. M. I., & De Melo Franco, B. D. G. (2011). Bacteriocin production and resistance to drugs are advantageous features for Lactobacillus acidophilus La-14, a potential probiotic strain. New Microbiologica, 34(4), 357–370.
Vinderola, G., Burns, P., & Reinheimer, J. (2017). Probiotics in Nondairy Products. In Vegetarian and Plant-Based Diets in Health and Disease Prevention. 809–835. https://doi.org/10.1016/B978-0-12-803968-7.00044-7
Walstra, P., Wouters, J. T. M., & Geurts, T. J. (2006). Dairy Science and Technology. (2nd ed.) Roca Ranton: CRC Press.
Yerlikaya, O., & Akbulut, N. (2019). Potential use of probiotic Enterococcus faecium and Enterococcus durans strains in Izmir Tulum cheese as adjunct culture. Journal of Food Science and Technology, 56(4), 2175–2185. https://doi.org/10.1007/s13197-019-03699-5
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2020 Priscila Lima Magarotto de Paula; Marina Levorato de Moraes; Janaína Schueler; Nathália Aparecida Andrade de Souza; Márcia Cristina Furlaneto; Luciana Furlaneto-Maia; Marly Sayuri Katsuda
This work is licensed under a Creative Commons Attribution 4.0 International License.
Authors who publish with this journal agree to the following terms:
1) Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
2) Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
3) Authors are permitted and encouraged to post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work.