Antimicrobial effect of selected lactic acid bacteria against microorganisms with decarboxylase activity
Keywords:biogenic amines, lactic acid bacteria, bacteriocins, nisin, Enterococcus spp., Staphylococcus spp.
The main purpose of this study was to evaluate the antimicrobial activity of twenty-one bacteriocinogenic lactic acid bacteria (12 strains of Lactococcus lactis subsp. lactis, 4 strains of Lactobacillus gasseri, 3 strains of Lb. helveticus and 2 strains of Lb. acidophilus, LAB) against 28 Staphylococcus and 33 Enterococcus strains able to produce tyramine, putrescine, 2-phenylethylamine and cadaverine. The antimicrobial activity of cell-free supernatants (CFS) from tested LAB was examined by an agar-well diffusion assay. Nine out of twenty-one strains (33%) showed the inhibitory effect on tested enterococci and staphylococci, namely 9 strains of Lactococcus lactis subsp. lactis. The diameters of inhibition zones ranged between 7 mm and 14 mm. The biggest diameter of 14 mm inhibition was obtained with the CFS's from strains CCDM 670 and CCDM 731 on Enterococcus sp. E16 and E28. The cell-free supernatants from Lactococcus lactis subsp. lactis CCDM 71 and from Lactococcus lactis subsp. lactis CCDM 731 displayed the broadest antibacterial activity (52% inhibition of all tested strains). On the other hand, the cell-free supernatants from the screened Lactobacillus strains did not show any inhibitory effect on the tested Staphylococcus and Enterococcus strains. Nowadays, the great attention is given to the antibacterial substances produced by lactic acid bacteria. With the ability to produce a variety of metabolites displaying inhibitory effect, the LAB have great potential in biopreservation of food.
Bargossi, E., Tabanelli, G., Montanari, Ch., Lanciotti, R., Gatto, V., Gardini, F., Torriani, S. 2015. Tyrosine decarboxylase activity of enterococci grown in media with different nutritional potential: tyramine and 2-phenylethylamine accumulation and tyrDC gene expression. Frontiers in Microbiology, vol. 6, p. 1-10. https://doi.org/10.3389/fmicb.2015.00259 PMid:25914676
Bhardwaj, S., Dhawale, K. B. J., Patil, M., Divase, S. 2013. Enterococcus faecium and Enterococcus faecalis, the nosocomial pathogens with special reference to multi-drug resistance and phenotypic characterization. International Journal of Pharmaceutical Science and Practice, vol. 2, no. 1, p. 1-10.
Bover-Cid, S., Hugas, M., Izquierdo-Pulido a, M., Carmen Vidal-Carou, M. 2001. Amino acid-decarboxylase activity of bacteria isolated from fermented pork sausages. International Journal of Food Microbiology, vol. 66, no.3, p. 185-189. https://doi.org/10.1016/S0168-1605(00)00526-2
Buňková, L., Buňka, F., Dráb, V., Kráčmar, S., Kubáň, V. 2012. Effects of NaCl, lactose and availability of oxygen on tyramine production by the Enterococcus durans CCDM 53. European Food Research and Technology, vol. 234, no.6, p. 973-979. https://doi.org/10.1007/s00217-012-1714-y
Buňková, L., Buňka, F., Hlobilová, M., Vaňátková, Z., Nováková, D. 2009. Tyramine production of technological important strains of Lactobacillus, Lactococcus and Streptococcus. European Food Research and Technology, vol. 229, no. 3, p. 533-538. https://doi.org/10.1007/s00217-009-1075-3
Buňková, L., Buňka, F., Mantlová, G., Čabalová, A., Sedláček, I., Švec, P., Pachlová, V., Kráčmar, S. 2010. The effect of ripening and storage conditions on the distribution of tyramine, putrescine and cadaverine in Edam-cheese. Food Microbiology, vol. 27, no. 7, p. 880-888. https://doi.org/10.1016/j.fm.2010.04.014 PMid:20688229
Buňková, L., Gál, R., Lorencová, E., Jančová, P., Doležalová, M., Kmeť, V., Buňka, F. 2016. Microflora of farm and hunted pheasants in relation to biogenic amines production. European Journal of Wildlife Research, vol. 62, no. 3, p. 341-352. https://doi.org/10.1007/s10344-016-1008-y
Callejón, S., Sendra, R., Ferrer, S., Pardo, I. 2014. Identification of a novel enzymatic activity from lactic acid bacteria able to degrade biogenic amines in wine. Applied Microbiology and Biotechnology, vol. 98, no. 1, p. 185-98. https://doi.org/10.1007/s00253-013-4829-6 PMid:23515835
Capozzi, V., Russo, P., Ladero, V., Fernández, M., Fiocco, D., Alvarez, M., Grieco, F., Spano, G. 2012. Biogenic amines degradation by Lactobacillus plantarum: toward a potential application in wine. Frontiers in Microbiology, vol. 3, p. 122. https://doi.org/10.3389/fmicb.2012.00122 PMid:22485114
Chen, H., Hoover, D. G. 2003. Bacteriocins and their food applications. Comprehensive Reviews in Food Science and Food Safety, vol. 2, no. 3, p. 82-100. https://doi.org/10.1111/j.1541-4337.2003.tb00016.x
Cizeikiene, D., Juodeikiene, G., Paskevicius, A., Bartkiene, E. 2013. Antimicrobial activity of lactic acid bacteria against pathogenic and spoilage microorganism isolated from food and their control in wheat bread. Food Control, vol. 31, no. 2, p. 539-545. https://doi.org/10.1016/j.foodcont.2012.12.004
Cleveland, T. J., Montville, I. F., Nes, M. L. Chikindas, M. L. 2001. Bacteriocins: Safe, natural antimicrobials for food preservation. International Journal of Food Microbiology, vol. 71, no. 1, p. 1-20. https://doi.org/10.1016/S0168-1605(01)00560-8
Dapkevicius, M. L.N. E., Nouta, M. J. R., Rombouts, F. M., Houben, J. H., Wymenga, W. 2000. Biogenic amine formation and degradation by potential fish silage starter microorganisms. International Journal of Food Microbiology, vol. 57, no. 1-2, p. 107-114. https://doi.org/10.1016/S0168-1605(00)00238-5
EFSA, 2006. Question number EFSA-Q-2005-031. Opinion of the Scientific Panel on Food Additives, Flavourings, Processing Aids and Materials in Contact with Food on a request from the Commission related to the use of nisin (E 234) as a food additive [online] The EFSA Journal, vol. 314, p. 1-16 [cit. 2017-2-09] Available at: https://www.efsa.europa.eu/sites/default/files/scientific_output/files/main_documents/314.pdf.
Enan, G., Abdel-Shafi, S., Ouda, S., Negm, S. 2013. Novel Antibacterial Activity of Lactococcus Lactis Subspecies Lactis Z11 Isolated from Zabady. International Journal of Biomedical Science, vol. 9, no. 3, p. 174-180. PMid:24151453
Fadda, S., Vignolo, G., Oliver, G. 2001. Tyramine degradation and tyramine/histamine production by lactic acid bacteria and Kocuria strains. Biotechnology Letters, vol. 23, 2015-2019. https://doi.org/10.1023/A:1013783030276
Favaro, L., Penna, A. L. B., Todorov, S. D. 2015. Bacteriocinogenic LAB from cheeses - Application in biopreservation? Trends in Food Science & Technology, vol. 41, no. 1, p. 37-48. https://doi.org/10.1016/j.tifs.2014.09.001
Franz, C. M., Huch M., Abriouel, H., Holzapfel, W., Gálvez, A. 2011. Enterococci as probiotics and their implications in food safety. International Journal of Food Microbiology, vol. 151, no. 2, p. 125-140. https://doi.org/10.1016/j.ijfoodmicro.2011.08.014 PMid:21962867
Gálvez, A., Abriouel, H., López, R. L., Ben Omar, N. 2007. Bacteriocin-based strategies for food biopreservation. International Journal of Food Microbiology, vol. 120, no. 1-2, p. 51-70. https://doi.org/10.1016/j.ijfoodmicro.2007.06.001 PMid:17614151
García-Ruiz, A, González-Rompinelli, E. M., Bartolomé, B., Moreno-Arribas, M. V. 2011. Potential of wine-associated lactic acid bacteria to degrade biogenic amines. International Journal of Food Microbiology, vol. 148, no. 2, p. 115-120. https://doi.org/10.1016/j.ijfoodmicro.2011.05.009 PMid:21641669
Gardini, F., Özogul, Y., Suzzi, G., Tabanelli, G., Özogul, F. 2016. Technological Factors Affecting Biogenic Amine Content in Foods: A Review. Frontiers in Microbiology, vol. 7, p. 1-18.
Jiménez, E., Ladero, V., Chico, I., Maldonado-Barragán, A., López, M., Martín, V., Fernández, L., Fernández, M., Álvarez, M. A., Torres, C., Rodríguez, J. M. 2013. Antibiotic resistance, virulence determinants and production of biogenic amines among enterococci from ovine, feline, canine, porcine and human milk. BMC Microbiology, vol. 13, p. 288. https://doi.org/10.1186/1471-2180-13-288 PMid:24325647
Karska-Wysockib, B., Bazoa, M., Smoragiewicza, W. 2010. Antibacterial activity of Lactobacillus acidophilus and Lactobacillus casei against methicillin-resistant Staphylococcus aureus (MRSA). Microbiological Research, vol. 165, no. 8, p. 674-686. https://doi.org/10.1016/j.micres.2009.11.008 PMid:20116228
Ladero V., Fernández M., Calles-Enríquez M., Sánchez-Llana E., Cañedo E., Martin M. C., Alvarez, M. A. 2012. Is the production of the biogenic amines tyramine and putrescine a species-level trait in enterococci? Food Microbiology, vol. 30, no. 1, p. 132-138. https://doi.org/10.1016/j.fm.2011.12.016 PMid:22265293
Ladero, V., Calles, M., Ferna´ndez, M., Alavrez, M. 2010. Toxicological Effects of Dietary Biogenic Amines. Current Nutrition and Food Science, vol. 6, no. 2, p. 145-156. https://doi.org/10.2174/157340110791233256
Lee, N.-K., Jin Han, E., Jun Han, K., Paik, H.-D. 2013. Antimicrobial Effect of Bacteriocin KU24 Produced by Lactococcus lactis KU24 against Methicillin-Resistant Staphylococcus aureus. Journal of Food Science, vol. 78, no. 3, p. M465-M469. https://doi.org/10.1111/1750-3841.12053 PMid:23398212
Martuscelli, M., Crudele, M. A, Gardini, F., Suzzi, G. 2000. Biogenic amine formation and oxidation by Staphylococcus xylosus strains from artisanal fermented sausages. Letters in Applied Microbiology, vol. 31, no. 3, p. 228-232. https://doi.org/10.1046/j.1365-2672.2000.00796.x PMid:10972734
McAuliffe, O., Ross, R. P., Hill, C. 2001. Lantibiotics: structure, biosynthesis and mode of action. FEMS Microbiology Reviews, vol. 25, no. 3, p. 285-308. https://doi.org/10.1111/j.1574-6976.2001.tb00579.x
Olaoye, O. A. 2016. Antimicrobial Activities of Five Strains Of Lactococcus Isolated from Beef Against Indicator Organisms of Public Health Significance. Turkish Journal of Agriculture - Food Science and Technology, vol. 4, no. 10, p. 887-892.
Perez, R. H., Zendo, T., Sonomoto, K. 2014. Novel bacteriocins from lactic acid bacteria (LAB): various structures and applications. Microbial Cell Factories, vol. 13, no. Suppl 1, p. S3.
Pleva, P., Buňková, L., Lauková, A., Lorencová, E., Kubáň, V., Buňka, F. 2012. Decarboxylation activity of enterococci isolated from rabbit meat and staphylococci isolated from trout intestines. Veterinary Microbiology, vol. 159, no. 3-4, p. 438-442. https://doi.org/10.1016/j.vetmic.2012.04.028 PMid:22608104
Reis, J. A., Paula A. T., Casarotti, S. N., Penna, A. L. B. 2012. Lactic Acid Bacteria Antimicrobial Compounds: Characteristics and Applications. Food Engineering Reviews, vol. 4, no. 2, p. 124-140. https://doi.org/10.1007/s12393-012-9051-2
Ross, R. P., Morgan, S., Hill, C. 2002. Preservation and fermentation: past, present and future. International Journal of Food Microbiology, vol. 79, no. 1-2, p. 3-16. https://doi.org/10.1016/S0168-1605(02)00174-5
Şanlibaba, P., Akkoç, n., Akçelik, M. 2009. Identification and Characterisation of Antimicrobial Activity of Nisin A Produced by Lactococcus lactis subsp. lactis LL27. Czech Journal of Food Sciences, vol. 27, p. 55-64.
Santos, M. H. S. 1996. Biogenic amines: their importance in foods. International Journal of Food Microbiology, vol. 29, no. 2-3, p. 213-231. https://doi.org/10.1016/0168-1605(95)00032-1
Shalaby, A. R. 1996. Significance of biogenic amines to food safety and human health. Food Research International, vol. 29, no. 7, p. 675-690. https://doi.org/10.1016/S0963-9969(96)00066-X
Šušković, J., Kos, B., Beganović, J., Pavunc, A. L., Habjanič, K., Matošić, S. 2010. Antimicrobial activity - The most important property of probiotic and starter lactic acid bacteria. Food Technology and Biotechnology, vol. 48, no. 3, p. 296-307.
Suzzi, G., Gardini, F. 2003. Biogenic amines in dry fermented sausages: a review. International Journal of Food Microbiology, vol. 88, no. 1, p. 41-54. https://doi.org/10.1016/S0168-1605(03)00080-1
Xie, Ch., Wang, H., Deng, Sh., Xu, X. 2016. The inhibition of cell-free supernatant of Lactobacillus plantarum on production of putrescine and cadaverine by four amine-positive bacteria in vitro. LWT - Food Science and Technology, vol. 67, p. 106-111. https://doi.org/10.1016/j.lwt.2015.11.028
How to Cite
LicenseAuthors who publish with this journal agree to the following terms:
- 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.
- 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.
- 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 (See The Effect of Open Access).