Background and objective: Presently, there is a growing interest in food produced without the addition of chemical preservatives. Lactic acid bacteria have a high potential to control the growth of undesirable microorganisms. In this work, the antifungal activity of eight strains of lactobacilli isolated from plant sources and foodstuffs (tartar sauce, wheat flour, barley flour, sourdough) were tested against Fusarium culmorum DMF301 and Penicillium expansum DMF04.
Materials and methods: Antifungal activity of live cells of lactobacilli and their heat-treated supernatants was determined by agar diffusion method at 30°C, the radial growth of fungi was measured. Organic acid production of tested strains was examined by HPLC.
Results and conclusion: Live cells of three Lactobacillus plantarum strains showed the highest antifungal activities. Fusarium culmorum DMF301 was more sensitive to the activity of lactobacilli. Heat-treated bacterial supernatants (100°C, 10 min) were also tested, being added at 10 or 20% v v-1 to the culture medium; growth of Fusarium culmorum DMF301was inhibited by range of 80-90% compared to controls at 10% supernatant concentration and fully at 20%. However, after neutralization, only the heat treated supernatant from Lactobacillus plantarum CCDM 583 had partially effective antifungal activity. The mutual inhibition of lactobacilli strains reduced their antifungal activity. Statistically significant differences in activity against Fusarium culmorum DMF 301 were found using individual strains of Lactobacillus plantarum CCDM 583 and MP2 or their combination. For use in combination with other cultures, it is therefore necessary to verify the compatibility of various strains of lactobacilli.
Conflict of interest: The authors declare no conflict of interest.
Muhialdin BJ, Hassan Z, Sadon SK. Antifungal activity of Lactobacillus fermentum Te007, Pediococcus pentosaceus Te010, Lactobacillus pentosus G004, and L. paracasei D5 on selected foods. J Food Sci. 2011; 76(7):493-499. doi:10.1111/j.1750-3841.2011.02292.
Oliveira PM, Zannini E, Arendt EK. Cereal fungal infection, mycotoxins, and lactic acid bacteria mediated bioprotection: From crop farming to cereal products. Food Microbiol. 2014; 37:78-95. doi:10.1016/j.fm.2013.06.003.
Gänzle M, Ripari V. Composition and function of sourdough microbiota: From ecological theory to bread quality. Int J Food Microbiol. 2016; 239:19-25. doi:10.1016/j.ijfoodmicro.2016.05.004.
De Vuyst L, Van Kerrebroeck S, Harth H, Huys G, Daniel H-M, Weckx S. Microbial ecology of sourdough fermentations: diverse or uniform? Food Microbiol. 2014; 37:11-29. doi: 10.1016/j.fm.2013.06.002.
Gänzle MG Enzymatic and bacterial conversions during sourdough fermentation. Food Microbiol. 2014; 37:2-10. doi:10.1016/j.fm.2013.04.007.
Galle S, Arendt EK. Exopolysaccharides from sourdough lactic acid bacteria. Crit Rev Food Sci Nutr. 2014; 54(7):891-901. doi:10.1080/10408398.2011.617474.
De Vuyst L, Neysens P. The sourdough microflora: biodiversity and metabolic interactions. Trends Food Sci Technol. 2005; 16:43-56. doi:10.1016/j.tifs.2004.02.012.
Gül H, Özçelik S, Sağdiç O, Certel M. Sourdough bread production with lactobacilli and S. cerevisiae isolated from sourdoughs. Process Biochem. 2005; 40(2):691-697. doi:10.1016/j.procbio.2004.01.044
Black BA, Zannini E, Curtis JC, Gänzle MG. Antifungal hydroxy fatty acids produced during sourdough fermentation: microbial and enzymatic pathways, and antifungal activity in bread. Appl Environ Microbiol. 2013; 79(6):1866-1873. doi:10.1128/AEM.03784-12.
Cortés-Zavaleta O, López-Malo A, Hernández-Mendoza A, García HS. Antifungal activity of lactobacilli and its relationship with 3-phenyllactic acid production. Int J Food Microbiol. 2014; 173:30-35. doi:10.1016/j.ijfoodmicro.2013.12.016.
Reis JA, Paula AT, Casarotti SN, Penna ALB. Lactic acid bacteria antimicrobial compounds: characteristics and applications. Food Eng Rev. 2012; 4(2):124-140. doi:10.1007/s12393-012-051-2.
Sangmanee P, Hongpattarakere T. Inhibitory of multiple antifungal components produced by Lactobacillus plantarum K35 on growth, aflatoxin production and ultrastructure alterations of Aspergillus flavus and Aspergillus parasiticus. Food Control. 2014; 40:224-233. doi:10.1016/j.foodcont.2013.12.005.
Dagnas S, Gauvry E, Onno B, Membré J-M. Quantifying effect of lactic, acetic, and propionic acids on growth of moulds isolated from spoiled bakery products. J Food Prot. 2015; 78(9):1689-1698. doi.org/10.4315/0362-028X.JFP-15-046.
Dalié DKD, Deschamps AM, Richard-Forget F. Lactic acid bacteria – Potential for control of mould growth and mycotoxins: A Review. Food Control. 2010; 21:370-380. doi:10.1016/j.foodcont.2009.07.011.
Stiles J, Penkar S, Plocková M, Chumchalova J, Bullerman LB. Antifungal activity of sodium acetate and Lactobacillus rhamnosus. J Food Prot. 2002; 65(7):1188-1191.
Ventimiglia G, Alfonzo A, Galluzzo P, Corona O, Francesca N, Caracappa S, Moschetti G, Settanni L. Codominance of Lactobacillus plantarum and obligate heterofermentative lactic acid bacteria during sourdough fermentation. Food Microbiol. 2015; 51:57-68. doi:10.1016/j.fm.2015.04.011
Naz S, Gueguen-Minerbe M, Cretenet M, Vernoux JP. Aromatic amino acids as precursors of antimicrobial metabolites in Geotrichum candidum. FEMS Microbiol Lett. 2013; 344(1):39-47. doi:10.1111/1574-6968.
Sathe SJ, Nawani NN, Dhakephalkar PK, Kapadnis BP. Antifungal lactic acid bacteria with potential to prolong shelf-life of fresh vegetables. J. Appl. Microbiol. 2007; 103(6):2622-2628. doi:10.1111/j.1365-2672.2007.03525.x.
Prange A, Modrow H, Hormes J, Kramer J, Kohler P. Influence of mycotoxin producing fungi (Fusarium, Aspergillus, Penicillium) on gluten proteins during suboptimal storage of wheat after harvest and competitive interactions between field and storage fungi. J Agric Food Chem. 2005; 53(17):6930-6938. doi: 10.1021/jf050821t.
Schillinger U, Villarreal JV. Inhibition of Penicillium nordicum in MRS medium by lactic acid bacteria isolated from foods. Food Control. 2010; 21(2):107-111. doi:10.1016/j.foodcont.2008.11.010.
Yang EJ, Chang HC. Purification of a new antifungal compound produced by Lactobacillus plantarum AF1 isolated from kimchi. Int J Food Microbiol. 2010; 139(1-2):56-63. doi:10.1016/j.ijfoodmicro.2010.02.012.
Demirbaᶊ F, Ispirli H, Kurnaz AA, Yilmaz MT, Dertli E. Antimicrobial and functional properties of lactic acid bacteria isolated from sourdoughs. Food Sci Technol. 2017; 79:361-366. doi:10.1016/j.lwt.2017.01.067.
Zhang L, Taal MA, Boom RM, Chen XD, Schutyser MAI. Effect of baking conditions and storage on the viability of Lactobacillus plantarum supplemented to bread. LWT-Food Sci Technol. 2018; 87:318-325. doi:10.1016/j.lwt.2017.09.005.
Besbes E, Jury V, Monteau J-Y, Le Bail A. Effect of baking conditions and storage with crust on the moisture profile, local textural properties and staling kinetics of pan bread. LWT – Food Sci Technol. 2014; 58(2):658-666. doi:10.1016/j.lwt.2014.02.037.
Rouse S, Harnett D, Vaughan A, Van Sinderen D. Lactic acid bacteria with potential to eliminate fungal spoilage in foods. J Appl Microbiol. 2008; 104(3):915-923. doi:10.1111/j.1365-2672.2007.03619.x.
Gerez CL, Torino MI, Rollán G, Font de Valdez G. Prevention of bread mould spoilage by using lactic acid bacteria with antifungal properties. Food Control. 2009; 20(2):144-148. doi:10.1016/j.foodcont.2008.03.005.
Laref N, Guessas B. Antifungal activity of newly isolates of lactic acid bacteria. Innov Rom Food Biotechnol. 2013; 13:80-88.
Gerez CL, Torres MJ, Font de Valdez G, Rollán G. Control of spoilage fungi by lactic acid bacteria. Biol Control. 2013; 64(3):231-237. doi:10.1016/j.biocontrol.2012.10.009.
De Muynck C, Leroy AIJ, De Maeseneire S, Arnaut F, Soetaert W, Vandamme EJ (2004) Potential of selected lactic acid bacteria to produce food compatible antifungal metabolites. Microbiol Res. 2004; 159(4):339-346. doi:10.1016/j.micres.2004.07.002.
Le Lay C, Mounier J, Vasseur V, Weill A, Le Blay G, Barbier G. In vitro and in situ screening of lactic acid bacteria and propionibacteria antifungal activities against bakery product spoilage molds. Food Control. 2016; 60:247-255. doi:10.1016/j.foodcont.2015.07.034.
Axel C, Röcker B, Brosnan B, Zannini E, Furey A, Coffey A, Arendt EK. Application of Lactobacillus amylovorus DSM19280 in gluten-free sourdough bread to improve the microbial shelf life. Food Microbiol. 2015; 47:36-44. doi:10.1016/j.fm.2014.10.005.
Crowley S, Mahony J, van Sinderen D. Comparative analysis of two antifungal Lactobacillus plantarum isolates and their application as bioprotectants in refrigerated foods. J Appl Microbiol. 2012; 113(6):1417-1427. doi:10.1111/jam.12012.
Deepthi BV, Poornachandra Rao K, Chennapa G, Naik MK, Chandrashekara KT, Sreenivasa MY. Antifungal attributes of Lactobacillus plantarum MYS6 against Fumonisin producing Fusarium proliferatum associated with poultry feeds. PLoS One 2016; 11(6):e0155122. doi:10.1371/journal.pone.0155122.
Delavenne E, Trunet C, Barbier G, Mounier J, Le Blay G. Characterization of the antifungal activity of Lactobacillus harbinensis K.V9.3.1Np and Lactobacillus rhamnosus K.C8.3.1I in yogurt. Food Microbiol. 2015; 45:10-17. doi: 10.1016/j.fm.2014.04.017.
Russo P, Arena MP, Fiocco D, Capozzi V, Drider D, Spano G: Lactobacillus plantarum with broad antifungal activity: A promising approach to increase safety and shelf-life of cereal-based products. Int J Food Microbiol. 2017; 247:48-54. doi: 10.1016/j.ijfoodmicro.2016.04.027.