Antifungal activity of lactic acid bacteria isolated from Masske, camel dough, and local yogurt against Aspergillus flavus and Aspergillus niger
Subject Areas :
Food Science and Technology
A. Nasrollahzadeh
1
(M.Sc, Graduated in Food Science and Technology, Gorgan University of Agricultural Sciences and Natural Resources, Gorgan, Iran)
M. Khomeiri
2
(Associate professor, Department of Food Science and Technology, Gorgan University of Agricultural Sciences and Natural Resources, Gorgan, Iran)
A. Sadeghi
3
(Associate professor, Department of Food Science and Technology, Gorgan University of Agricultural Sciences and Natural Resources, Gorgan, Iran)
M. Mahmoudi
4
(Ph.D, Department of Food Science and Technology, Gorgan University of Agricultural Sciences and Natural Resources, Gorgan, Iran)
M. Ebrahimi
5
(Ph.D, Department of Food Science and Technology, Gorgan University of Agricultural Sciences and Natural Resources, Gorgan, Iran)
Received: 2019-10-27
Accepted : 2020-01-22
Published : 2020-01-21
Keywords:
Antifungal,
Aspergillus flavus,
Lactic acid bacteria,
Aspergillus niger,
inhibitory,
Abstract :
In animal and food products, different types of chemical preservatives and antibiotics are used to inhibit the growth of Aspergillus flavus and other toxicogenic fungi. The aim of this study was to investigate the antifungal activity of Lactic Acid Bacteria Isolated from Masske, Chal, and local yogurt against Aspergillus flavus and Aspergillus niger. For this purpose, isolates previously tested for antibacterial effects were used. The isolates of Lactobacillus plantarum B38, Enterococcus faecium 8C and Lactobacillus ramonosus Y89 with the highest inhibitory effect on pathogenic bacteria were selected and their antifungal effects against toxin-producing molds were evaluated using the overlay method. The results showed that lactic acid isolates at the end of the fourth day prevented the growth of Aspergillus niger and Enterococcus faecium, Lactobacillus rhamnosus and Lactobacillus plantarum showed 70.84%, 37.65% and 43.31% of inhibitory activity, respectively. The results also showed that Lactobacillus rhamnosus had the highest (62.35%) inhibitory effect on Aspergillus niger (p < 0.05). The results of the study on the effect of lactic acid isolates on the growth of Aspergillus flavus showed that all tested bacteria had inhibitory properties on the molds and Lactobacillus rhamnosus with 83.8% had the highest inhibitory effect on Aspergillus flavus (p < 0.05). Consequently, due to the inhibitory ability of the lactic acid bacteria, they can be used as bio-preservatives along with synthetic preservatives in the food industry.
References:
· Abushelaibi, A., Al-Mahadin, S., El-Tarabily, K., Shah, N.P. and Ayyash, M. (2017). Characterization of potential probiotic lactic acid bacteria isolated from camel milk. LWT - Food Science and Technology, 79: 316–325.
· Ahmadova, A., Todorov, S.D., Hadji-Sfaxi, I., Choiset, Y., Rabesona, H., Messaoudi, S., et al. (2013). Antimicrobial and antifungal activities of Lactobacillus curvatus strain isolated from homemade Azerbaijani cheese. Anaerobe, 20: 42–49.
· Arora, D.K., Das, S. and Sukumar, M. (2013). Analyzing Microbes: Manual of Molecular Biology Techniques. Springer Berlin Heidelberg, pp. 135–152.
· Burt, S. (2004). Essential oils: Their antibacterial properties and potential applications in foods, a review. International Journal of Food Microbiology, 94: 223–253.
· Cortés-Zavaleta, O., López-Malo, A., Hernández-Mendoza, A., and García, H. (2014). Antifungal activity of lactobacilli and its relationship with 3-phenyllactic acid production. International Journal of Food Microbiology, 173: 30–35.
· Dali, D. K. D., Deschamps, A. M. and Richard-Forget, F. (2010). Lactic acid bacteria e potential for control of mould growth and mycotoxins: a review. Food Control, 21: 370–380.
· Delavenne, E., Ismail, R., Pawtowski, A., Mounier, J., Barbier, G. and Le Blay G. (2012). Assessment of lactobacilli strains as yogurt bioprotective cultures. Food Control, 30: 206–213.
· Filtenborg, O., Frisvad, J.C. and Thrane, U. (1996). Moulds in food spoilage. International Journal of Food Microbiology, 33(1): 85–102.
· Gaggia, F., Di Gioia, D., Baffoni, L. and Biavati, B. (2011). The role of protective and probiotic cultures in food and feed and their impact in food safety. Trends in Food Science and Technology, 22: 58–66.
· Gerbaldo, G.A., Barberis, C., Pascual, L., Dalcero, A. and Barberis, L. (2012). Antifungal activity of two Lactobacillus strains with potential probiotic properties. FEMS Microbiology Letters, 332: 27–33.
· Gerez, C., Torres, M., deValdez, G.F. and Rollán, G. (2013). Control of spoilage fungi by lactic acid bacteria. Biological Control, 64(3): 231–237.
· Guimarães, A., Venancio, A., and Abrunhosa, L. (2018). Antifungal effect of organic acids from lactic acid bacteria on Penicillium nordicum. Food Additives and Contaminants: Part A, 35(9): 1803–1818.
· Jung, S., Hwang, H., and Lee, J.H. (2019). Effect of lactic acid bacteria on phenyllactic acid production in kimchi. Food Control, 106, 106701.
· Lavermicocca, P., Valerio, F., Evidente, A., Lazzaroni, S., Corsetti, A. and Gobbetti, M. (2000). Purification and characterization of novel antifungal compounds from the sourdough Lactobacillus plantarum strain 21B. Applied Microbiology, 66: 4084–4090.
· Lavermicocca, P., Valerio, F. and Visconti, A. (2003). Antifungal activity of phenyllactic acid against molds isolated from bakery products. Applied and Environmental Microbiology, 69: 634–640.
· Leite, A.M.O., Miguel, M.A.L., Peixoto, R.S., Ruas-Madiedo, P., Paschoalin, V.M. F., Mayo, B. and Delgado, S. (2015). Probiotic potential of selected lactic acid bacteria strains isolated from Brazilian kefir grains. Journal of Dairy Science, 98: 1–11.
· Leroy, F. and De Vuyst L. (2004). Lactic acid bacteria as functional starter cultures for the food fermentation industry. Trends in Food Science and Technology, 15(2): 67–78.
· Li, H., Zhang, S., Lu, J., Liu, L., Uluko, H., Pang, X. et al. (2014). Antifungal activities and effect of Lactobacillus casei AST18 on the mycelia morphology and ultrastructure of Penicillium chrysogenum. Food Control, 43: 57–64.
· Lotfi, H., Hejazi, M. A., Maleki Zanjani, B. and Barzegari A. (2010). Isolation, biochemical and molecular identification of potentiallly probiotic bacteria from traditional dairy products from Heris and Sarab Regions. Journal of Food Research, 1: 1–17. (In Persian)
· Leyva Salas, M., Thierry, A., Lemaître, M., Garric, G., Harel-Oger, M., Chatel, M. and Coton, E. (2018). Antifungal activity of lactic acid bacteria combinations in dairy mimicking models and their potential as bioprotective cultures in pilot scale applications. Frontiers in Microbiology, 9, 1787.
· Lynch, K.M., Pawlowska, A.M., Brosnan, B., Coffey, A., Zannini, E., Furey, A. et al. (2014). Application of Lactobacillus amylovorus as an antifungal adjunct to extend the shelf-life of Cheddar cheese. International Dairy Journal, 34(1): 167–173.
· Magnusson, J. and Schnürer, J. (2001). Lactobacillus coryniformis subsp. coryniformis strain Si3 produces a broad-spectrum proteinaceous antifungal compound. Applied and Environmental Microbiology, 67: 1–5.
· Magnusson, J., Ström, K., Roos, S., Sjögren, J. and Schnürer, J. (2003). Broad and complex antifungal activity among environmental isolates of lactic acid bacteria. FEMS Microbiology Letters, 219(1): 129–135.
· Nanda, D.K., Tomar, S.K., Singh, R., Mal, G., Singh, P., Arora, D.K. and Kumar, D. (2011). Phenotypic and genotypic characterisation of Lactobacilli isolated from camel cheese produced in India. International Journal of Dairy Technology, 64(3): 437–443.
· Nasrollahzadeh, A., Khomeiri, M., Sadeghi, A, Mahmudi, M. and Ebrahimi M. (2019). Identification and evaluation of the antimicrobial potential of strains derived from traditional fermented dairy products of Iran as a biological preservative against Listeria monocytogenes, Staphylococcus aureus, Salmonella enterica and Escherichia coli. Pathogens, 8(2): 71–91.
· Oliveira, P.M., Zannini, E. and Arendt, E.K. (2014). Cereal fungal infection, mycotoxins, and lactic acid bacteria mediated bioprotection: from crop farming to cereal products. Food Microbiology, 37: 78–95.
· Parkin, D.M., Bray, F., Ferlay, J. and Pisani, P. (2005). Global cancer statistics, 2002. CA: A Cancer Journal for Clinicians Cancer, 55: 74–108.
· Pawlowska, A.M., Zannini, E., Coffey, A. and Arendt, E.K. (2012). “Green Preservatives”: combating fungi in the food and feed industry by applying antifungal lactic acid bacteria. Advances in Food and Nutrition Research, 66: 66: 217–238.
· Rossetti, L. and Giraffa, G. (2005). Rapid identification of dairy lactic acid bacteria by M13-generated, RAPD-PCR fingerprint databases. Journal of Microbiological Methods, 63(2): 135-144.
· Rouse, S., Harnett, D., Vaughan, A. and Sinderen D. (2008). Lactic acid bacteria with potential to eliminate fungal spoilage in foods. Journal of Applied Microbiology, 104(3): 915–923.
· Schnürer, J. and Magnusson, J. (2005). Antifungal lactic acid bacteria as biopreservatives. Trends in Food Science and Technology, 16(1): 70–78.
· Sengun, I., Yaman, D. and Gonul, S. (2008). Mycotoxins and mould contamination in cheese: a review. World Mycotoxin Journal, 1(3): 291–298.
· Siedler, S., Balti, R. and Neves, A.R. (2019). Bioprotective mechanisms of lactic acid bacteria against fungal spoilage of food. Current Opinion in Biotechnology, 56: 138-146.
· Stroem, K., Schnuerer, J. and Melin P. (2005). Co-cultivation of antifungal Lactobacillus plantarum MiLAB 393 and Aspergillus nidulans, evaluation of effects on fungal growth and protein expression. FEMS Microbiology Letters, 246: 119–124.
· Tropcheva, R., Nikolova, D., Evstatieva, Y. and Danova, S. 2014. Antifungal activity and identification of Lactobacilli, isolated from traditional dairy product “katak”. Anaerobe, 28: 78-84.
· Yang, E. and Chang, H. (2010). Purification of a new antifungal compound produced by Lactobacillus plantarum AF1 isolated from kimchi. International Journal of Food Microbiology, 139(1): 56–63.
· Zhang, J., Wang, X. J., Yan, Y.J., Jiang, L., Wang, J.D., Li B.J. et al. (2010). Isolation and identification of 5-hydroxyl-5-methyl-2-hexenoic acid from Actinoplanes sp. HBDN08 with antifungal activity. Bioresource Technology, 101(21): 8383–8388.
_||_
· Abushelaibi, A., Al-Mahadin, S., El-Tarabily, K., Shah, N.P. and Ayyash, M. (2017). Characterization of potential probiotic lactic acid bacteria isolated from camel milk. LWT - Food Science and Technology, 79: 316–325.
· Ahmadova, A., Todorov, S.D., Hadji-Sfaxi, I., Choiset, Y., Rabesona, H., Messaoudi, S., et al. (2013). Antimicrobial and antifungal activities of Lactobacillus curvatus strain isolated from homemade Azerbaijani cheese. Anaerobe, 20: 42–49.
· Arora, D.K., Das, S. and Sukumar, M. (2013). Analyzing Microbes: Manual of Molecular Biology Techniques. Springer Berlin Heidelberg, pp. 135–152.
· Burt, S. (2004). Essential oils: Their antibacterial properties and potential applications in foods, a review. International Journal of Food Microbiology, 94: 223–253.
· Cortés-Zavaleta, O., López-Malo, A., Hernández-Mendoza, A., and García, H. (2014). Antifungal activity of lactobacilli and its relationship with 3-phenyllactic acid production. International Journal of Food Microbiology, 173: 30–35.
· Dali, D. K. D., Deschamps, A. M. and Richard-Forget, F. (2010). Lactic acid bacteria e potential for control of mould growth and mycotoxins: a review. Food Control, 21: 370–380.
· Delavenne, E., Ismail, R., Pawtowski, A., Mounier, J., Barbier, G. and Le Blay G. (2012). Assessment of lactobacilli strains as yogurt bioprotective cultures. Food Control, 30: 206–213.
· Filtenborg, O., Frisvad, J.C. and Thrane, U. (1996). Moulds in food spoilage. International Journal of Food Microbiology, 33(1): 85–102.
· Gaggia, F., Di Gioia, D., Baffoni, L. and Biavati, B. (2011). The role of protective and probiotic cultures in food and feed and their impact in food safety. Trends in Food Science and Technology, 22: 58–66.
· Gerbaldo, G.A., Barberis, C., Pascual, L., Dalcero, A. and Barberis, L. (2012). Antifungal activity of two Lactobacillus strains with potential probiotic properties. FEMS Microbiology Letters, 332: 27–33.
· Gerez, C., Torres, M., deValdez, G.F. and Rollán, G. (2013). Control of spoilage fungi by lactic acid bacteria. Biological Control, 64(3): 231–237.
· Guimarães, A., Venancio, A., and Abrunhosa, L. (2018). Antifungal effect of organic acids from lactic acid bacteria on Penicillium nordicum. Food Additives and Contaminants: Part A, 35(9): 1803–1818.
· Jung, S., Hwang, H., and Lee, J.H. (2019). Effect of lactic acid bacteria on phenyllactic acid production in kimchi. Food Control, 106, 106701.
· Lavermicocca, P., Valerio, F., Evidente, A., Lazzaroni, S., Corsetti, A. and Gobbetti, M. (2000). Purification and characterization of novel antifungal compounds from the sourdough Lactobacillus plantarum strain 21B. Applied Microbiology, 66: 4084–4090.
· Lavermicocca, P., Valerio, F. and Visconti, A. (2003). Antifungal activity of phenyllactic acid against molds isolated from bakery products. Applied and Environmental Microbiology, 69: 634–640.
· Leite, A.M.O., Miguel, M.A.L., Peixoto, R.S., Ruas-Madiedo, P., Paschoalin, V.M. F., Mayo, B. and Delgado, S. (2015). Probiotic potential of selected lactic acid bacteria strains isolated from Brazilian kefir grains. Journal of Dairy Science, 98: 1–11.
· Leroy, F. and De Vuyst L. (2004). Lactic acid bacteria as functional starter cultures for the food fermentation industry. Trends in Food Science and Technology, 15(2): 67–78.
· Li, H., Zhang, S., Lu, J., Liu, L., Uluko, H., Pang, X. et al. (2014). Antifungal activities and effect of Lactobacillus casei AST18 on the mycelia morphology and ultrastructure of Penicillium chrysogenum. Food Control, 43: 57–64.
· Lotfi, H., Hejazi, M. A., Maleki Zanjani, B. and Barzegari A. (2010). Isolation, biochemical and molecular identification of potentiallly probiotic bacteria from traditional dairy products from Heris and Sarab Regions. Journal of Food Research, 1: 1–17. (In Persian)
· Leyva Salas, M., Thierry, A., Lemaître, M., Garric, G., Harel-Oger, M., Chatel, M. and Coton, E. (2018). Antifungal activity of lactic acid bacteria combinations in dairy mimicking models and their potential as bioprotective cultures in pilot scale applications. Frontiers in Microbiology, 9, 1787.
· Lynch, K.M., Pawlowska, A.M., Brosnan, B., Coffey, A., Zannini, E., Furey, A. et al. (2014). Application of Lactobacillus amylovorus as an antifungal adjunct to extend the shelf-life of Cheddar cheese. International Dairy Journal, 34(1): 167–173.
· Magnusson, J. and Schnürer, J. (2001). Lactobacillus coryniformis subsp. coryniformis strain Si3 produces a broad-spectrum proteinaceous antifungal compound. Applied and Environmental Microbiology, 67: 1–5.
· Magnusson, J., Ström, K., Roos, S., Sjögren, J. and Schnürer, J. (2003). Broad and complex antifungal activity among environmental isolates of lactic acid bacteria. FEMS Microbiology Letters, 219(1): 129–135.
· Nanda, D.K., Tomar, S.K., Singh, R., Mal, G., Singh, P., Arora, D.K. and Kumar, D. (2011). Phenotypic and genotypic characterisation of Lactobacilli isolated from camel cheese produced in India. International Journal of Dairy Technology, 64(3): 437–443.
· Nasrollahzadeh, A., Khomeiri, M., Sadeghi, A, Mahmudi, M. and Ebrahimi M. (2019). Identification and evaluation of the antimicrobial potential of strains derived from traditional fermented dairy products of Iran as a biological preservative against Listeria monocytogenes, Staphylococcus aureus, Salmonella enterica and Escherichia coli. Pathogens, 8(2): 71–91.
· Oliveira, P.M., Zannini, E. and Arendt, E.K. (2014). Cereal fungal infection, mycotoxins, and lactic acid bacteria mediated bioprotection: from crop farming to cereal products. Food Microbiology, 37: 78–95.
· Parkin, D.M., Bray, F., Ferlay, J. and Pisani, P. (2005). Global cancer statistics, 2002. CA: A Cancer Journal for Clinicians Cancer, 55: 74–108.
· Pawlowska, A.M., Zannini, E., Coffey, A. and Arendt, E.K. (2012). “Green Preservatives”: combating fungi in the food and feed industry by applying antifungal lactic acid bacteria. Advances in Food and Nutrition Research, 66: 66: 217–238.
· Rossetti, L. and Giraffa, G. (2005). Rapid identification of dairy lactic acid bacteria by M13-generated, RAPD-PCR fingerprint databases. Journal of Microbiological Methods, 63(2): 135-144.
· Rouse, S., Harnett, D., Vaughan, A. and Sinderen D. (2008). Lactic acid bacteria with potential to eliminate fungal spoilage in foods. Journal of Applied Microbiology, 104(3): 915–923.
· Schnürer, J. and Magnusson, J. (2005). Antifungal lactic acid bacteria as biopreservatives. Trends in Food Science and Technology, 16(1): 70–78.
· Sengun, I., Yaman, D. and Gonul, S. (2008). Mycotoxins and mould contamination in cheese: a review. World Mycotoxin Journal, 1(3): 291–298.
· Siedler, S., Balti, R. and Neves, A.R. (2019). Bioprotective mechanisms of lactic acid bacteria against fungal spoilage of food. Current Opinion in Biotechnology, 56: 138-146.
· Stroem, K., Schnuerer, J. and Melin P. (2005). Co-cultivation of antifungal Lactobacillus plantarum MiLAB 393 and Aspergillus nidulans, evaluation of effects on fungal growth and protein expression. FEMS Microbiology Letters, 246: 119–124.
· Tropcheva, R., Nikolova, D., Evstatieva, Y. and Danova, S. 2014. Antifungal activity and identification of Lactobacilli, isolated from traditional dairy product “katak”. Anaerobe, 28: 78-84.
· Yang, E. and Chang, H. (2010). Purification of a new antifungal compound produced by Lactobacillus plantarum AF1 isolated from kimchi. International Journal of Food Microbiology, 139(1): 56–63.
· Zhang, J., Wang, X. J., Yan, Y.J., Jiang, L., Wang, J.D., Li B.J. et al. (2010). Isolation and identification of 5-hydroxyl-5-methyl-2-hexenoic acid from Actinoplanes sp. HBDN08 with antifungal activity. Bioresource Technology, 101(21): 8383–8388.
