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Inhibitory Activity of Lactic Acid Bacteria against Fungal Spoilage

유산균의 곰팡이 억제 활성

  • Received : 2019.06.18
  • Accepted : 2019.06.26
  • Published : 2019.06.30

Abstract

Food spoilage by fungi is responsible for considerable food waste and economical losses. Among the food products, fermented dairy products are susceptible to deterioration due to the growth of fungi, which are resistant to low pH and can proliferate at low storage temperatures. For controlling fungal growth in dairy products, potassium sorbate and natamycin are the main preservatives used, and natamycin is approved by most countries for use in cheese surface treatment. However, a strong societal demand for less processed and preservative-free food has emerged. In the dairy products, lactic acid bacteria (LAB) are naturally present or used as cultures and play a key role in the fermentation process. Fermentation is a natural preservation technique that improves food safety, nutritional value, and specific organoleptic features. Production of organic acids is one of the main features of the LAB used for outcompeting organisms that cause spoilage, although other mechanisms such as antifungal peptides obtained from the cleavage of food proteins and competition for nutrients also play a role. More studies for better understanding these mechanisms are required to increase antifungal LAB available in the market.

Keywords

References

  1. Arena, M. P., Silvain, A., Normanno, G., Grieco, F., Drider, D., Spano, G. and Fiocco, D. 2016. Use of Lactobacillus plantarum strains as a bio-control strategy against food-borne pathogenic microorganisms. Front. Microbiol. 7:464.
  2. Arroyo-Lopez, F. N., Bautista-Gallego, J., Duran-Quintana, M. C. and Garrido-Fernandez, A. 2008. Modelling the inhibition of sorbic and benzoic acids on a native yeast cocktail from table olives. Food Microbiol. 25:566-574. https://doi.org/10.1016/j.fm.2008.02.007
  3. Aunsbjerg, S. D., Honore, A. H., Marcussen, J., Ebrahimi, P., Vogensen, F. K., Benfeldt, C., Skov, T. and Knochel, S. 2015. Contribution of volatiles to the antifungal effect of Lactobacillus paracasei in defined medium and yogurt. Int. J. Food Microbiol. 194:46-53. https://doi.org/10.1016/j.ijfoodmicro.2014.11.007
  4. Bellamy, W., Wakabayashi, H., Takase, M., Kawase, K., Shimamura, S. and Tomita, M. 1993. Killing of Candida albicans by lactoferricin B, a potent antimicrobial peptide derived from the N-terminal region of bovine lactoferrin. Med. Microbiol. Immunol. 182:97-105. https://doi.org/10.1007/BF00189377
  5. Berni, E. and Scaramuzza, N. 2013. Effect of ethanol on growth of Chrysonilia sitophila ('the red bread mould') and Hyphopichia burtonii ('the chalky mould') in sliced bread. Lett. Appl. Microbiol. 57:344-349. https://doi.org/10.1111/lam.12119
  6. Black, B. A., Zannini, E., Curtis, J. M. and Ganzle, M. G. 2013. Antifungal hydroxy fatty acids produced during sourdough fermentation: microbial and enzymatic pathways, and antifungal activity in bread. Appl. Environ. Microbiol. 79:1866-1873. https://doi.org/10.1128/AEM.03784-12
  7. Bougherra, F., Dilmi-Bouras, A., Balti, R., Przybylski, R., Adoui, F., Elhameur, H., Chevalier, M., Flahaut, C., Dhulster, P. and Naima, N. 2017. Antibacterial activity of new peptide from bovine casein hydrolyzed by a serine metalloprotease of Lactococcus lactis subsp. lactis BR16. J. Funct. Foods. 32:112-122. https://doi.org/10.1016/j.jff.2017.02.026
  8. Broberg, A., Jacobsson, K., Strom, K. and Schnurer, J. 2007. Metabolite profiles of lactic acid bacteria in grass silage. Appl. Environ. Microbiol. 73:5547-5552. https://doi.org/10.1128/AEM.02939-06
  9. Brosnan, B., Coffey, A., Arendt, E. K. and Furey, A. 2012. Rapid identification, by use of the LTQ Orbitrap hybrid FT mass spectrometer, of antifungal compounds produced by lactic acid bacteria. Anal. Bioanal. Chem. 403:2983-2995. https://doi.org/10.1007/s00216-012-5955-1
  10. Brudzynski, K., Abubaker, K., St-Martin, L. and Castle, A. 2011. Re-examining the role of hydrogen peroxide in bacteriostatic and bactericidal activities of honey. Front. Microbiol. 2:213. https://doi.org/10.3389/fmicb.2011.00213
  11. Bruni, N., Capuccino, M. T., Biasibetti, E., Pessione, E., Cirrincione, S., Giraudo, L., Corona, A. and Dosio, F. 2016. Antimicrobial activity of lactoferrin-related peptides and applications in human and veterinary medicine. Molecules. 21:752. https://doi.org/10.3390/molecules21060752
  12. Chen, C., Chen, X., Jiang, M., Rui, X., Li, W. and Dong, M. 2014. A newly discovered bacteriocin from Weissella hellenica D1501 associated with Chinese Dong fermented meat (Nanx Wudl). Food Control. 42:116-124. https://doi.org/10.1016/j.foodcont.2014.01.031
  13. Cleusix, V., Lacroix, C., Vollenweider, S., Duboux, M. and Le Blay, G. 2007. Inhibitory activity spectrum of reuterin produced by Lactobacillus reuteri against intestinal bacteria. BMC Microbiol. 7:101. https://doi.org/10.1186/1471-2180-7-101
  14. Corsetti, A., Gobbetti, M., Rossi, J. and Damiani, P. 1998. Antimould activity of sourdough lactic acid bacteria: identification of a mixture of organic acids produced by Lactobacillus sanfrancisco CB1. Appl. Microbiol. Biotechnol. 50:253-256. https://doi.org/10.1007/s002530051285
  15. Crowley, S., Mahony, J. and van Sinderen, D. 2013. Current perspectives on antifungal lactic acid bacteria as natural bio-preservatives. Trends Food Sci. Technol. 33:93-109. https://doi.org/10.1016/j.tifs.2013.07.004
  16. De Vuyst, L. and Leroy, F. 2007. Bacteriocins from lactic acid bacteria: production, purification, and food applications. J. Mol. Microbiol. Biotechnol. 13:194-199. https://doi.org/10.1159/000104752
  17. Elshaghabee, F. M., Bockelmann, W., Meske, D., de Vrese, M., Walte, H. G., Schrezenmeir, J. and Heller, K. J. 2016. Ethanol production by selected intestinal microorganisms and lactic acid bacteria growing under different nutritional conditions. Front. Microbiol. 7:47. https://doi.org/10.3389/fmicb.2016.00047
  18. Engels, C., Schwab, C., Zhang, J., Stevens, M. J., Bieri, C., Ebert, M. O., McNeill K., Sturla, S. J. and Lacroix C. 2016. Acrolein contributes strongly to antimicrobial and heterocyclic amine transformation activities of reuterin. Sci. Rep. 6:36246. https://doi.org/10.1038/srep36246
  19. Farmery, M., Jones', C., Eady, E., Cove, J. and Cunliffe, W. 1994. In vitro activity of azelaic acid, benzoyl peroxide and zinc acetate against antibiotic-resistant propionibacteria from acne patients. J. Dermatolog. Treat. 5:63-65. https://doi.org/10.3109/09546639409084531
  20. Faruck, M. O., Yusof, F. and Chowdhury, S. 2016. An overview of antifungal peptides derived from insect. Peptides. 80:80-88. https://doi.org/10.1016/j.peptides.2015.06.001
  21. Fermandes, K. E. and Carter, D. A. 2017. The antifungal activity of lactoferrin and its derived peptides: mechanisms of action and synergy with drugs against fungal pathogens. Front. Microbiol. 8:2.
  22. Ganzle, M. G. and Vogel, R. F. 2003. Studies on the mode of action of reutericyclin. Appl. Environ. Microbiol. 69:1305-1307. https://doi.org/10.1128/AEM.69.2.1305-1307.2003
  23. Garmiene, G., Salomskiene, J., Jasutiene, I., Macioniene, I. and Miliauskiene, I. 2010. Production of benzoic acid by lactic acid bacteria from Lactobacillus, Lactococcus and Streptococcus genera in milk. Milchwissenschaft. 65:295-298.
  24. Gerwien, F., Skrahina, V., Kasper, L., Hube, B. and Brunke, S. 2018. Metals in fungal virulence. FEMS Microbiol. Rev. 42:1-21.
  25. Gifford, J. L., Hunter, H. N. and Vogel, H. J. 2005. Lactoferricin: a lactoferrin-derived peptide with antimicrobial, antiviral, antitumor and immunological properties. Cell Mol. Life Sci. 62:2588-2598. https://doi.org/10.1007/s00018-005-5373-z
  26. Guo, J., Brosnan, B., Furey, A., Arendt, E., Murphy, P. and Coffey, A. 2012. Antifungal activity of Lactobacillus against Microsporum canis, Microsporum gypseum and Epidermophyton floccosum. Bioeng. Bugs. 3:104-113.
  27. Hill, R. D., Lahav, E. and Givol, D. 1974. A rennin-sensitive bond in ${\alpha}$s1 B-casein. J. Dairy Res. 41:147-153. https://doi.org/10.1017/S0022029900015028
  28. Honore, A. H., Aunsbjerg, S. D., Ebrahimi, P., Thorsen, M., Benfeldt, C., Knochel, S. and Skov, T. 2016. Metabolic footprinting for investigation of antifungal properties of Lactobacillus paracasei. Anal. Bioanal. Chem. 408:83-96. https://doi.org/10.1007/s00216-015-9103-6
  29. Kashket, E. R. 1987. Bioenergetics of lactic acid bacteria: cytoplasmic pH and osmotolerance. FEMS Microbiol. Lett. 46:233-244. https://doi.org/10.1111/j.1574-6968.1987.tb02463.x
  30. Lahov, E. and Regelson, W. 1996. Antibacterial and immunostimulating casein-derived substances from milk: Casecidin, isracidin peptides. Food Chem. Toxicol. 34:131-145. https://doi.org/10.1016/0278-6915(95)00097-6
  31. Larsen, B. and White, S. 1995. Antifungal effect of hydrogen peroxide on catalaseproducing strains of Candida spp. Infect. Dis. Obstet. Gynecol. 3:73-78. https://doi.org/10.1155/S1064744995000354
  32. Lastauskiene, E., Zinkeviciene, A., Girkontaite, I., Kaunietis, A. and Kvedariene, V. 2014. Formic acid and acetic acid induce a programmed cell death in pathogenic Candida species. Curr. Microbiol. 69:303-310. https://doi.org/10.1007/s00284-014-0585-9
  33. Le Lay, C., Coton, E., Le Blay, G., Chobert, J. M., Haertle, T., Choiset, Y., Van Long, N. N., Meslet-Cladiere, L. and Mounier, J. 2016. Identification and quantification of antifungal compounds produced by lactic acid bacteria and propionibacteria. Int. J. Food Microbiol. 239:79-85. https://doi.org/10.1016/j.ijfoodmicro.2016.06.020
  34. Leon Pelaez, A. M., Serna Catano, C. A., Quintero Yepes, E. A., Gamba Villarroel, R. R., De Antoni, G. L. and Giannuzzi, L. 2012. Inhibitory activity of lactic acid and acetic acid on Aspergillus flavus growth for food preservation. Food Control. 24:177-183. https://doi.org/10.1016/j.foodcont.2011.09.024
  35. Leyva Salas, M., Mounier, J., Valence, F., Coton, M., Thierry, A. and Coton, E. 2017. Antifungal microbial agents for food biopreservation-a review. Microorganisms. 5:37. https://doi.org/10.3390/microorganisms5030037
  36. Lindgren, S. E. and Dobrogosz, W. J. 1990. Antagonistic activities of lactic acid bacteria in food and feed fermentations. FEMS Microbiol. Rev. 7:149-163. https://doi.org/10.1111/j.1574-6968.1990.tb04885.x
  37. Liu, Z., Zeng, M., Dong, S., Xu, J., Song, H. and Zhao, Y. 2007. Effect of an antifungal peptide from oyster enzymatic hydrolysates for control of gray mold (Botrytis cinerea) on harvested strawberries. Postharvest Biol. Technol. 46:95-98. https://doi.org/10.1016/j.postharvbio.2007.03.013
  38. Lupetti, A., Paulusma-Annema, A., Welling M. M., Senesi, S., van Dissel, J. T. and Nibbering, P. H. 2000. Candidacidal activities of human lactoferrin peptides derived from the N terminus. Antimicrob. Agents Chemother. 44:3257-3263. https://doi.org/10.1128/AAC.44.12.3257-3263.2000
  39. Maple, P. A., Hamilton-Miller, J. M. and Brumfitt, W. 1992. Comparison of the in-vitro activities of the topical antimicrobials azelaic acid, nitrofurazone, silver sulphadiazine and mupirocin against methicillin-resistant Staphylococcus aureus. J. Antimicro. Chemother. 29:661-668. https://doi.org/10.1093/jac/29.6.661
  40. Narendranath, N. V., Thomas, K. C. and Ingledew, W. M. 2001. Effects of acetic acid and lactic acid on the growth of Saccharomyces cerevisiae in a minimal medium. J. Ind. Microbiol. Biotechnol. 26:171-177. https://doi.org/10.1038/sj.jim.7000090
  41. Ndagano, D., Lamoureux, T., Dortu, C., Vandermoten, S. and Thonart, P. 2011. Antifungal activity of 2 lactic acid bacteria of the Weissella Genus isolated from food. J. Food Sci. 76:M305-M311. https://doi.org/10.1111/j.1750-3841.2011.02257.x
  42. Niku-Paavola, M. L., Laitila, A., Mattila-Sandholm, T. and Haikara, A. 1999. New types of antimicrobial compounds produced by Lactobacillus plantarum. J. Appl. Microbiol. 86:29-35. https://doi.org/10.1046/j.1365-2672.1999.00632.x
  43. Olonisakin, O. O., Jeff-Agboola, Y. A., Ogidi, C. O. and Akinyele, B. J. 2017. Isolation of antifungal lactic acid bacteria (LAB) from "Kunu" against toxigenic Aspergillus flavus. Prev. Nutr. Food Sci. 22:138-143. https://doi.org/10.3746/pnf.2017.22.2.138
  44. Ostling, C. E. and Lindgren, S. E. 1993. Inhibition of enterobacteria and Listeria growth by lactic, acetic and formic acids. J. Appl. Bacteriol. 75:18-24. https://doi.org/10.1111/j.1365-2672.1993.tb03402.x
  45. Ozcelik, S., Kuley, E. and Ozogul, F. 2016. Formation of lactic, acetic, succinic, propionic, formic and butyric acid by lactic acid bacteria. LWT-Food Sci. Technol. 73:536-542. https://doi.org/10.1016/j.lwt.2016.06.066
  46. Qvirist, L. A., De Filippo, C., Strati, F., Stefanini, I., Sordo, M., Andlid, T., Felis, G. E., Mattarelli, P. and Cavalieri, D. 2016. Isolation, identification and characterization of yeasts from fermented goat milk of the Yaghnob valley in Tajikistan. Front. Microbiol. 7:1-17.
  47. Rautenbach, M., Troskie, A. M. and Vosloo, J. A. 2016. Antifungal peptides: to be or not to be membrane active. Biochimie. 130:132-145. https://doi.org/10.1016/j.biochi.2016.05.013
  48. Rizzello, C. G., Cassone, A., Coda, R. and Gobbetti, M. 2011. Antifungal activity of sourdough fermented wheat germ used as an ingredient for bread making. Food Chem. 127:952-959. https://doi.org/10.1016/j.foodchem.2011.01.063
  49. Russo, P., Fares, C., Longo, A., Spano, G. and Capozzi, V. 2017. Lactobacillus plantarum with broad antifungal activity as a protective starter culture for bread production. Foods. 6:110. https://doi.org/10.3390/foods6120110
  50. Ryan, L. A., Dal Bello, F., Arendt, E. K. and Koehler, P. 2009. Detection and quantitation of 2,5-diketopiperazines in wheat sourdough and bread. J. Agric. Food Chem. 57:9563-9568. https://doi.org/10.1021/jf902033v
  51. Ryan, L. A., Zannini, E., Dal Bello, F., Pawlowska, A., Koehler, P. and Arendt, E. K. 2011. Lactobacillus amylovorus DSM 19280 as a novel food-grade antifungal agent for bakery products. Int. J. Food Microbiol. 146:276-283. https://doi.org/10.1016/j.ijfoodmicro.2011.02.036
  52. Sah, B. N. P., Vasiljevic, T., McKechnie, S. and Donkor, O. N. 2018. Antioxidative and antibacterial peptides derived from bovine milk proteins. Crit. Rev. Food Sci. Nutr. 58:726-740. https://doi.org/10.1080/10408398.2016.1217825
  53. Schaefer, L., Auchtung, T. A., Hermans, K. E., Whitehead, D., Borhan, B. and Britton, R. A. 2010. The antimicrobial compound reuterin (3-hydroxypropionaldehyde) induces oxidative stress via interaction with thiol groups. Microbiology. 156:1589-1599. https://doi.org/10.1099/mic.0.035642-0
  54. Schnurer, J. and Magnusson, J. 2005. Antifungal lactic acid bacteria as biopreservatives. Trends Food Sci. Technol. 16:70-78. https://doi.org/10.1016/j.tifs.2004.02.014
  55. Schwenninger, S. M., Lacroix, C., Truttmann, S., Jans, C., Sporndli, C., Bigler, L. and Meile, L. 2008. Characterization of low-molecular-weight antiyeast metabolites produced by a food-protective Lactobacillus-Propionibacterium coculture. J. Food Prot. 71:2481-2487. https://doi.org/10.4315/0362-028X-71.12.2481
  56. Siedler, S., Balti, R. and Neves, A. R. 2019. Bioprotective mechanisms of lactic acid bacteria against fungal spoilage of food. Curr. Opin. Biotechnol. 56:138-146. https://doi.org/10.1016/j.copbio.2018.11.015
  57. Sjogren, J., Magnusson, J., Broberg, A., Schnurer, J. and Kenne, L. 2003. Antifungal 3-hydroxy fatty acids from Lactobacillus plantarum MiLAB 14. Appl. Environ. Microbiol. 69:7554-7557. https://doi.org/10.1128/AEM.69.12.7554-7557.2003
  58. Song, R., Shi, Q, Gninguue, A., Wei, R. and Luo, H. 2017. Purification and identification of a novel peptide derived from by-products fermentation of spiny head croaker (Collichthys lucidus) with antifungal effects on phytopathogens. Process Biochem. 62:184-192. https://doi.org/10.1016/j.procbio.2017.07.024
  59. Stratford, M., Plumridge, A., Nebe-von-Caron, G. and Archer, D. B. 2009. Inhibition of spoilage mould conidia by acetic acid and sorbic acid involves different modes of action, requiring modification of the classical weak-acid theory. Int. J. Food Microbiol. 136:37-43. https://doi.org/10.1016/j.ijfoodmicro.2009.09.025
  60. Strom, K., Sjogren, J., Broberg, A. and Schnurer, J. 2002. Lactobacillus plantarum MiLAB 393 produces the antifungal cyclic dipeptides cyclo(L-Phe-L-Pro) and cyclo (L-Phetrans-4-OH-L-Pro) and 3-phenyllactic acid. Appl. Environ. Microbiol. 68:4322-4327. https://doi.org/10.1128/AEM.68.9.4322-4327.2002
  61. Urbiene, S. and Leskauskaite, D. 2006. Formation of some organic acids during fermentation of milk. Pol. J. Food Nutr. Sci. 56:277-281.
  62. Valerio, F., Lavermicocca, P., Pascale, M. and Visconti, A. 2004. Production of phenyllactic acid by lactic acid bacteria: an approach to the selection of strains contributing to food quality and preservation. FEMS Microbiol. Lett. 233:289-295. https://doi.org/10.1111/j.1574-6968.2004.tb09494.x
  63. Vandenbergh, P. A. 1993. Lactic acid bacteria, their metabolic products and interference with microbial growth. FEMS Microbiol. Rev. 12:221-237. https://doi.org/10.1111/j.1574-6976.1993.tb00020.x
  64. Yang, E. J. Kim, Y. S. and Chang, H. C. 2011. Purification and characterization of antifungal $\delta$-dodecalactone from Lactobacillus plantarum AF1 isolated from Kimchi. J. Food Prot. 74:651-657. https://doi.org/10.4315/0362-028X.JFP-10-512
  65. Yang, E., Fan, L., Jiang, Y., Doucette, C. and Fillmore, S. 2012. Antimicrobial activity of bacteriocin-producing lactic acid bacteria isolated from cheeses and yogurts. AMB Express. 2:1-12. https://doi.org/10.1186/2191-0855-2-1
  66. Yeaman, M. R. and Yount, N. Y. 2003. Mechanisms of antimicrobial peptide action and resistance. Pharmacol. Rev. 55:27-55. https://doi.org/10.1124/pr.55.1.2
  67. Yu, H. S., Lee, N. K., Jeon, H. L., Eom, S. J., Yoo, M. Y., Lim S. D. and Paik, H. D. 2016. Benzoic acid production with respect to starter culture and incubation temperature during yogurt fermentation using response surface methodology. Korean J. Food Sci. Anim. Resour. 36:427-434. https://doi.org/10.5851/kosfa.2016.36.3.427
  68. Zerva, L., Hollis, R. J. and Pfaller, M. A. 1996. In vitro susceptibility testing and DNA typing of Saccharomyces cerevisiae clinical isolates. J. Clin. Microbiol. 34:3031-3034. https://doi.org/10.1128/JCM.34.12.3031-3034.1996
  69. Zhang, C., Brandt, M. J., Schwab, C. and Ganzle, M. G. 2010. Propionic acid production by cofermentation of Lactobacillus buchneri and Lactobacillus diolivorans in sourdough. Food Microbiol. 27:390-395. https://doi.org/10.1016/j.fm.2009.11.019

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