Identification and quantification of antifungal compounds produced by lactic acid bacteria and propionibacteria

International Journal of Food Microbiology

Volumn 239, Issue , 2016, Pages 79-85

  Le Lay, Céline ^a   Coton, Emmanuel ^a   Le Blay, Gwenaëlle ^a   Chobert, Jean Marc ^b   Haertlé, Thomas ^b   Choiset, Yvan ^b   Van Long, Nicolas Nguyen ^a   Meslet Cladière, Laurence ^a   Mounier, Jérôme ^a  

^a UNIVERSITÉ DE BREST   (France)

^b INRA   (France)

Author keywords

Antifungal; Germination; Growth; Lactic acid bacteria; Moulds

Indexed keywords

2 DEOXYCITIDINE; 2 HYDROXYDODECANOIC ACID; 3 (4 HYDROXY 3 METHOXYPHENYL)PROPANOIC ACID; 3 (4 HYDROXYPHENYL)PROPIONIC ACID; 3 HYDROXYDECANOIC ACID; 4 HYDROXYBENZOIC ACID; ANTIFUNGAL AGENT; ATROLACTIC ACID; AZELAIC ACID; BENZOIC ACID; CAFFEIC ACID; CATECHOL; CYTIDINE; DECANOIC ACID; DEXTRO LEVO BETA HYDROXYLAURIC ACID; DEXTRO LEVO BETA HYDROXYMYRISTIC ACID; DEXTRO LEVO PARA HYDROXYPHENYLLACTIC ACID; DIHYDROCAFFEIC ACID; FERULIC ACID; GLUCURONIC ACID; HEXANOIC ACID; HYDROCINNAMIC ACID; HYDROGEN PEROXIDE; HYDROXYISOCAPROIC ACID; HYDROXYPHENYLLACTIC ACID; METHYLCINNAMIC ACID; PARA COUMARIC ACID; SALICYLIC ACID; SUCCINIC ACID; UNCLASSIFIED DRUG; VANILLIC ACID; ACETIC ACID; ALCOHOL; DICARBOXYLIC ACID; HEXANOIC ACID DERIVATIVE; LACTIC ACID; PROPIONIC ACID DERIVATIVE;

ANTIFUNGAL ACTIVITY; ARTICLE; ASPERGILLUS NIGER; ASPERGILLUS REPENS; BACTERIUM CULTURE; COLORIMETRY; ENZYMATIC ASSAY; FUNGUS GROWTH; GERMINATION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IN VITRO STUDY; LACTIC ACID BACTERIUM; LACTOBACILLUS BREVIS; LACTOBACILLUS REUTERI; LACTOBACILLUS SPICHERI; LEUCONOSTOC; LEUCONOSTOC CITREUM; MASS SPECTROMETRY; NONHUMAN; PENICILLIUM; PENICILLIUM CORYLOPHILUM; PH; PROPIONIBACTERIACEAE; PROPIONIBACTERIUM FREUDENREICHII; SUPERNATANT; EUROTIUM; FUNGUS SPORE; GROWTH, DEVELOPMENT AND AGING; LACTOBACILLACEAE; METABOLISM; MICROBIAL SENSITIVITY TEST; PROPIONIBACTERIUM;

ACETIC ACID; ANTIFUNGAL AGENTS; ASPERGILLUS NIGER; CAPROATES; DICARBOXYLIC ACIDS; ETHANOL; EUROTIUM; HYDROGEN PEROXIDE; HYDROGEN-ION CONCENTRATION; LACTIC ACID; LACTOBACILLACEAE; MICROBIAL SENSITIVITY TESTS; PENICILLIUM; PROPIONATES; PROPIONIBACTERIUM; SPORES, FUNGAL;

EID: 84977585164     PISSN: 01681605     EISSN: 18793460     Source Type: Journal    
DOI: 10.1016/j.ijfoodmicro.2016.06.020     Document Type: Article

References (48)

1. Axel, C., Brosnan, B., Zannini, E., Peyer, L.C., Furey, A., Coffey, A., Arendt, E.K., Antifungal activities of three different Lactobacillus species and their production of antifungal carboxylic acids in wheat sourdough. Appl. Microbiol. Biotechnol. 100 (2016), 1701–1711.
2. Axel, C., Zannini, E., Arendt, E.K., Mould spoilage of bread and its biopreservation: a review of current strategies for bread shelf life extension. Crit. Rev. Food Sci. Nutr.(0), 2016, 10.1080/10408398.2016.1147417 (Mar 15).
3. Axelsson, L.T., Chung, T.C., Dobrogosz, W.J., Lindgren, S.E., Production of a broad spectrum antimicrobial substance by Lactobacillus reuteri. Microb. Ecol. Health Dis. 2 (1989), 131–136.
4. Batish, V.K., Roy, U., Lal, R., Grower, S., Antifungal attributes of lactic acid bacteria-a review. Crit. Rev. Biotechnol. 17 (1997), 209–225.
5. Bergsson, G., Arnfinnsson, J., Steingrimsson, O., Thormar, H., Killing of gram-positive cocci by fatty acids and monoglycerides. APMIS 109 (2001), 670–678.
6. Biede, S.L., Hammond, E.G., Swiss cheese flavor: II. Organoleptic analysis 1, 2. J. Dairy Sci. 62 (1979), 238–248.
7. Brosnan, B., Coffey, A., Arendt, E.K., Furey, A., Rapid identification, by use of the LTQ Orbitrap hybrid FT mass spectrometer, of antifungal compounds produced by lactic acid bacteria. Anal. Bioanal. Chem. 403 (2012), 2983–2995.
8. Brosnan, B., Coffey, A., Arendt, E.K., Furey, A., The QuEChERS approach in a novel application for the identification of antifungal compounds produced by lactic acid bacteria cultures. Talanta 129 (2014), 364–373.
9. Buckenhüskes, H.J., Jensen, H.A., Andersson, R., Fernández, A.G., Rodrigo, M., Fermented Vegetables. Food Microbiology: Fundamentals and Frontiers, second ed., 1997, ASM Press, Washington, DC, 595–609.
10. Caplice, E., Fitzgerald, G., Food fermentations: role of microorganisms in food production and preservation. Int. J. Food Microbiol. 50 (1999), 131–149.
11. Circle, S.J., Stone, L., Boruff, C.S., Acrolein determination by means of tryptophan. A colorimetric micromethod. Ind. Eng. Chem. Anal. Ed. 17 (1945), 259–262.
12. Cleusix, V., Lacroix, C., Vollenweider, S., Duboux, M., Le Blay, G., Inhibitory activity spectrum of reuterin produced by Lactobacillus reuteri against intestinal bacteria. BMC Microbiol., 7, 2007, 101.
13. Coda, R., Rizzello, G., Nigro, F., De Angelis, M., Arnault, P., Gobbetti, M., Long-term fungal inhibitory activity of water-soluble extracts of Phaseolus vulgaris cv. Pinto and sourdough lactic acid bacteria during bread storage. Appl. Environ. Microbiol. 74 (2008), 7391–7398.
14. Corsetti, A., Gobbetti, M., Rossi, J., Damiani, P., Antimould activity of sourdough lactic acid bacteria: identification of a mixture of organic acids produced by Lactobacillus sanfrancisco CB1. Appl. Microbiol. Biotechnol. 50 (1998), 253–256.
15. Crowley, S., Mahony, J., Van Sinderen, D., Current perspectives on antifungal lactic acid bacteria as natural bio-preservatives. Trends Food Sci. Technol. 33 (2013), 93–109.
16. Dagnas, S., Gauvry, E., Onno, B., Membré, J.-M., Quantifying effect of lactic, acetic, and propionic acids on growth of molds isolated from spoiled bakery products. J. Food Prot. 78 (2015), 1689–1698.
17. Dal Bello, F.D., Clarke, C.I., Ryan, L.A.M., Ulmer, H., Schober, T.J., Ström, K., Sjogren, J., Van Sinderen, D., Schnurer, J., Arendt, E.K., Improvement of the quality and shelf life of wheat bread by fermentation with the antifungal strain Lactobacillus plantarum FST 1.7. J. Cereal Sci. 45 (2007), 309–318.
18. Dang, T.D.T., Vermeulen, A., Ragaert, P., Devlieghere, F., A peculiar stimulatory effect of acetic and lactic acid on growth and fermentative metabolism of Zygosaccharomyces bailii. Food Microbiol. 26 (2009), 320–327.
19. Dantigny, P., Guilmart, A., Radoi, F., Bensoussan, M., Zwietering, M., Modelling the effect of ethanol on growth rate of food spoilage moulds. Int. J. Food Microbiol. 98 (2005), 261–269.
20. Dantigny, P., Nanguy, S.P.M., Judet-Correia, D., Bensoussan, M., A new model for germination of fungi. Int. J. Food Microbiol. 146 (2011), 176–181.
21. Dao, T., Dejardin, J., Bensoussan, M., Dantigny, P., Use of the Weibull model to describe inactivation of dry‐harvested conidia of different Penicillium species by ethanol vapours. J. Appl. Microbiol. 109 (2010), 408–414.
22. Guo, J., Brosnan, B., Furey, A., Arendt, E., Murphy, P., Coffey, A., Antifungal activity of Lactobacillus against Microsporum canis, Microsporum gypseum and Epidermophyton floccosum. Bioeng. Bugs 3 (2012), 104–113.
23. Honoré, A.H., Aunsbjerg, S.D., Ebrahimi, P., Thorsen, M., Benfeldt, C., Knøchel, S., Skov, T., Metabolic footprinting for investigation of antifungal properties of Lactobacillus paracasei. Anal. Bioanal. Chem. 408 (2016), 83–96.
24. Huh, C.K., Hwang, T.Y., Identification of antifungal substances of Lactobacillus sakei subsp. ALI033 and antifungal activity against Penicillium brevicompactum strain FI02. Prev. Nutr. Food Sci. 21 (2016), 52–56.
25. Ito, A., Sato, Y., Kudo, S., Sato, S., Nakajima, H., Toba, T., The screening of hydrogen peroxide-producing lactic acid bacteria and their application to inactivating psychrotrophic food-borne pathogens. Curr. Microbiol. 47 (2003), 231–236.
26. Langa, S., Martín-Cabrejas, I., Montiel, R., Landete, J.M., Medina, M., Arqués, J.L., Short communication: combined antimicrobial activity of reuterin and diacetyl against foodborne pathogens. J. Dairy Sci. 97 (2014), 6116–6121.
27. Lavermicocca, P., Valerio, F., Evidente, A., Lazzaroni, S., Corsetti, A., Gobbetti, M., Purification and characterization of novel antifungal compounds from the sourdough Lactobacillus plantarum strain 21B. Appl. Environ. Microbiol. 66 (2000), 4084–4090.
28. Lavermicocca, P., Valerio, F., Visconti, A., Antifungal activity of phenyllactic acid against molds isolated from bakery products. Appl. Environ. Microbiol. 69 (2003), 634–640.
29. Le Lay, C., Mounier, J., Vasseur, V., Weill, A., Le Blay, G., Barbier, G., Coton, E., In vitro and in situ screening of lactic acid bacteria and propionibacteria antifungal activities against bakery product spoilage molds. Food Control 60 (2016), 247–255.
30. Legan, J.D., Mould spoilage of bread: the problem and some solutions. Int. Biodeterior. Biodegrad. 32 (1993), 33–53.
31. Leistner, L., Stable and Safe Fermented Sausages World-wide. Cook, P.E., (eds.) Campbell-Platt Fermented Meats, 1995, Springer, US, 160–175.
32. Leroy, F., De Vuyst, L., Lactic acid bacteria as functional starter cultures for the food fermentation industry. Trends Food Sci. Technol. 15 (2004), 67–78.
33. Lindgren, S.E., Dobrogosz, W.J., Antagonistic activities of lactic acid bacteria in food and feed fermentations. FEMS Microbiol. Lett. 87 (1990), 149–164.
34. Magnusson, J., Ström, K., Roos, S., Sjögren, J., Schnürer, J., Broad and complex antifungal activity among environmental isolates of lactic acid bacteria. FEMS Microbiol. Lett. 219 (2003), 129–135.
35. Mantere-Alhonen, S., Makinen, E., A new type of sour milk with propionibacteria. Meijeritieteellinen Aikakauskirja 45 (1987), 49–61.
36. Niku‐Paavola, M.L., Laitila, A., Mattila‐Sandholm, T., Haikara, A., New types of antimicrobial compounds produced by Lactobacillus plantarum. J. Appl. Microbiol. 86 (1999), 29–35.
37. Pitt, J.I., Hocking, A.D., Fungi and Food Spoilage. third ed., 2009, Springer, New York.
38. Poute, J.G. Jr., Tsen, C.C., Bakery products. Beuchat, L.R., (eds.) Food and Beverage Mycology, second ed., 1987, AVI Van Nostrand Reinhold, New York, 233–267.
39. Rizzello, C.G., Cassone, A., Coda, R., Gobbetti, M., Antifungal activity of sourdough fermented wheat germ used as an ingredient for bread making. Food Chem. 127 (2011), 952–959.
40. Ryan, L.A., Zannini, E., Dal Bello, F., Pawlowska, A., Koehler, P., Arendt, E.K., Lactobacillus amylovorus DSM 19280 as a novel food-grade antifungal agent for bakery products. Int. J. Food Microbiol. 146 (2011), 276–283.
41. Saithong, P., Panthavee, W., Boonyaratanakornkit, M., Sikkhamondhol, C., Use of a starter culture of lactic acid bacteria in plaa-som, a Thai fermented fish. J. Biosci. Bioeng. 110 (2010), 553–557.
42. Schnürer, J., Magnusson, J., Antifungal lactic acid bacteria as biopreservatives. Trends Food Sci. Technol. 16 (2005), 70–78.
43. Schwenninger, S.M., Lacroix, C., Truttmann, S., Jans, C., Spörndli, C., Bigler, L., Meile, L., Characterization of low-molecular-weight antiyeast metabolites produced by a food-protective Lactobacillus-Propionibacterium coculture. J. Food Prot. 71 (2008), 2481–2487.
44. Sjögren, J., Magnusson, J., Broberg, A., Schnürer, J., Kenne, L., Antifungal 3-hydroxy fatty acids from Lactobacillus plantarum MiLAB 14. Appl. Environ. Microbiol. 69 (2003), 7554–7557.
45. Ström, K., Sjögren, J., Broberg, A., Schnürer, J., Lactobacillus plantarum MiLAB 393 produces the antifungal cyclic dipeptides cyclo (L-Phe-L-pro) and cyclo (L-Phe-trans-4-OH-L-pro) and 3-phenyllactic acid. Appl. Environ. Microbiol. 68 (2002), 4322–4327.
46. Talarico, T.L., Dobrogosz, W.J., Chemical characterization of an antimicrobial substance produced by Lactobacillus reuteri. Antimicrob. Agents Chemother. 33 (1989), 674–679.
47. Thierry, A., Maillard, M.B., Yvon, M., Conversion of L-leucine to isovaleric acid by Propionibacterium freudenreichii TL 34 and ITGP23. Appl. Environ. Microbiol. 68 (2002), 608–615.
48. Valerio, F., Di Biase, M., Lattanzio, V.M., Lavermicocca, P., Improvement of the antifungal activity of lactic acid bacteria by addition to the growth medium of phenylpyruvic acid, a precursor of phenyllactic acid. Int. J. Food Microbiol. 222 (2016), 1–7.