Aktywność przeciwgrzybowa bakterii fermentacji mlekowej z rodzaju Lactobacillus

• Autorzy: Elżbieta Klewicka , Lidia Lipińska

Warianty tytułu

Antifungal Activity of Lactic Acid Bacteria of Lactobacillus Genus

• Języki publikacji: PL

Abstrakty

Jedną z metod ochrony żywności fermentowanej przed bytującymi w niej niepożądanymi mikroorganizmami jest zastosowanie bakterii mlekowych jako naturalnych biokonserwantów. Szczególnie korzystna jest obecność bakterii fermentacji mlekowej (LAB) w żywności. Oprócz spodziewanej aktywności antybakteryjnej i przeciwgrzybowej LAB cechują się korzystnym wpływem na organizm człowieka poprzez stymulowanie przewodu pokarmowego do zapobiegania zakażeniom pokarmowym i poprawę ogólnego stanu zdrowia. Spektrum aktywności przeciwgrzybowej bakterii z rodzaju Lactobacillus, która jest głównym przedmiotem niniejszej publikacji, wynika z syntezy metabolitów o właściwościach przeciwgrzybowych: pierwotnych - kwas mlekowy i kwas octowy oraz wtórnych - inne kwasy organiczne, cykliczne dipeptydy, kwasy tłuszczowe i ich hydroksylowane pochodne, związki niskocząsteczkowe, bakteriocyny, nadtlenek wodoru. Zdolność do syntezy powyższych związków nie jest cechą wszystkich bakterii z rodzaju Lactobacillus, a jedynie cechą szczepową pojedynczych kultur. Z tego względu poszukuje się szczepów bakterii mlekowych o szerokim spektrum aktywności antagonistycznej wobec grzybów, a także sposobów rozszerzenia tej aktywności, np. przez dobór optymalnych warunków fermentacji czy modyfikację składu podłoża i tym samym zmianę metabolizmu bakterii. (abstrakt oryginalny)

EN

One of the methods of protecting fermented foods against undesirable microorganisms living therein is using the lactic acid bacteria as natural bio-preservatives. The occurrence of lactic acid bacteria (LAB) in food is particularly beneficial. In addition to their expected antibacterial and antifungal activities, LAB are also characterized by their advantageous effect on human health for they stimulate gastrointestinal track to prevent food-borne infections and they improve overall health. The spectrum of antifungal activity of bacteria of the Lactobacillus genus, which is the main subject in this paper, results from the synthesis of metabolites with antifungal properties, i.e. of primary metabolites: lactic acid and acetic acid, and of secondary metabolites: other organic acids, cyclic dipeptides, fatty acids and their hydroxylated derivatives, low molecular weight compounds, bacteriocins, and hydrogen peroxide. The ability to synthesize the above named compounds is not a feature common to all bacteria of the Lactobacillus genus; it is a strainlinked ability of some individual bacterial cultures. Therefore, such strains of lactic acid bacteria are sought, which have a broad spectrum of antagonistic activity against fungi as are the methods of increasing that activity, for example by selecting optimal conditions of the fermentation process or by modifying the composition of a medium, thus, changing the metabolism of lactic acid bacteria. (original abstract)

Słowa kluczowe

PL

Żywność; Jakość żywności; Mikrobiologia; Towaroznawstwo żywności

EN

Food; Food quality; Microbiology; Food commodities

• Czasopismo: Żywność: nauka - technologia - jakość
• Rocznik: 23 (2016)
• Numer: nr 1 (104)
• Strony: 17--31

Twórcy

autor

Elżbieta Klewicka

• Politechnika Łódzka

autor

Lidia Lipińska

• Politechnika Łódzka

Bibliografia

• [1] Ahmadova A., Todorov S.D., Hadji-Sfaxi I., Choiset Y., Rabesona H., Messaoudi S., Kuliyev A., Franco B.D., Chobert J.M., Haertlé T.: Antimicrobial and antifungal activities of Lactobacillus curvatus strain isolated from homemade Azerbaijani cheese. Anaerobe, 2013, 20, 42-49.
• [2] Arasu M.V., Al-Dhabi N.A., Rejiniemon T.S., Lee K.D., Huxley V.A.J., Kim D.H., Duraipandiyan V., Karuppiah P., Choi K.C.: Identification and characterization of Lactobacillus brevis P68 with antifungal, antioxidant and probiotic functional properties. Indian J. Microbiol., 2015, 55 (1), 19-28.
• [3] Arouri A., Mouritsen O.G.: Membrane-perturbing effect of fatty acids and lysolipids. Prog. Lipid Res., 2013, 52 (1), 130-140.
• [4] Axel C., Zannini E., Arendt E.K., Waters D.M., Czerny M.: Quantification of cyclic dipeptides from cultures of Lactobacillus brevis R2Δ by HRGC/MS using stable isotope dilution assay. Anal. Bioanal. Chem., 2014, 406 (9-10), 2433-2444.
• [5] Belguesmia Y., Rabesona H., Mounier J., Pawtowsky A., Le Blay G., Barbier G., Haertlé T., Chobert J.M.: Characterization of antifungal organic acids produced by Lactobacillus harbinensis K.V9.3.1Np immobilized in gellan-xanthan beads during batch fermentation. Food Control, 2014, 36 (1), 205-211.
• [6] Belz M.C., Mairinger R., Zannini E., Ryan L.A., Cashman K.D., Arendt E.K.: The effect of sourdough and calcium propionate on the microbial shelf-life of salt reduced bread. Appl. Microbiol. Biotechnol., 2012, 96 (2), 493-501.
• [7] Black B.A., Zannini E., Curtis J.M., Gänzle M.G.: 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.
• [8] Cheong E.Y.L., Sandhu A., Jayabalan J., Kieu Le T.T., Nhiep N.T., My Ho H.T., Zwielehner J., Bansa N., Turner M.S.: Isolation of lactic acid bacteria with antifungal activity against the common cheese spoilage mould P. commune and their potential as biopreservatives in cheese. Food Control, 2014, 46, 91-97.
• [9] Cortés-Zavaleta O., López-Malo A., Hernández-Mendoza A., García H.S.: Antifungal activity of lactobacilli and its relationship with 3-phenyllactic acid production. Int. J. Food Microbiol., 2014, 173, 30-35.
• [10] Crowley S., Mahony J., Morrissey J.P., Van Sinderen D.: Transcriptomic and morphological profiling of Aspergillus fumigatus Af293 in response to antifungal activity produced by Lactobacillus plantarum 16. Microbiology, 2013, 159 (Pt 10), 2014-2024.
• [11] Crowley S., Mahony J., Van Sinderen D.: Broad-spectrum antifungal-producing lactic acid bacteria and their application in fruit models. Folia Microbiol., 2013, 58 (4), 291-299.
• [12] Dal Bello F., Clarke C.I., Ryan L.A.M., Ulmer H., Schober T.J., Ström K., Sjögren J., Van Sinderen D., Schnürer 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., 2007, 45 (3), 309-318.
• [13] De Muynck C., Leroy A.I., De Maeseneire S., Arnaut F., Soetaert W., Vandamme E.J.: Potential of selected lactic acid bacteria to produce food compatible antifungal metabolites. Microbiol. Res., 2004, 159 (4), 339-346.
• [14] Delavenne E., Cliquet S., 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 (Pt A), 10-17. DOI: 10.1016/j.fm.2014.04.017.
• [15] Delavenne E., Ismail R., Pawtowski A., Mounier J., Barbier G., Le Blay G.: Assessment of lactobacilli strains as yogurt bioprotective cultures. Food Control, 2013, 30 (1), 206-213.
• [16] Delavenne E., Mounier J., Déniel F., Barbier G., Le Blay G.: Biodiversity of antifungal lactic acid bacteria isolated from raw milk samples from cow, ewe and goat over one-year period. Int. J. Food Microbiol., 2012, 155 (3), 185-190.
• [17] Falagas M.E., Betsi G.I., Athanasiou S.: Probiotics for prevention of recurrent vulvovaginal candidiasis: A review. J. Antimicrob. Chemother., 2006, 58 (2), 266-272.
• [18] Fhoula I., Najjari A., Turki Y., Jaballah S., Boudabous A., Ouzari H.: Diversity and antimicrobial properties of lactic acid bacteria isolated from rhizosphere of olive trees and desert truffles of Tunisia. Biomed Res. Int., 2013, 2013, 1-14.
• [19] Gerez C.L., Torres M.J., Font de Valdez G., Rollán G.: Control of spoilage fungi by lactic acid bacteria. Biol. Control, 2013, 64 (3), 231-237.
• [20] Goderska K., Rychlik T., Andrzejewska E., Szkaradkiewicz A., Czarnecki Z.: Antagonistyczny wpływ Lactobacillus acidophilus DSM 20079 i DSM 20242 na bakterie patogenne izolowane od ludzi. Żywność. Nauka. Technologia. Jakość, 2012, 82 (3), 114-131.
• [21] 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, 2012, 3 (2), 104-113.
• [22] Gupta R., Srivastava S.: Antifungal effect of antimicrobial peptides (AMPs LR14) derived from Lactobacillus plantarum strain LR/14 and their applications in prevention of grain spoilage. Food Microbiol., 2014, 42, 1-7.
• [23] Hassan Y.I., Bullerman L.B.: Antifungal activity of Lactobacillus paracasei ssp tolerans isolated from a sourdough bread culture. Int. J. Food Microbiol., 2008, 121 (1), 112-115.
• [24] Ho P.H., Luo J.B., Adams M.C.: Lactobacilli and dairy propionibacterium with potential as biopreservatives against food fungi and yeast contamination. Appl. Biochem. Microbiol., 2009, 45 (4), 414-418.
• [25] Kim J.D.: Antifungal activity of lactic acid bacteria isolated from Kimchi against Aspergillus fumigatus. Mycobiology, 2005, 33 (4), 210-214.
• [26] Klewicka E.: Antifungal activity of lactic acid bacteria of genus Lactobacillus sp. In the presence of polyols. Acta Alimentaria, 2007, 36 (4), 495-499.
• [27] Klewicka E., Klewicki R.: In vitro fermentation of galactosyl derivatives of polyols by Lactobacillus strains. Czech J. Food Sci., 2009, 27 (1), 65-70.
• [28] Klewicka E., Libudzisz Z.: Antagonistic activity of Lactobacillus acidophilus bacteria toward selected food-contaminating bacteria. Pol. J. Food Nutr. Sci., 2004, 13/54 (2), 169-174.
• [29] Klewicki R., Klewicka E.: Antagonistic activity of lactic acid bacteria as probiotics against selected bacteria of the Enterobaceriacae family in the presence of polyols and their galactosyl derivatives. Biotechnol. Lett., 2004, 26 (4), 317-320.
• [30] Köhler G.A., Assefa S., Reid G.: Probiotic interference of Lactobacillus rhamnosus GR-1 and Lactobacillus reuteri RC-14 with the opportunistic fungal pathogen Candida albicans. Infect. Dis. Obstet. Gynecol., 2012, 2012, 1-14.
• [31] Kwak M.K., Liu R., Kim M.K., Moon D., Kim A.H., Song S.H., Kang S.O.: Cyclic dipeptides from lactic acid bacteria inhibit the proliferation of pathogenic fungi. J. Microbiol., 2014, 52 (1), 64-70.
• [32] Li H., Liu L., Zhang S., Cui W., Lv J.: Identification of antifungal compounds produced by Lactobacillus casei AST18. Curr. Microbiol., 2012, 65 (2), 156-161.
• [33] Li H., Liu L., Zhang S., Uluko H., Cui W., Lv J.: Potential use of Lactobacillus casei AST18 as a bioprotective culture in yogurt. Food Control, 2013, 34 (2), 675-680.
• [34] Li H., Zhang S., Lu J., Liu L., Uluko H., Pang X., Sun Y., Xue H., Zhao L., Kong F., Lv J.: Antifungal activities and effect of Lactobacillus casei AST18 on the mycelia morphology and ultrastructure of Penicillium chrysogenum. Food Control, 2014, 43, 57-64.
• [35] Lynch K.M., Pawlowska A.M., Brosnan B., Coffey A., Zannini E., Furey A., McSweeney P.L.H., Waters D.M., Arendt E.K.: Application of Lactobacillus amylovorus as an antifungal adjunct to extend the shelf-life of Cheddar cheese. Int. Dairy J., 2014, 34 (1), 167-173.
• [36] Magnusson J.: Antifungal activity of lactic acid bacteria. PhD thesis, Swedish University of Agricultural Sciences, Uppsala, Sweden 2003, 397.
• [37] Mauch A., Dal Bello F., Coffey A., Arendt E.K.: The use of Lactobacillus brevis PS1 to in vitro inhibit the outgrowth of Fusarium culmorum and other common Fusarium species found on barley. Int. J. Food Microbiol., 2010, 141 (1-2), 116-121.
• [38] Mu W., Yang Y., Jia J., Zhang T., Jiang B.: Production of 4-hydroxyphenyllactic acid by Lactobacillus sp. SK007 fermentation. J. Biosci. Bioeng., 2010, 109 (4), 369-371.
• [39] Mu W., Yu S., Zhu L., Zhang T., Jiang B.: Recent research on 3-phenyllactic acid, a broad-spectrum antimicrobial compound. Appl. Microbiol. Biotechnol., 2012, 95 (5), 1155-1163.
• [40] Nyanzi R., Awouafack M.D., Steenkamp P., Jooste P.J., Eloff J.N.: Anticandidal activity of cell extracts from 13 probiotic Lactobacillus strains and characterisation of lactic acid and a novel fatty acid derivative from one strain. Food Chem., 2014, 164, 470-475.
• [41] Ogunshe A.A.O., Omotoso M.A., Bello V.B.: The in vitro antimicrobial activities of metabolites from lactobacillus strains on Candida species implicated in Candida vaginitis. Malays J. Med. Sci., 2011, 18 (4), 13-25.
• [42] Oranusi S.U., Braide W., Oguoma O.I.: Antifungal properties of lactic acid bacteria (LAB) isolated from Ricinus communis, Pentaclethra macrophylla and yoghurts. 2013, Glob. Adva. Res. J. Food Sci. Technol., 2013, 2 (1), 01-06.
• [43] Quan X., Zhang L., Li Y., Liang C.: TCF2 Attenuates FFA-induced damage in islet β-cells by regulating production of insulin and ROS. Int. J. Mol. Sci., 2014, 15 (8), 13317-13332.
• [44] Rather I.A., Seo B.J., Rejish Kumar V.J., Choi U.H., Choi K.H., Lim J.H., Park Y.H.: Isolation and characterization of a proteinaceous antifungal compound from Lactobacillus plantarum YML007 and its application as a food preservative. Lett. Appl. Microbiol., 2013, 57 (1), 69-76.
• [45] 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., 2011, 127 (3), 952-959.
• [46] 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.
• [47] 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., 2011, 146 (3), 276-283.
• [48] 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.
• [49] Schnürer J., Magnusson J.: Antifungal lactic acid bacteria as biopreservatives. 2005, Trends Food Sci. Technol., 2005, 16 (1-3), 70-78.
• [50] Schwenninger S.M., Meile L.: A mixed culture of Propionibacterium jensenii and Lactobacillus paracasei subsp. paracasei inhibits food spoilage yeasts. Syst. Appl. Microbiol., 2004, 27, 229-237.
• [51] Sjögren J., Magnusson J., Broberg A., Schnürer J., Kenne L.: Antifungal 3-hydroxy fatty acids from Lactobacillus plantarum MiLAB 14. Appl. Environ. Microbiol., 2003, 69 (12), 7554-7557.
• [52] Sorrentino E., Reale A., Tremonte P., Maiuro L., Succi M., Tipaldi L., Coppola R.: Lactobacillus plantarum 29 inhibits Penicillium spp. involved in the spoilage of black truffles (Tuber aestivum). J. Food Sci., 2013, 78 (8), M1188-M1194.
• [53] Souza J.L., Da Silva A.F., Carvalho P.H., Pacheco B.S., Pereira C.M., Lund R.G.: Aliphatic fatty acids and esters: Inhibition of growth and exoenzyme production of Candida, and their cytotoxicity in vitro: Anti-Candida effect and cytotoxicity of fatty acids and esters. Arch. Oral. Biol., 2014, 59 (9), 880-886.
• [54] 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., 2002, 68 (9), 4322-4327.
• [55] Suomalainen T.H., Mäyrä-Mäkinen A.M.: Propionic acid bacteria as protective cultures in fermented milks and breads. Le Lait, 1999, 79 (1), 165-174.
• [56] Tropcheva R., Nikolova D., Evstatieva Y., Danova S.: Antifungal activity and identification of Lactobacilli, isolated from traditional dairy product "katak". Anaerobe, 2014, 28, 78-84.
• [57] Valan Arasu M., Jung M.W., Ilavenil S., Jane M., Kim D.H., Lee K.D., Park H.S., Hur T.Y., Choi G.J., Lim Y.C., Al-Dhabi N.A., Choi K.C.: Isolation and characterization of antifungal compound from Lactobacillus plantarum KCC-10 from forage silage with potential beneficial properties. J. Appl. Microbiol., 2013, 115 (5), 1172-1185.
• [58] Varsha K.K., Priya S., Devendra L., Nampoothiri K.M.: Control of spoilage fungi by protective lactic acid bacteria displaying probiotic properties. Appl. Biochem. Biotechnol., 2014, 172 (7), 3402-3413.
• [59] Voulgari K., Hatzikamari M., Delepoglou A., Georgakopoulos P., Litopoulou-Tzanetaki E., Tzanetakis N.: Antifungal activity of non-starter lactic acid bacteria isolates from dairy products. Food Control, 2010, 21 (2), 136-142.
• [60] Wang H., Sun Y., Chen Ch., Sun Z., Zhou Y., Shen F., Zhang H., Dai Y.: Genome shuffling of Lactobacillus plantarum for improving antifungal activity. Food Control, 2013, 32 (2), 341-347.
• [61] Yang E.J., Chang H.C.: Antifungal activity of Lactobacillus plantarum isolated from kimchi. Korean J. Microbiol. Biotechnol., 2008, 36 (4), 276-284.
• [62] Yang E.J., Chang H.C.: Purification of a new antifungal compound produced by Lactobacillus plantarum AF1 isolated from kimchi. Int. J. Food Microbiol., 2010, 139 (1-2), 56-63.
• [63] Yang S.C., Lin Ch.H., Sung C.T., Fang J.Y.: Antibacterial activities of bacteriocins: application in foods and pharmaceuticals. Front Microbiol., 2014, 5, 241.
• [64] Zamani-Zadeh M., Soleimanian-Zad S., Sheikh-Zeinoddin M.: Biocontrol of gray mold disease on strawberry fruit by integration of Lactobacillus plantarum A7 with ajwain and cinnamon essential oils. J. Food Sci., 2013, 78 (10), M1582-M1588.
• [65] Zheng J., Gänzle M.G., Lin X.B., Ruan L., Sun M.: Diversity and dynamics of bacteriocins from human microbiome. Environ. Microbiol., 2015, 17(6), 2133-2143.

Identyfikatory

DOI

10.15193/zntj/2016/104/098