Generic placeholder image

Current Green Chemistry

Author(s): Rubi Ahuja and Minhaj Ahmad Khan*

DOI: 10.2174/0122133461284473240408075321

DownloadDownload PDF Flyer Cite As
Lactic Acid Bacteria As Biological Control Agent For Controlling Aspergillus Growth and Aflatoxin Production: A Review

Page: [351 - 368] Pages: 18

  • * (Excluding Mailing and Handling)

Explore Articles
About Journal
For Authors
For Editors
For Reviewers

Abstract

Aspergillus sp., a ubiquitous filamentous fungus, poses significant challenges to the food industry as a common spoilage and mycotoxin producing organism. The conventional use of chemical preservatives to control Aspergillus contamination raises concerns about potential health risks and environmental impacts. Therefore, alternative approaches, such as the utilization of natural biopreservatives, as inexpensive, safe, and promising mycotoxin decontamination strategies are being explored. Lactic acid bacteria have gained considerable attention as potential candidates due to their antimicrobial properties and long-standing safe use in food fermentation. This review provides a thorough summary of the potential of lactic acid bacteria as biopreservatives against Aspergillus sp. The inhibitory mechanisms of lactic acid bacteria against the proliferation of Aspergillus and mycotoxin yield are explored, highlighting the role of organic acids, antimicrobial peptides, and other bioactive compounds. The versatile application of lactic acid bacteria based natural preservatives across a range of food matrices, storage conditions, etc. is also addressed. Further research is warranted to optimize lactic acid bacteria strains, explore synergistic combinations, and investigate their efficacy in real food systems. Implementing lactic acid bacteria based biopreservative strategies could significantly enhance food safety and quality by reducing Aspergillus contamination and mycotoxin risks.

Keywords: Biopreservative, mycotoxin, surface assimilation, inhibition, antifungal product, bacteriocin, detoxification.

Graphical Abstract

[1]
Meijer, G.W.; Lähteenmäki, L.; Stadler, R.H.; Weiss, J. Issues surrounding consumer trust and acceptance of existing and emerging food processing technologies. Crit. Rev. Food Sci. Nutr., 2021, 61(1), 97-115.
[http://dx.doi.org/10.1080/10408398.2020.1718597] [PMID: 32003225]
[2]
Mahato, D.K.; Lee, K.E.; Kamle, M.; Devi, S.; Dewangan, K.N.; Kumar, P.; Kang, S.G. Aflatoxins in food and feed: An overview on prevalence, detection and control strategies. Front. Microbiol., 2019, 10, 2266.
[http://dx.doi.org/10.3389/fmicb.2019.02266] [PMID: 31636616]
[3]
Adeyeye, S.A.O. Mycotoxins in foods: Impact on health. Current Developments in Biotechnology and Bioengineering; Elsevier, 2022, pp. 261-271.
[4]
Kolawole, O.; Meneely, J.; Petchkongkaew, A.; Elliott, C. A review of mycotoxin biosynthetic pathways: Associated genes and their expressions under the influence of climatic factors. Fungal Biol. Rev., 2021, 37, 8-26.
[http://dx.doi.org/10.1016/j.fbr.2021.04.003]
[5]
Roze, L.V.; Hong, S.Y.; Linz, J.E. Aflatoxin biosynthesis: current frontiers. Annu. Rev. Food Sci. Technol., 2013, 4(1), 293-311.
[http://dx.doi.org/10.1146/annurev-food-083012-123702] [PMID: 23244396]
[6]
Awuchi, C.G.; Ondari, E.N.; Ogbonna, C.U.; Upadhyay, A.K.; Baran, K.; Okpala, C.O.R.; Korzeniowska, M.; Guiné, R.P.F. Mycotoxins affecting animals, foods, humans, and plants: Types, occurrence, toxicities, action mechanisms, prevention, and detoxification strategies—A revisit. Foods, 2021, 10(6), 1279.
[http://dx.doi.org/10.3390/foods10061279] [PMID: 34205122]
[7]
Kumar, LK; Verma, SK; Chandel, R; Thumar, M; Singh, D; Onteru, SK. Aflatoxin M1 causes cytotoxicity and intestinal epithelial cell integrity damage in differentiated human Caco-2 cells. Res. Sq., 2023, PPR666352.
[http://dx.doi.org/10.21203/rs.3.rs-2927109/v1]
[8]
Kumar, P.; Mahato, D.K.; Kamle, M.; Mohanta, T.K.; Kang, S.G. Aflatoxins: A global concern for food safety, human health and their management. Front. Microbiol., 2017, 7, 2170.
[http://dx.doi.org/10.3389/fmicb.2016.02170] [PMID: 28144235]
[9]
Peivasteh-Roudsari, L; Pirhadi, M; Shahbazi, R; Eghbaljoo-Gharehgheshlaghi, H; Sepahi, M; Mirza Alizadeh, A Mycotoxins: Impact on health and strategies for prevention and detoxification in the food chain. Food. Rev. Int., 2022, 38(sup1), 193-224.
[10]
Balan, B.; Dhaulaniya, A.S.; Kumar, M.; Kumar, M.; Kumar, P. Aflatoxins in food: Prevalence, health effects, and emerging trends in its mitigation: An updated review. Food Safety and Health, 2024, 2(1), 1-6.
[11]
Verheecke, C.; Liboz, T.; Darriet, M.; Sabaou, N.; Mathieu, F. in vitro interaction of actinomycetes isolates with Aspergillus flavus: Impact on aflatoxins B1 and B2 production. Lett. Appl. Microbiol., 2014, 58(6), 597-603.
[http://dx.doi.org/10.1111/lam.12233] [PMID: 24698210]
[12]
Shehata, M.G.; Badr, A.N.; El Sohaimy, S.A.; Asker, D.; Awad, T.S. Characterization of antifungal metabolites produced by novel lactic acid bacterium and their potential application as food biopreservatives. Ann. Agric. Sci., 2019, 64(1), 71-78.
[http://dx.doi.org/10.1016/j.aoas.2019.05.002]
[13]
Greeff-Laubscher, M.R.; Beukes, I.; Marais, G.J.; Jacobs, K. Mycotoxin production by three different toxigenic fungi genera on formulated abalone feed and the effect of an aquatic environment on fumonisins. Mycology, 2020, 11(2), 105-117.
[http://dx.doi.org/10.1080/21501203.2019.1604575] [PMID: 32923019]
[14]
Medeiros, F.H.V.; Martins, S.J.; Zucchi, T.D.; Melo, I.S.; Batista, L.R.; Machado, J.C. Biological control of mycotoxin-producing molds. Cienc. Agrotec., 2012, 36(5), 483-497.
[http://dx.doi.org/10.1590/S1413-70542012000500001]
[15]
Abedi, E.; Pourmohammadi, K.; Mousavifard, M.; Sayadi, M. Comparison between surface hydrophobicity of heated and thermosonicated cells to detoxify aflatoxin B1 by co-culture Lactobacillus plantarum and Lactobacillus rhamnosus in sourdough: Modeling studies. Lebensm. Wiss. Technol., 2022, 154, 112616.
[http://dx.doi.org/10.1016/j.lwt.2021.112616]
[16]
Samuel, A. Fungal mycotoxins in foods: A review. Cogent Food Agric., 2016, 2, 121-127.
[17]
Bansal, A.; Sharma, M.; Pandey, A.; Shankar, J. Aflatoxins: Occurrence, Biosynthesis Pathway, Management, and Impact on Health. In: Fungal Resources for Sustainable Economy: Current Status and Future Perspectives; Springer, 2023; pp. 565-594.
[http://dx.doi.org/10.1007/978-981-19-9103-5_21]
[18]
Omara, T.; Kiprop, A.K.; Wangila, P.; Wacoo, A.P.; Kagoya, S.; Nteziyaremye, P.; Peter Odero, M.; Kiwanuka Nakiguli, C.; Baker Obakiro, S. The scourge of aflatoxins in Kenya: A 60-year review (1960 to 2020). J. Food Qual., 2021, 2021, 1-31.
[http://dx.doi.org/10.1155/2021/8899839]
[19]
Wacoo, A.; Mukisa, I.; Meeme, R.; Byakika, S.; Wendiro, D.; Sybesma, W.; Kort, R. Probiotic enrichment and reduction of aflatoxins in a traditional African maize-based fermented food. Nutrients, 2019, 11(2), 265.
[http://dx.doi.org/10.3390/nu11020265] [PMID: 30691002]
[20]
Misihairabgwi, J.M.; Ezekiel, C.N.; Sulyok, M.; Shephard, G.S.; Krska, R. Mycotoxin contamination of foods in Southern Africa: A 10-year review (2007–2016). Crit. Rev. Food Sci. Nutr., 2019, 59(1), 43-58.
[http://dx.doi.org/10.1080/10408398.2017.1357003] [PMID: 28799776]
[21]
Joshi, P.; Chauysrinule, C.; Mahakarnchanakul, W.; Maneeboon, T. Multi-mycotoxin contamination, mold incidence and risk assessment of aflatoxin in maize kernels originating from Nepal. Microbiol. Res., 2022, 13(2), 258-277.
[http://dx.doi.org/10.3390/microbiolres13020021]
[22]
Zhang, W.; Liu, Y.; Liang, B.; Zhang, Y.; Zhong, X.; Luo, X.; Huang, J.; Wang, Y.; Cheng, W.; Chen, K. Probabilistic risk assessment of dietary exposure to aflatoxin B1 in Guangzhou, China. Sci. Rep., 2020, 10(1), 7973.
[http://dx.doi.org/10.1038/s41598-020-64295-8] [PMID: 32409649]
[23]
Udovicki, B.; Djekic, I.; Gajdos Kljusuric, J.; Papageorgiou, M.; Skendi, A.; Djugum, J.; Rajkovic, A. Exposure assessment and risk characterization of aflatoxins intake through consumption of maize products in the adult populations of Serbia, Croatia and Greece. Food Addit. Contam. Part A Chem. Anal. Control Expo. Risk Assess., 2019, 36(6), 940-951.
[http://dx.doi.org/10.1080/19440049.2019.1600748] [PMID: 31009320]
[24]
Belasli, A.; Herrera, M.; Ariño, A.; Djenane, D. Occurrence and exposure assessment of major mycotoxins in foodstuffs from Algeria. Toxins, 2023, 15(7), 449.
[http://dx.doi.org/10.3390/toxins15070449] [PMID: 37505718]
[25]
Foerster, C.; Ríos-Gajardo, G.; Gómez, P.; Muñoz, K.; Cortés, S.; Maldonado, C.; Ferreccio, C. Assessment of mycotoxin exposure in a rural county of Chile by urinary biomarker determination. Toxins, 2021, 13(7), 439.
[http://dx.doi.org/10.3390/toxins13070439] [PMID: 34202116]
[26]
Ali, S.; Battaglini Franco, B.; Theodoro Rezende, V.; Gabriel Dionisio Freire, L.; Lima de Paiva, E.; Clara Fogacio Haikal, M.; Leme Guerra, E.; Eliana Rosim, R.; Gustavo Tonin, F.; Savioli Ferraz, I.; Antonio Del Ciampo, L.; Augusto Fernandes de Oliveira, C. Exposure assessment of children to dietary mycotoxins: A pilot study conducted in Ribeirão Preto, São Paulo, Brazil. Food Res. Int., 2024, 180, 114087.
[http://dx.doi.org/10.1016/j.foodres.2024.114087] [PMID: 38395556]
[27]
Hathout, A.S.; Abel-Fattah, S.M.; Abou-Sree, Y.H.; Fouzy, A.S.M. Incidence and exposure assessment of aflatoxins and ochratoxin A in Egyptian wheat. Toxicol. Rep., 2020, 7, 867-873.
[http://dx.doi.org/10.1016/j.toxrep.2020.07.003] [PMID: 32760654]
[28]
Kortei, N.K.; Annan, T.; Kyei-Baffour, V.; Essuman, E.K.; Okyere, H.; Tettey, C.O. Exposure and risk characterizations of ochratoxins A and aflatoxins through maize (Zea mays) consumed in different agro-ecological zones of Ghana. Sci. Rep., 2021, 11(1), 23339.
[http://dx.doi.org/10.1038/s41598-021-02822-x] [PMID: 34857860]
[29]
Peles, F.; Sipos, P.; Kovács, S.; Győri, Z.; Pócsi, I.; Pusztahelyi, T. Biological control and mitigation of aflatoxin contamination in commodities. Toxins, 2021, 13(2), 104.
[http://dx.doi.org/10.3390/toxins13020104] [PMID: 33535580]
[30]
Ben Taheur, F.; Kouidhi, B.; Al Qurashi, Y.M.A.; Ben Salah-Abbès, J.; Chaieb, K. Review: Biotechnology of mycotoxins detoxification using microorganisms and enzymes. Toxicon, 2019, 160, 12-22.
[http://dx.doi.org/10.1016/j.toxicon.2019.02.001] [PMID: 30772433]
[31]
Møller, C.O.A.; Freire, L.; Rosim, R.E.; Margalho, L.P.; Balthazar, C.F.; Franco, L.T.; Sant’Ana, A.S.; Corassin, C.H.; Rattray, F.P.; Oliveira, C.A.F. Effect of lactic acid bacteria strains on the growth and aflatoxin production potential of Aspergillus parasiticus, and their ability to bind aflatoxin B1, ochratoxin A, and zearalenone in vitro. Front. Microbiol., 2021, 12, 655386.
[http://dx.doi.org/10.3389/fmicb.2021.655386] [PMID: 33967993]
[32]
Ogunremi, O.R.; Freimüller Leischtfeld, S.; Mischler, S.; Miescher Schwenninger, S. Antifungal activity of lactic acid bacteria isolated from kunu-zaki, a cereal-based Nigerian fermented beverage. Food Biosci., 2022, 49, 101648.
[http://dx.doi.org/10.1016/j.fbio.2022.101648]
[33]
Pérez-Ramos, A.; Madi-Moussa, D.; Coucheney, F.; Drider, D. Current knowledge of the mode of action and immunity mechanisms of lab-bacteriocins. Microorganisms, 2021, 9(10), 2107.
[http://dx.doi.org/10.3390/microorganisms9102107] [PMID: 34683428]
[34]
Juodeikiene, G.; Basinskiene, L.; Bartkiene, E.; Matusevicius, P. Mycotoxin decontamination aspects in food, feed and renewables using fermentation processes. Struc. Funct. Food. Eng., 2012, 171-204.
[35]
Liu, L.; Xie, M.; Wei, D. Biological detoxification of mycotoxins: Current status and future advances. Int. J. Mol. Sci., 2022, 23(3), 1064.
[http://dx.doi.org/10.3390/ijms23031064] [PMID: 35162993]
[36]
Abdi, M.; Asadi, A.; Maleki, F.; Kouhsari, E.; Fattahi, A.; Ohadi, E. Microbiological detoxification of mycotoxins: Focus on mechanisms and advances. Infect. Disord. Drug. Targets., 2021, 21(3), 339-357.
[http://dx.doi.org/10.2174/1871526520666200616145150]
[37]
Nasrollahzadeh, A.; Mokhtari, S.; Khomeiri, M.; Saris, P. Mycotoxin detoxification of food by lactic acid bacteria. Int. J. Food. Contam., 2022, 9(1), 1-9.
[http://dx.doi.org/10.1186/s40550-021-00087-w]
[38]
Lili, Z.; Junyan, W.; Hongfei, Z.; Baoqing, Z.; Bolin, Z. Detoxification of cancerogenic compounds by lactic acid bacteria strains. Crit. Rev. Food Sci. Nutr., 2018, 58(16), 2727-2742.
[http://dx.doi.org/10.1080/10408398.2017.1339665] [PMID: 29053003]
[39]
Kumara, S.S.; Bashisht, A.; Venkateswaran, G.; Hariprasad, P.; Gayathri, D. Characterization of novel Lactobacillus fermentum from curd samples of indigenous cows from Malnad region, Karnataka, for their aflatoxin B 1 binding and probiotic properties. Probiotics Antimicrob. Proteins, 2019, 11(4), 1100-1109.
[http://dx.doi.org/10.1007/s12602-018-9479-7] [PMID: 30368716]
[40]
Haskard, C.A.; El-Nezami, H.S.; Kankaanpää, P.E.; Salminen, S.; Ahokas, J.T. Surface binding of aflatoxin B(1) by lactic acid bacteria. Appl. Environ. Microbiol., 2001, 67(7), 3086-3091.
[http://dx.doi.org/10.1128/AEM.67.7.3086-3091.2001] [PMID: 11425726]
[41]
Adami Ghamsari, F.; Tajabadi Ebrahimi, M.; Bagheri Varzaneh, M.; Iranbakhsh, A.; Akhavan Sepahi, A. In vitro reduction of mycotoxin deoxynivalenol by organic adsorbent. J. Food Process. Preserv., 2021, 45(3), e15212.
[http://dx.doi.org/10.1111/jfpp.15212]
[42]
Zhai, Y.; Hu, S.; Zhong, L.; Lu, Z.; Bie, X.; Zhao, H.; Zhang, C.; Lu, F. Characterization of deoxynivalenol detoxification by Lactobacillus paracasei LHZ-1 isolated from yogurt. J. Food Prot., 2019, 82(8), 1292-1299.
[http://dx.doi.org/10.4315/0362-028X.JFP-18-581] [PMID: 31310167]
[43]
Luo, Y.; Liu, X.; Yuan, L.; Li, J. Complicated interactions between bio-adsorbents and mycotoxins during mycotoxin adsorption: Current research and future prospects. Trends Food Sci. Technol., 2020, 96, 127-134.
[http://dx.doi.org/10.1016/j.tifs.2019.12.012]
[44]
Wacoo, A.P.; Atukunda, P.; Muhoozi, G.; Braster, M.; Wagner, M.; van den Broek, T.J.; Sybesma, W.; Westerberg, A.C.; Iversen, P.O.; Kort, R. Aflatoxins: Occurrence, exposure, and binding to Lactobacillus species from the gut microbiota of rural Ugandan children. Microorganisms, 2020, 8(3), 347.
[http://dx.doi.org/10.3390/microorganisms8030347] [PMID: 32121365]
[45]
Lewandowski, Z.; Boltz, J.P. Biofilms in water and wastewater treatment. In: Water-Quality Engineering; Elsevier, 2011; 4, pp. 529-570.
[http://dx.doi.org/10.1016/B978-0-444-53199-5.00095-6]
[46]
Salas-Jara, M.; Ilabaca, A.; Vega, M.; García, A. Biofilm forming Lactobacillus: New challenges for the development of probiotics. Microorganisms, 2016, 4(3), 35.
[http://dx.doi.org/10.3390/microorganisms4030035] [PMID: 27681929]
[47]
Nahle, S.; Atoui, A.; Assaf, J.C.; El Khoury, A.; Louka, N.; Chokr, A. Time-dependent effect of surface material on Lactobacillus rhamnosus GG biofilm formation and gene expression. Microbiology, 2023, 92(1), 55-65.
[http://dx.doi.org/10.1134/S0026261721102142] [PMID: 36864390]
[48]
Assaf, J.C.; Khoury, A.E.; Chokr, A.; Louka, N.; Atoui, A. A novel method for elimination of aflatoxin M1 in milk using Lactobacillus rhamnosus GG biofilm. Int. J. Dairy Technol., 2019, 72(2), 248-256.
[http://dx.doi.org/10.1111/1471-0307.12578]
[49]
Nahle, S.; El Khoury, A.; Savvaidis, I.; Chokr, A.; Louka, N.; Atoui, A. Detoxification approaches of mycotoxins: By microorganisms, biofilms and enzymes. Int. J. Food. Contam., 2022, 9(1), 3.
[http://dx.doi.org/10.1186/s40550-022-00089-2]
[50]
Afshar, P.; Shokrzadeh, M.; Raeisi, S.N.; Ghorbani-HasanSaraei, A.; Nasiraii, L.R. Aflatoxins biodetoxification strategies based on probiotic bacteria. Toxicon, 2020, 178, 50-58.
[http://dx.doi.org/10.1016/j.toxicon.2020.02.007] [PMID: 32250747]
[51]
Hathout, A.S.; Aly, S.E. Biological detoxification of mycotoxins: A review. Ann. Microbiol., 2014, 64(3), 905-919.
[http://dx.doi.org/10.1007/s13213-014-0899-7]
[52]
Wafula, E.N.; Muhonja, C.N.; Kuja, J.O.; Owaga, E.E.; Makonde, H.M.; Mathara, J.M.; Kimani, V.W. Lactic acid bacteria from african fermented cereal-based products: Potential biological control agents for mycotoxins in kenya. J. Toxicol., 2022, 2022, 1-17.
[http://dx.doi.org/10.1155/2022/2397767] [PMID: 35242183]
[53]
Sipos, P.; Peles, F.; Brassó, D.L.; Béri, B.; Pusztahelyi, T.; Pócsi, I.; Győri, Z. Physical and chemical methods for reduction in aflatoxin content of feed and food. Toxins, 2021, 13(3), 204.
[http://dx.doi.org/10.3390/toxins13030204] [PMID: 33808964]
[54]
Pankaj, S.K.; Shi, H.; Keener, K.M. A review of novel physical and chemical decontamination technologies for aflatoxin in food. Trends Food Sci. Technol., 2018, 71, 73-83.
[http://dx.doi.org/10.1016/j.tifs.2017.11.007]
[55]
Jalili, M.; Jinap, S. Role of sodium hydrosulphite and pressure on the reduction of aflatoxins and ochratoxin A in black pepper. Food Control, 2012, 27(1), 11-15.
[http://dx.doi.org/10.1016/j.foodcont.2012.02.022]
[56]
Peng, Z.; Chen, L.; Zhu, Y.; Huang, Y.; Hu, X.; Wu, Q.; Nüssler, A.K.; Liu, L.; Yang, W. Current major degradation methods for aflatoxins: A review. Trends Food Sci. Technol., 2018, 80, 155-166.
[http://dx.doi.org/10.1016/j.tifs.2018.08.009]
[57]
Deshpande, S. Toxic metals, radionuclides, and food packaging contaminants; Deshpande SS editör Hand Book of Food Toxicology Marcel Dekker, Inc: New York, USA, 2002, pp. 783-810.
[58]
Ben Taheur, F.; Mansour, C.; Kouidhi, B.; Chaieb, K. Use of lactic acid bacteria for the inhibition of Aspergillus flavus and Aspergillus carbonarius growth and mycotoxin production. Toxicon, 2019, 166, 15-23.
[http://dx.doi.org/10.1016/j.toxicon.2019.05.004] [PMID: 31095961]
[59]
Mateo, E.M.; Tarazona, A.; Jiménez, M.; Mateo, F. Lactic acid bacteria as potential agents for biocontrol of aflatoxigenic and ochratoxigenic fungi. Toxins, 2022, 14(11), 807.
[http://dx.doi.org/10.3390/toxins14110807] [PMID: 36422981]
[60]
Simões, L.; Fernandes, N.; Teixeira, J.; Abrunhosa, L.; Dias, D.R. Brazilian table olives: A source of lactic acid bacteria with antimycotoxigenic and antifungal activity. Toxins, 2023, 15(1), 71.
[http://dx.doi.org/10.3390/toxins15010071] [PMID: 36668890]
[61]
Zheng, X.; Wei, W.; Rao, S.; Gao, L.; Li, H.; Yang, Z. Degradation of patulin in fruit juice by a lactic acid bacteria strain Lactobacillus casei YZU01. Food Cont., 2020, 112, 107147.
[http://dx.doi.org/10.1016/j.foodcont.2020.107147]
[62]
Cruz, P.O.; Matos, C.J.; Nascimento, Y.M.; Tavares, J.F.; Souza, E.L.; Magalhães, H.I.F. Efficacy of potentially probiotic fruit-derived Lactobacillus fermentum, L. paracasei and L. plantarum to remove aflatoxin M1 in vitro. Toxins, 2020, 13(1), 4.
[http://dx.doi.org/10.3390/toxins13010004] [PMID: 33374495]
[63]
Punia Bangar, S.; Sharma, N.; Bhardwaj, A.; Phimolsiripol, Y. Lactic acid bacteria. Qual. Assur. Saf. Crops Foods, 2022, 14(2), 13-31.
[http://dx.doi.org/10.15586/qas.v14i2.1014]
[64]
Zhao, Y.; Zhang, C.; Folly, Y.M.E.; Chang, J.; Wang, Y.; Zhou, L.; Zhang, H.; Liu, Y. Morphological and transcriptomic analysis of the inhibitory effects of Lactobacillus plantarum on Aspergillus flavus growth and aflatoxin production. Toxins, 2019, 11(11), 636.
[http://dx.doi.org/10.3390/toxins11110636] [PMID: 31683906]
[65]
mohammadi, R.; Abbaszadeh, S.; Sharifzadeh, A.; Sepandi, M.; Taghdir, M.; Youseftabar Miri, N.; Parastouei, K. in vitro activity of encapsulated lactic acid bacteria on aflatoxin production and growth of Aspergillus Spp. Food Sci. Nutr., 2021, 9(3), 1282-1288.
[http://dx.doi.org/10.1002/fsn3.2015] [PMID: 33747444]
[66]
Ouyang, W.; Liao, Z.; Yang, X.; Zhang, X.; Zhu, X.; Zhong, Q.; Wang, L.; Fang, X.; Wang, J. Microbial composition of water kefir grains and their application for the detoxification of aflatoxin B1. Toxins, 2024, 16(2), 107.
[http://dx.doi.org/10.3390/toxins16020107] [PMID: 38393185]
[67]
Nasrollahzadeh, A.; Mokhtari, S.; Khomeiri, M.; Saris, P.E.J. Antifungal preservation of food by lactic acid bacteria. Foods, 2022, 11(3), 395.
[http://dx.doi.org/10.3390/foods11030395] [PMID: 35159544]
[68]
Rahayu, E.S.; Triyadi, R.; Khusna, R.N.B.; Djaafar, T.F.; Utami, T.; Marwati, T.; Hatmi, R.U. indigenous yeast, lactic acid bacteria, and acetic acid bacteria from cocoa bean fermentation in Indonesia can inhibit fungal-growth-producing mycotoxins. Fermentation, 2021, 7(3), 192.
[http://dx.doi.org/10.3390/fermentation7030192]
[69]
Siedler, S.; Balti, R.; Neves, A.R. Bioprotective mechanisms of lactic acid bacteria against fungal spoilage of food. Curr. Opin. Biotechnol., 2019, 56, 138-146.
[http://dx.doi.org/10.1016/j.copbio.2018.11.015] [PMID: 30504082]
[70]
Muhialdin, B.J.; Algboory, H.L.; Kadum, H.; Mohammed, N.K.; Saari, N.; Hassan, Z.; Meor Hussin, A.S. Antifungal activity determination for the peptides generated by Lactobacillus plantarum TE10 against Aspergillus flavus in maize seeds. Food Cont., 2020, 109, 106898.
[http://dx.doi.org/10.1016/j.foodcont.2019.106898]
[71]
Luz, C.; D’Opazo, V.; Quiles, J.M.; Romano, R.; Mañes, J.; Meca, G. Biopreservation of tomatoes using fermented media by lactic acid bacteria. Lebensm. Wiss. Technol., 2020, 130, 109618.
[http://dx.doi.org/10.1016/j.lwt.2020.109618]
[72]
Pradhan, S.; Ananthanarayan, L.; Prasad, K.; Bhatnagar-Mathur, P. Anti-fungal activity of lactic acid bacterial isolates against aflatoxigenic fungi inoculated on peanut kernels. Lebensm. Wiss. Technol., 2021, 143, 111104.
[http://dx.doi.org/10.1016/j.lwt.2021.111104]
[73]
Illueca, F.; Moreno, A.; Calpe, J.; Nazareth, T.M.; Dopazo, V.; Meca, G.; Quiles, J.M.; Luz, C. Bread biopreservation through the addition of lactic acid bacteria in sourdough. Foods, 2023, 12(4), 864.
[http://dx.doi.org/10.3390/foods12040864] [PMID: 36832942]
[74]
Abdel-Nasser, A.; Hathout, A.S.; Badr, A.N.; Barakat, O.S.; Fathy, H.M. Extraction and characterization of bioactive secondary metabolites from lactic acid bacteria and evaluating their antifungal and antiaflatoxigenic activity. Biotechnol. Rep., 2023, 38, e00799.
[http://dx.doi.org/10.1016/j.btre.2023.e00799] [PMID: 37206916]
[75]
Purnawita, W.; Rahayu, W.P.; Lioe, H.N.; Nurjanah, S.; Maryam, R. Antifungal activity of reuterin against aflatoxigenic Aspergillus flavus. J. Microbiol. Biotechnol. Food. Sci., 2023, 13(2), e10032.
[http://dx.doi.org/10.55251/jmbfs.10032]
[76]
Nazareth, T.M.; Luz, C.; Torrijos, R.; Quiles, J.M.; Luciano, F.B.; Mañes, J.; Meca, G. Potential application of lactic acid bacteria to reduce aflatoxin B1 and fumonisin B1 occurrence on corn kernels and corn ears. Toxins, 2019, 12(1), 21.
[http://dx.doi.org/10.3390/toxins12010021] [PMID: 31906161]
[77]
Dopazo, V.; Musto, L.; Nazareth, T.M.; Lafuente, C.; Meca, G.; Luz, C. Revalorization of rice bran as a potential ingredient for reducing fungal contamination in bread by lactic acid bacterial fermentation. Food Biosci., 2024, 58, 103703.
[http://dx.doi.org/10.1016/j.fbio.2024.103703]
[78]
Dopazo, V.; Navarré, A.; Calpe, J.; Riolo, M.; Moreno, A.; Meca, G.; Luz, C. Revalorization of beer brewing waste as an antifungal ingredient for bread biopreservation. Food Biosci., 2024, 58, 103588.
[http://dx.doi.org/10.1016/j.fbio.2024.103588]
[79]
EL Houssni, I.; Khedid, K.; Zahidi, A.; Hassikou, R. The inhibitory effects of lactic acid bacteria isolated from sourdough on the mycotoxigenic fungi growth and mycotoxins from wheat bread. Biocatal. Agric. Biotechnol., 2023, 50, 102702.
[http://dx.doi.org/10.1016/j.bcab.2023.102702]
[80]
Guimarães, A.; Venancio, A.; Abrunhosa, L. Antifungal effect of organic acids from lactic acid bacteria on Penicillium nordicum. Food Addit. Contam. Part A Chem. Anal. Control Expo. Risk Assess., 2018, 35(9), 1803-1818.
[http://dx.doi.org/10.1080/19440049.2018.1500718] [PMID: 30016195]
[81]
Abdul Hakim, B.N.; Xuan, N.J.; Oslan, S.N.H. A comprehensive review of bioactive compounds from lactic acid bacteria: Potential functions as functional food in dietetics and the food industry. Foods, 2023, 12(15), 2850.
[http://dx.doi.org/10.3390/foods12152850] [PMID: 37569118]
[82]
Arena, M.P.; Silvain, A.; Normanno, G.; Grieco, F.; Drider, D.; Spano, G.; Fiocco, D. Use of Lactobacillus plantarum strains as a bio-control strategy against food-borne pathogenic microorganisms. Front. Microbiol., 2016, 7, 464.
[http://dx.doi.org/10.3389/fmicb.2016.00464] [PMID: 27148172]
[83]
Kim, J.; Kim, Y.M.; Lebaka, V.R.; Wee, Y.J. Lactic acid for green chemical industry: Recent advances in and future prospects for production technology, recovery, and applications. Fermentation, 2022, 8(11), 609.
[http://dx.doi.org/10.3390/fermentation8110609]
[84]
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., 2015, 78(9), 1689-1698.
[http://dx.doi.org/10.4315/0362-028X.JFP-15-046] [PMID: 26319723]
[85]
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 Cont., 2014, 40, 224-233.
[http://dx.doi.org/10.1016/j.foodcont.2013.12.005]
[86]
Fugaban, J.I.I.; Jung, E.S.; Todorov, S.D.; Holzapfel, W.H. Evaluation of antifungal metabolites produced by lactic acid bacteria. Probiotics Antimicrob. Proteins, 2023, 15(5), 1447-1463.
[http://dx.doi.org/10.1007/s12602-022-09995-5] [PMID: 36227534]
[87]
Vougiouklaki, D.; Tsironi, T.; Papaparaskevas, J.; Halvatsiotis, P.; Houhoula, D. Characterization of Lacticaseibacillus rhamnosus, Levilactobacillus brevis and Lactiplantibacillus plantarum metabolites and evaluation of their antimicrobial activity against food pathogens. Appl. Sci., 2022, 12(2), 660.
[http://dx.doi.org/10.3390/app12020660]
[88]
Parappilly, S.J.; Idicula, D.V.; Chandran, A.; Mathil Radhakrishnan, K.; George, S.M. Antifungal activity of human gut lactic acid bacteria against aflatoxigenic Aspergillus flavus MTCC 2798 and their potential application as food biopreservative. J. Food Saf., 2021, 41(6), e12942.
[http://dx.doi.org/10.1111/jfs.12942]
[89]
Bukhari, S.A.; Salman, M.; Numan, M.; Javed, M.R.; Zubair, M.; Mustafa, G. Characterization of antifungal metabolites produced by Lactobacillus plantarum and Lactobacillus coryniformis isolated from rice rinsed water. Mol. Biol. Rep., 2020, 47(3), 1871-1881.
[http://dx.doi.org/10.1007/s11033-020-05281-1] [PMID: 32006197]
[90]
Jung, S.; Hwang, H.; Lee, J.H. Effect of lactic acid bacteria on phenyllactic acid production in kimchi. Food Cont., 2019, 106, 106701.
[http://dx.doi.org/10.1016/j.foodcont.2019.06.027]
[91]
Wangprasertkul, J.; Siriwattanapong, R.; Harnkarnsujarit, N. Antifungal packaging of sorbate and benzoate incorporated biodegradable films for fresh noodles. Food Contr., 2021, 123, 107763.
[http://dx.doi.org/10.1016/j.foodcont.2020.107763]
[92]
Guimarães, A.; Santiago, A.; Teixeira, J.A.; Venâncio, A.; Abrunhosa, L. Anti-aflatoxigenic effect of organic acids produced by Lactobacillus plantarum. Int. J. Food Microbiol., 2018, 264, 31-38.
[http://dx.doi.org/10.1016/j.ijfoodmicro.2017.10.025] [PMID: 29107194]
[93]
Yépez, A.; Luz, C.; Meca, G.; Vignolo, G.; Mañes, J.; Aznar, R. Biopreservation potential of lactic acid bacteria from Andean fermented food of vegetal origin. Food Control, 2017, 78, 393-400.
[http://dx.doi.org/10.1016/j.foodcont.2017.03.009]
[94]
Engels, C.; Schwab, C.; Zhang, J.; Stevens, M.J.A.; Bieri, C.; Ebert, M.O.; McNeill, K.; Sturla, S.J.; Lacroix, C. Acrolein contributes strongly to antimicrobial and heterocyclic amine transformation activities of reuterin. Sci. Rep., 2016, 6(1), 36246.
[http://dx.doi.org/10.1038/srep36246] [PMID: 27819285]
[95]
Schaefer, L.; Auchtung, T.A.; Hermans, K.E.; Whitehead, D.; Borhan, B.; Britton, R.A. The antimicrobial compound reuterin (3-hydroxypropionaldehyde) induces oxidative stress via interaction with thiol groups. Microbiology, 2010, 156(6), 1589-1599.
[http://dx.doi.org/10.1099/mic.0.035642-0] [PMID: 20150236]
[96]
Vimont, A.; Fernandez, B.; Ahmed, G.; Fortin, H.P.; Fliss, I. Quantitative antifungal activity of reuterin against food isolates of yeasts and moulds and its potential application in yogurt. Int. J. Food. Microbiol., 2019, 289, 182-188.
[http://dx.doi.org/10.1016/j.ijfoodmicro.2018.09.005] [PMID: 30253311]
[97]
Gerez, C.L.; Torres, M.J.; Font de Valdez, G.; Rollán, G. Control of spoilage fungi by lactic acid bacteria. Biol. Cont., 2013, 64(3), 231-237.
[http://dx.doi.org/10.1016/j.biocontrol.2012.10.009]
[98]
Salman, M.; Tariq, A.; Ijaz, A.; Naheed, S.; Hashem, A.; Abd Allah, E.F.; Soliman, M.H.; Javed, M.R. in vitro antimicrobial and antioxidant activities of Lactobacillus coryniformis BCH-4 bioactive compounds and determination of their bioprotective effects on nutritional components of Maize (Zea mays L.). Molecules, 2020, 25(20), 4685.
[http://dx.doi.org/10.3390/molecules25204685] [PMID: 33066377]
[99]
Muhialdin, B.J.; Hassan, Z.; Saari, N. in vitro antifungal activity of lactic acid bacteria low molecular peptides against spoilage fungi of bakery products. Ann. Microbiol., 2018, 68(9), 557-567.
[http://dx.doi.org/10.1007/s13213-018-1363-x]
[100]
Guillén, G; López Caballero, M; Alemán, A Lacey, A.L.; Giménez, B.; Montero Gracia, P. Antioxidant and antimicrobial peptide fractions from squid and tuna skin gelatin. Chem. Environ. Sci., 2010.
[101]
Joo, S.H. Cyclic peptides as therapeutic agents and biochemical tools. Biomol. Ther., 2012, 20(1), 19-26.
[http://dx.doi.org/10.4062/biomolther.2012.20.1.019] [PMID: 24116270]
[102]
Bartkiene, E.; Lele, V.; Ruzauskas, M.; Domig, K.J.; Starkute, V.; Zavistanaviciute, P.; Bartkevics, V.; Pugajeva, I.; Klupsaite, D.; Juodeikiene, G.; Mickiene, R.; Rocha, J.M. Lactic acid bacteria isolation from spontaneous sourdough and their characterization including antimicrobial and antifungal properties evaluation. Microorganisms, 2019, 8(1), 64.
[http://dx.doi.org/10.3390/microorganisms8010064] [PMID: 31905993]
[103]
Ciulla, M.G.; Gelain, F. Structure activity relationships of antibacterial peptides. Microb. Biotechnol., 2023, 16(4), 757-777.
[http://dx.doi.org/10.1111/1751-7915.14213] [PMID: 36705032]
[104]
Kovacevik, B.; Veličkovska, S.K.; Esatbeyoglu, T.; Cvetkovski, A.; Qamar, M.; Rocha, J.M. Biopreservation in flours and bread. In: Novel Approaches in Biopreservation for Food and Clinical Purposes; CRC Press, 2024; pp. 130-204.
[105]
Ouiddir, M.; Bettache, G.; Leyva Salas, M.; Pawtowski, A.; Donot, C.; Brahimi, S.; Mabrouk, K.; Coton, E.; Mounier, J. Selection of Algerian lactic acid bacteria for use as antifungal bioprotective cultures and application in dairy and bakery products. Food Microbiol., 2019, 82, 160-170.
[http://dx.doi.org/10.1016/j.fm.2019.01.020] [PMID: 31027770]
[106]
Zhao, Z.; Simpson, D.J.; Gänzle, M.G. Bioprotective lactobacilli in Crescenza and Gouda cheese models to inhibit fungal spoilage. Int. Dairy J., 2024, 152, 105883.
[http://dx.doi.org/10.1016/j.idairyj.2024.105883]
[107]
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.
[http://dx.doi.org/10.1128/AEM.69.12.7554-7557.2003] [PMID: 14660414]
[108]
Zhao, X.; Zhou, J.; Tian, R.; Liu, Y. Microbial volatile organic compounds: Antifungal mechanisms, applications, and challenges. Front. Microbiol., 2022, 13, 922450.
[http://dx.doi.org/10.3389/fmicb.2022.922450] [PMID: 35910607]
[109]
Suzuki, K.; Shono, F.; Kai, H.; Uno, T.; Uyeda, M. Inhibition of topoisomerases by fatty acids. J. Enzyme Inhib., 2000, 15(4), 357-366.
[http://dx.doi.org/10.1080/14756360009040693] [PMID: 10995067]
[110]
Guimarães, A.; Venâncio, A. The potential of fatty acids and their derivatives as antifungal agents: A review. Toxins, 2022, 14(3), 188.
[http://dx.doi.org/10.3390/toxins14030188] [PMID: 35324685]
[111]
Soltani, S.; Hammami, R.; Cotter, P.D.; Rebuffat, S.; Said, L.B.; Gaudreau, H.; Bédard, F.; Biron, E.; Drider, D.; Fliss, I. Bacteriocins as a new generation of antimicrobials: Toxicity aspects and regulations. FEMS Microbiol. Rev., 2021, 45(1), fuaa039.
[http://dx.doi.org/10.1093/femsre/fuaa039] [PMID: 32876664]
[112]
Darbandi, A.; Asadi, A.; Mahdizade Ari, M.; Ohadi, E.; Talebi, M.; Halaj Zadeh, M.; Darb Emamie, A.; Ghanavati, R.; Kakanj, M. Bacteriocins: Properties and potential use as antimicrobials. J. Clin. Lab. Anal., 2022, 36(1), e24093.
[http://dx.doi.org/10.1002/jcla.24093] [PMID: 34851542]
[113]
Šušković, J.; Kos, B.; Beganović, J.; Leboš Pavunc, A.; Habjanič, K.; Matošić, S. Antimicrobial activity–the most important property of probiotic and starter lactic acid bacteria. Food Technol. Biotechnol., 2010, 48(3), 296-307.
[114]
Roshanak, S.; Shahidi, F.; Yazdi, F.T.; Javadmanesh, A.; Movaffagh, J. Evaluation of antimicrobial activity of Buforin I and Nisin and the synergistic effect of their combination as a novel antimicrobial preservative. J. Food Prot., 2020, 83(11), 2018-2025.
[http://dx.doi.org/10.4315/JFP-20-127] [PMID: 32502264]
[115]
And, H.C.; Hoover, D.G. Bacteriocins and their food applications. Compr. Rev. Food Sci. Food Saf., 2003, 2(3), 82-100.
[http://dx.doi.org/10.1111/j.1541-4337.2003.tb00016.x] [PMID: 33451234]
[116]
Hernández-González, J.C.; Martínez-Tapia, A.; Lazcano-Hernández, G.; García-Pérez, B.E.; Castrejón-Jiménez, N.S. Bacteriocins from lactic acid bacteria. A powerful alternative as antimicrobials, probiotics, and immunomodulators in veterinary medicine. Animals, 2021, 11(4), 979.
[http://dx.doi.org/10.3390/ani11040979] [PMID: 33915717]
[117]
Cotter, P.D.; Hill, C.; Ross, R.P. Bacteriocins: Developing innate immunity for food. Nat. Rev. Microbiol., 2005, 3(10), 777-788.
[http://dx.doi.org/10.1038/nrmicro1273] [PMID: 16205711]
[118]
Liu, G.; Nie, R.; Liu, Y.; Mehmood, A. Combined antimicrobial effect of bacteriocins with other hurdles of physicochemic and microbiome to prolong shelf life of food: A review. Sci. Total Environ., 2022, 825, 154058.
[http://dx.doi.org/10.1016/j.scitotenv.2022.154058] [PMID: 35217045]
[119]
van Staden, A.D.P.; van Zyl, W.F.; Trindade, M.; Dicks, L.M.T.; Smith, C. Therapeutic application of lantibiotics and other lanthipeptides: Old and new findings. Appl. Environ. Microbiol., 2021, 87(14), e00186-e21.
[http://dx.doi.org/10.1128/AEM.00186-21] [PMID: 33962984]
[120]
Chen, L.; Song, Z.; Tan, S.Y.; Zhang, H.; Yuk, H.G. Application of bacteriocins produced from lactic acid bacteria for microbiological food safety. Curr/Top. Lact. Acid. Bact. Probiot., 2020, 6(1), 1-8.
[http://dx.doi.org/10.35732/ctlabp.2020.6.1.1]
[121]
Kumariya, R.; Garsa, A.K.; Rajput, Y.S.; Sood, S.K.; Akhtar, N.; Patel, S. Bacteriocins: Classification, synthesis, mechanism of action and resistance development in food spoilage causing bacteria. Microb. Pathog., 2019, 128, 171-177.
[http://dx.doi.org/10.1016/j.micpath.2019.01.002] [PMID: 30610901]
[122]
Zapaśnik, A.; Sokołowska, B.; Bryła, M. Role of lactic acid bacteria in food preservation and safety. Foods, 2022, 11(9), 1283.
[http://dx.doi.org/10.3390/foods11091283] [PMID: 35564005]
[123]
Souza, L.V.; Rodrigues da Silva, R.; Falqueto, A.; Fusieger, A.; Martins, E.; Caggia, C.; Randazzo, C.L.; Carvalho, A.F. Evaluation of antifungal activity of lactic acid bacteria against fungi in simulated cheese matrix. Lebensm. Wiss. Technol., 2023, 182, 114773.
[http://dx.doi.org/10.1016/j.lwt.2023.114773]
[124]
Venegas-Ortega, M.G.; Flores-Gallegos, A.C.; Martínez-Hernández, J.L.; Aguilar, C.N.; Nevárez-Moorillón, G.V. Production of bioactive peptides from lactic acid bacteria: A sustainable approach for healthier foods. Compr. Rev. Food Sci. Food Saf., 2019, 18(4), 1039-1051.
[http://dx.doi.org/10.1111/1541-4337.12455] [PMID: 33336997]
[125]
Azeem, N.; Nawaz, M.; Anjum, A.A.; Saeed, S.; Sana, S.; Mustafa, A.; Yousuf, M.R. Activity and anti-aflatoxigenic effect of indigenously characterized probiotic lactobacilli against Aspergillus flavus—A common poultry feed contaminant. Animals, 2019, 9(4), 166.
[http://dx.doi.org/10.3390/ani9040166] [PMID: 30991667]
[126]
Zhao, S.; Hao, X.; Yang, F.; Wang, Y.; Fan, X.; Wang, Y. Antifungal activity of Lactobacillus plantarum ZZUA493 and its application to extend the shelf life of Chinese steamed buns. Foods, 2022, 11(2), 195.
[http://dx.doi.org/10.3390/foods11020195] [PMID: 35053928]
[127]
Dallagnol, A.M.; Bustos, A.Y.; Martos, G.I.; Valdez, G.F.; Gerez, C.L. Antifungal and antimycotoxigenic effect of Lactobacillus plantarum CRL 778 at different water activity values. Rev. Argent. Microbiol., 2019, 51(2), 164-169.
[http://dx.doi.org/10.1016/j.ram.2018.04.004] [PMID: 30144992]
[128]
Raman, J.; Kim, J.S.; Choi, K.R.; Eun, H.; Yang, D.; Ko, Y.J.; Kim, S.J. Application of lactic acid bacteria (LAB) in sustainable agriculture: Advantages and limitations. Int. J. Mol. Sci., 2022, 23(14), 7784.
[http://dx.doi.org/10.3390/ijms23147784] [PMID: 35887142]
[129]
Souza, L.V.; Martins, E.; Moreira, I.M.F.B.; de Carvalho, A.F. Strategies for the development of bioprotective cultures in food preservation. Int. J. Microbiol., 2022, 2022, 6264170.
[http://dx.doi.org/10.1155/2022/6264170]