Assessment of Enterococcus durans F21 Isolated from Lben, a Moroccan Fermented Milk as a Biopreservative Agent
Applied Food Biotechnology,
Vol. 10 No. 3 (2023),
17 May 2023
,
Page 191-204
https://doi.org/10.22037/afb.v10i3.41423
Abstract
Abstract
Background and Objective: Lactic acid bacteria used in food processing for a long time are known for their benefits to consumers and their ability to produce natural antimicrobial compounds used as bio-preservatives in foods. The aim of the present study was the characterization and assessment of F21 strain, isolated from Lben (a traditional Moroccan fermented milk), as food biopreservative.
Material and Methods: Isolate F21 was isolated from Lben, subjected to screening of inhibitory activity production, and identified based on morphological, biochemical and molecular identification. Then, the production and physicochemical characterization of the antagonistic substance were determined. Also, the safety profiling and biotechnological properties of isolate were evaluated. Finally, a biopreservative powder with antimicrobial activity was produced and assessed in various food systems (milk, ground beef and fresh cheese).
Results and Conclusion: Of the isolated lactic acid bacteria, Enterococcus durans F21, isolated from Lben (a traditional Moroccan fermented milk), was remarkably endowed with interesting enterocin-like substance (heat stable and pH resistant) active against potentially pathogens and food spoilages (Listeria monocytogenes, Listeria innocua, Enterococcus faecalis, Brochothrix thermosphacta, and Mycobacterium smegmatis). Concerning the safety properties, Enterococcus durans F21 was not hemolytic, sensible to antibiotics tested, unable to produce biogenic amines and other virulence enzymes (gelatinase, DNase and urease). In addition, Enterococcus durans F21 showed satisfactory biotechnological characteristics such as acidification power, exopoly-saccharides production and antioxidant activity. The biopreservative powder containing enterocin-like substance F21 that was achieved via freeze-drying showed a minimum inhibition concentration of 60 AU ml-1 against Listeria monocytogenes in culture media. In addition, this biopreservative powder (at 665 AU ml-1) was able to improve safety and shelf-life of numerous foods (milk, Jben and ground beef). Thus, these results provided foundations for further uses of Enterococcus durans F21 as producer of potential food biopreservative agent.
Conflict of interest: The authors declare no conflict of interest.
- ▪ Enterocin-like substance ▪ Freeze-drying ▪ Ground beef ▪ Jben ▪ Lactic acid bacteria ▪ Listeria monocytogenes
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References
WHO. World Health Organization. 2015. Foodborne disease burden epidemiology 2007-2015. Available from:https://apps.who.int/iris/bitstream/handle/10665/199350/9789241565165_eng.pdf?sequence=1.Last access 11 May 2023.
CAPM. Centre Anti-Poison et de Pharmacovigilance du Maroc. 2019. Toxicologie Maroc-N°43-4ème trimestre 2019. Available from (Last Access 14 March 2023): https://www.capm-sante.ma/uploads/documents/81.pdf.
Ananou S, Maqueda M, Martinez-Bueno M, Valdivia E. Biopreservation, an ecological approach to improve the safety and shelf-life of foods. In: Communicating current research and educational topics and trends in applied microbiology. Editor: Mendez-Vilas A. Formatex, Badajoz. 2007. Pp 475-486.
Akbar A, Ali I, Anal AK. Industrial perspectives of lactic acid bacteria for biopreservation and food safety. J Anim Plant Sci. 2016; 26(4): 938-948.
Terzic-Vidojevi A, Veljovic K, Popovic N, Tolinacki M, Golic N. Enterococci from raw-milk cheeses: Current knowledge on safety, technological and probiotic concerns. Foods. 2021; 2753(10): 1-17. https://doi.org/10.3390/foods10112753
Calasso M, Ercolini D, Mancini L, Stellato G, Minervini F, Di Cagno R, De Angelis M, Gobbelti M. Relationships among house, rind and core microbiotas during manufacture of traditional Italian cheeses at the same dairy plant. Food Microbiol. 2016; 54: 115-126. https://doi.org/10.1016/j.fm.2015.10.008
Kim HJ, Koo M. Occurrence, antimicrobial resistance and molecular diversity of Enterococcus faecium in processed pork meat products in korea. Foods. 2020; 9(9): 1-14. https://doi.org/10.14. 3390/foods9091283
Hamid NH, Daud HM, Kayansamruaj P, Hassim HA, Mohd Yusoff MS, Abu Bakar SN, Srisapoom P. Short- and long-term probiotic effects of Enterococcus hirae isolated from fermented vegetable wastes on the growth, immune responses and disease resistance of hybrid catfish (Clarias gariepinus, Clarias macro-cephalus). Fish Shellfish Immunol. 2021; 114: 1-19.https://doi.org/10.1016/j.fsi.2021.04.012
Foulquie Moreno MR, Sarantinopoulos P, Tsakalidou E, De Vuyst L. The role and application of enterococci in food and health. Int J Food Microbiol. 2006; 106(1): 1-24. https://doi.org/10.1016/j.ijfoodmicro.2005.06.026
Franz CMAP, Huch M, Abriouel H, Holzapfel W, Galvez A. Enterococci as probiotics and their implications in food safety. Int J Food Microbiol. 2011; 151(2): 125-140. https://doi.org/10.1016/j.ijfoodmicro.2011.08.014
Lavilla Lerma L, Benomar N, Sanchez Valenzuela A, Casado Munoz M del C, Galvez A, Abriouel H. Role of efrAB efflux pump in biocide tolerance and antibiotic resistance of Enterococcus faecalis and Enterococcus faecium isolated from traditional fermented foods and the effect of EDTA as EfrAB inhibitor. Food Microbiol. 2014; 44: 249-257. https://doi.org/10.1016/j.fm.2014.06.009
Liu J, Shi L, Tuo X, Ma X, Hou X, Jiang S, Lv S, Cheng Y, Guo D, Han B. Preparation, characteristic and anti-inflammatory effect of selenium nanoparticle-enriched probiotic strain Enterococcus durans A8-1. J Trace Elem Med Biol. 2022; 74: 127056. https://doi.org/10.1016/j.jtemb.2022.127056
Bhardwaj A, Malik RK, Chauhan P. Functional and safety aspects of enterococci in dairy foods. Indian J Microbiol. 2008; 48(3): 317-325. https://doi.org/10.1007/s12088-008-0041-2
Carasi P, Racedo SM, Jacquot C, Elie AM, Serradell M de los angeles, Urdaci MC. Enterococcus durans EP1 a promising anti-inflammatory probiotic able to stimulate sIgA and to increase Faecalibacterium prausnitzii abundance. Front Immunol. 2017; 8: 1-14. https://doi.org/10.3389/fimmu.2017.00088
Kanda T, Nishida A, Ohno M, Imaeda H, Shimada T, Inatomi O, Bamba S, Sugimoto M andoh A. Enterococcus durans TN-3 induces regulatory T cells and suppresses the development of dextran sulfate sodium (DSS)-induced experimental colitis. Plos One. 2016; 11(7): e0159705. https://doi.org/10.1371/journal.pone.0159705
Cavicchioli VQ, Carvalho OV de, Paiva JC de, Todorov SD, Silva Junior A, Nero LA. Inhibition of Herpes Simplex Virus 1 (HSV-1) and Poliovirus (PV-1) by bacteriocins from Lactococcus lactis subsp. lactis and Enterococcus durans strains isolated from goat milk. Int J Antimicrob Agents. 2018; 51(1): 33-37. https://doi.org/10.1016/j.ijantimicag.2017.04.020
Wang X, Yang Y, Huycke MM. Risks associated with enterococci as probiotics. Food Res Int. 2020; 129: 108788.https://doi.org/10.1016/j.foodres.2019.108788
Benkirane G, Ananou S, Dumas E, Ghnimi S, Gharsallaoui A. Moroccan traditional fermented dairy products: Current processing practices and physicochemical and microbiological properties-A review. J Microbiol Biotechnol Food Sci. 2022; 12(1): e5636. https://doi.org/10.55251/jmbfs.5636
Ananou S, Lotfi S, Azdad O, Nzoyikorera N. Production, recovery and characterization of an enterocin with anti-listerial activity produced by Enterococcus hirae OS1. Appl Food Biotechnol. 2020; 7(2): 103-114. https://doi.org/10.22037/afb.v7i2.27582
Ananou S, Munoz A, Galvez A, Martinez-Bueno M, Maqueda M, Valdivia E. Optimization of enterocin AS-48 production on a whey-based substrate. Int Dairy J. 2008; 18(9): 923-927. https://doi.org/10.1016/j.idairyj.2008.02.001
Carr FJ, Chill D, Maida N. The lactic acid bacteria: A literature survey. Crit Rev Microbiol. 2002; 28(4): 281-370.
https://doi.org/10.1080/1040-840291046759
Achemchem F, Martinez-Bueno M, Abrini J, Valdivia E, Maqueda M. Enterococcus faecium F58, a bacteriocinogenic strain naturally occurring in Jben, a soft, farmhouse goat’s cheese made in Morocco. J Appl Microbiol. 2005; 99(1): 141-150.https://doi.org/10.1111/j.1365-2672.2005.02586.x
An J, Zhu W, Liu Y, Zhang X, Sun L, Hong P, Wang Y, Xu C, Xu D, Liu H. Purification and characterization of a novel bacteriocin CAMT2 produced by Bacillus amyloliquefaciens isolated from marine fish Epinephelus areolatus. Food Control. 2015; 51: 278-282.http://doi.org/10.1016/j.foodcont.2014.11.038
Varada VV, Panneerselvam D, Pushpadass HA, Mallapa RH, Ram C, Kumar S. In vitro safety assessment of electrohydrodynamically encapsulated Lactiplantibacillus plant-arum CRD7 and Lacticaseibacillus rhamnosus CRD11 for probiotics use. Curr Res Food Sci. 2023; 6: 100507.https://doi.org/10.1016/j.crfs.2023.100507
Ananou S, Zentar H, Martinez-Bueno M, Galvez A, Maqueda M, Valdivia E. The impact of enterocin AS-48 on the shelf-life and safety of sardines (Sardina pilchardus) under different storage conditions. Food Microbiol. 2014; 44: 185-195.https://doi.org/10.1016/j.fm.2014.06.008
EUCAST. Europeen Committee on Antimicrobial Susceptibility Testing. 2021. Available from: www.sfm-microbiologie.org. Last access 28 April 2023.
Zhang Y, Hu P, Lou L, Zhan J, Fan M, Li D, Liao Q. Antioxidant activities of lactic acid bacteria for quality improvement of fermented sausage. J Food Sci. 2017; 82(12): 2960-2967.https://doi.org/10.1111/1750-3841.13975
Taj R, Masud T, Sohail A, Sammi S, Naz R, Sharma-Khanal BK, Nawaz MA. In vitro screening of EPS-producing Streptococcus thermophilus strains for their probiotic potential from Dahi. Food Sci Nutr. 2022; 10(7): 2347-2359. https://doi.org/10.1002/fsn3.2843
Achemchem F, Abrini J, Martinez-Bueno M, Valdivia E, Maqueda M. Control of Listeria monocytogenes in goat’s milk and goat’s jben by the bacteriocinogenic Enterococcus faecium F58 strain. J Food Prot. 2006; 69(10): 2370-2376.https://doi.org/10.4315/0362-028X-69.10.2370
Wu Y, Pang X, Wu Y, Liu X, Zhang X. Enterocins: Classification, synthesis, antibacterial mechanisms and food applications. Molecules. 2022; 27(7): 2258. https://doi.org/10.3390/molecules27072258
Zhou Y, Shi L, Wang J, Yuan J, Liu J, Liu L, Da R, Cheng Y, Han B. Probiotic potential analysis and safety evaluation of Enterococcus durans A8-1 isolated from a healthy chinese infant. Front Microbiol. 2021; 12(12): 1-13. https://doi.org/10.3389/fmicb.2021.799173
Yerlikaya O, Akbulut N. In vitro characterisation of probiotic properties of Enterococcus faecium and Enterococcus durans strains isolated from raw milk and traditional dairy products. Int J Dairy Technol. 2020; 73(1): 98-107. https://doi.org/10.1111/1471-0307.12645
Ennahar S, Asou Y, Zendo T, Sonomoto K, Ishizaki A. Biochemical and genetic evidence for production of enterocins A and B by Enterococcus faecium WHE 81. Int J Food Microbiol. 2001; 70(3): 291-301. https://doi.org/10.1016/S0168-1605(01)00565-7
Gutierrez J, Criado R, Martin M, Herranz C, Cintas LM, Hernandez PE. Production of enterocin P, an antilisterial pediocin-like bacteriocin from Enterococcus faecium P13, in Pichia pastons. Antimicrob Agents Chemother. 2005; 49(7): 3004-3008.https://doi.org/10.1128/AAC.49.7.3004-3008.2005
Ayi B. Enterococcal Infections. In: xPharm: The Comprehensive Pharmacology Reference. Editors: SJ Enna, David B. Bylund Elsevier, 2007. Pp 1-6. https://doi.org/10.1016/B978-008055232-3.60856-6
Li B, Zhan M, Evivie SE, Jin D, Zhao L, Chowdhury S, Chowh S, Sarker S, Huo G, Liu F. Evaluating the safety of potential probiotic Enterococcus durans KLDS6.0930 using whole genome sequencing and oral toxicity study. Front Microbiol. 2018; 9(1943): 1-15.https://doi.org/10.3389/fmicb.2018.01943
Yangzom T, Kumar Singh TS. Study of vancomycin and high-level aminoglycoside-resistant Enterococcus species and evaluation of a rapid spot test for enterococci from Central Referral Hospital, Sikkim, India. J Lab Physicians. 2019; 11(03): 192-199.https://doi.org/10.4103/jlp.jlp_5_19
Visintin S, Alessandria V, Valente A, Dolci P, Cocolin L. Molecular identification and physiological characterization of yeasts, lactic acid bacteria and acetic acid bacteria isolated from heap and box cocoa bean fermentations in West Africa. Int J Food Microbiol. 2016; 216: 69-78. https://doi.org/10.1016/j.ijfoodmicro.2015.09.004
Smit G, Smit BA, Engels WJM. Flavour formation by lactic acid bacteria and biochemical flavour profiling of cheese products. FEMS Microbiol Rev. 2005; 29(3): 591-610. https://doi.org/10.1016/j.femsre.2005.04.002
Graham K, Rea R, Simpson P, Stack H. Enterococcus faecalis milk fermentates display antioxidant properties and inhibitory activity towards key enzymes linked to hypertension and hyperglycaemia. J Funct Foods. 2019; 58: 292-300.https://doi.org/10.1016/j.jff.2019.04.052
Pieniz S andreazza R, Okeke BC, Camargo FAO, Brandelli A. Antimicrobial and antioxidant activities of Enterococcus species isolated from meat and dairy products. Braz J Biol. 2016; 75(4): 923-931. https://doi.org/10.1590/1519-6984.02814
Pieniz S, de Moura TM, Cassenego APV andreazza R, Frazzon APG, Camargo FA de O, Brandelli A. Evaluation of resistance genes and virulence factors in a food isolated Enterococcus durans with potential probiotic effect. Food Control. 2015; 51: 49-54.https://doi.org/10.1016/j.foodcont.2014.11.012
Ji K, Jang NY, Kim YT. Isolation of lactic acid bacteria showing antioxidative and probiotic activities from kimchi and infant feces. J Microbiol Biotechnol. 2015; 25(9): 1568-1577. https://doi.org/10.4014/jmb.1501.01077
Boubakeur B, Khadem H, Drabo MS, Ali A, Meddah AT. Probiotic properties and exopolysaccharides production of Stretptococcus thermophilus CNRZ 447 and Enterococcus durans NCBI 53345. Ukr Food J. 2021; 10(4): 853-872. https://doi.org/10.24263/2304-974X-2021-10-4-17
Mostafa H, El-Mezawy A, Geis, Heller K. Exopolysaccharide production by Enterococcus faecium. Milchwissenschaft. 2009; 64(4): 361-365.
Nguyen PT, Nguyen TT, Bui DC, Hong PT, Hoang QK, Nguyen HT. Exopolysaccharide production by lactic acid bacteria: The manipulation of environmental stresses for industrial applications. AIMS Microbiol. 2020; 6(4): 451-469.https://doi.org/10.3934/MICROBIOL.2020027
Dimitrieva-Moals GY, Unlu G. Development of freeze-dried bacteriocin-containing preparations from lactic acid bacteria to inhibit Listeria monocytogenes and Staphylococcus aureus. 2012; 4: 27-38. https://doi.org/10.1007/s12602-011-9088-1
Unlu G, Nielsen B, Ionita C. Inhibition of Listeria monocytogenes in hot dogs by surface application of freeze-dried bacteriocin-containing powders from lactic acid bacteria. Probiotics Antimicrob Proteins. 2016; 8(2): 102-110. https://doi.org/10.1007/s12602-016-9213-2
Yildirim Z, Oncul N, Yildirim M, Karabiyikli. Application of lactococcin BZ and enterocin KP against Listeria monocytogenes in milk as biopreservation agents. Acta Aliment. 2016; 45(4): 486-492.https://doi.org/10.1556/066.2016.45.4.4
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