Abstract
To prevent foodborne diseases and extend shelf life, antimicrobial agents may be used in food to inhibit the growth of undesired microorganisms. The present study was aimed to determine the antimicrobial and antifungal activities of the fermented medicinal plants extract using Lactobacillus acidophilus ATCC 4356. The fermentation kinetic parameters, biochemical composition and the volatile compounds of the fermented plant extract were assessed. The results showed that, the fermented plants extract exhibited high content in polyphenols, flavonoids, and tannins (152.7 mg AGE/L; 93.6 mg RE/L; and 62.1 mg CE/L, respectively) comparing to non-fermented the extract. The GC–MS headspace analyses showed the presence of 24 interesting volatile compounds. The richness of the fermented plants extracts in polyphenols and bioactive compound, such as Eucalyptol, Camphene, α-Phellandrene, α-Terpinene, improves their biological activity. In addition, the fermented plants extract exhibited a high antimicrobial potential against pathogenic bacteria and fungi determined by different methods. The maximum inhibition showed in the fermented plants extract against Escherichia coli 25922/3, Pseudomonas aeruginosa 27853 ATCC, Staphylococcus aureus 29213 ATCC, Enterococcus aerogenes 13048 ATCC, Phytophthora infestans P3 4/91 R + , P. infestans P4 20/01 R, P. infestans (GL-1). The obtained results support the hypothesis of using lactic fermentation as a functional ingredient to improve food preservation. The bioprocesses of fermentation technology enhance antimicrobial and antifungal activities which could be used in different industrial applications.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Anderson DM, Cembella AD, Hallegraeff GM (2012) Progress in understanding harmful algal blooms: paradigm shifts and new technologies for research, monitoring, and management. Ann Rev Mar Sci 4:143–176. https://doi.org/10.1146/annurev-marine-120308-081121
Barba FJ, Parniakov O, Pereira SA, Wiktor A, Grimi N, Boussetta N, Saraiva JA, Raso J, Martin-Belloso O, Witrowa-Rajchert D, Lebovka N (2015) Current applications and new opportunities for the use of pulsed electric fields in food science and industry. Int Food Res 77:773–798. https://doi.org/10.1016/j.foodres.2015.09.015
Begunova AV, Savinova OS, Rozhkova IV, Krysanova YI, Fedorova TV (2020) In vitro assessment of probiotic potential and functional properties of lactobacillus reuteri LR1. Appl Biochem Microbiol 56:544–552. https://doi.org/10.1134/S000368382005004X
Blanc PJ (1996) Characterization of the tea fungus metabolites. Biotech Lett 18(2):139–142. https://doi.org/10.1007/BF00128667
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72(1–2):248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Celiktas OY, Kocabas EH, Bedir E, Sukan FV, Ozek T, Baser KH (2007) Antimicrobial activities of methanol extracts and essential oils of Rosmarinus officinalis, depending on location and seasonal variations. Food Chem 100(2):553–559. https://doi.org/10.1016/j.foodchem.2005.10.011
Cetojevic-Simin DD, Bogdanovic GM, Cvetkovic DD, Velicanski AS (2008) Antiproliferative and antimicrobial activity of traditional Kombucha and Satureja montana L. Kombucha J BUON 13(3):395–401
Ciliao Filho M, Bertéli MBD, Valle JS, Paccola-Meirelles LD, Linde GA, Barcellos FG, Colauto NB (2017) Genetic diversity and pectinolytic activity of epiphytic yeasts from grape carposphere. Genet Mol Res. https://doi.org/10.4238/gmr16029698
Di Cagno R, Minervini G, Rizzello CG, De Angelis M, Gobbetti M (2011) Effect of lactic acid fermentation on antioxidant, texture, color and sensory properties of red and green smoothies. Food Microbiol 28(5):1062–1071. https://doi.org/10.1016/j.fm.2011.02.011
Di Cagno R, Filannino P, Gobbetti M (2017) Lactic acid fermentation drives the optimal volatile flavor-aroma profile of pomegranate juice. Int J Food Microbiol 248:56–62. https://doi.org/10.1016/j.ijfoodmicro.2017.02.014
Fisher MC, Henk DA, Briggs CJ, Brownstein JS, Madoff LC, McCraw SL, Gurr SJ (2012) Emerging fungal threats to animal, plant and ecosystem health. Nature 484(7393):186–194. https://doi.org/10.1038/nature10947
Freire AL, Ramos CL, da Costa Souza PN, Cardoso MG, Schwan RF (2017) Nondairy beverage produced by controlled fermentation with potential probiotic starter cultures of lactic acid bacteria and yeast. Int J Food Microbiol. https://doi.org/10.1016/j.ijfoodmicro.2017.02.011
Fry W (2008) Phytophthora infestans: the plant (and R gene) destroyer. Mol Plant Pathol 9(3):385–402. https://doi.org/10.1111/j.1364-3703.2007.00465.x
Gadhoumi H, Gullo M, De Vero L, Martinez-Rojas E, Saidani Tounsi M, Hayouni EA (2021) Design of a new fermented beverage from medicinal plants and organic sugarcane molasses via lactic fermentation. Appl Sci 11(13):6089. https://doi.org/10.3390/app11136089
Garcia-Solache MA, Casadevall A (2010) Global warming will bring new fungal diseases for mammals. Mbio. https://doi.org/10.1128/mBio.00061-10
Greenwalt CJ, Ledford RA, Steinkraus KH (1998) Determination and characterization of the antimicrobial activity of the fermented tea kombucha. LWT-Food Sci Technol 31(3):291–296. https://doi.org/10.1006/fstl.1997.0354
Henwood CJ, Livermore DM, James D, Warner M, Pseudomonas Study Group T (2001) Antimicrobial susceptibility of Pseudomonas aeruginosa: results of a UK survey and evaluation of the British Society for Antimicrobial Chemotherapy disc susceptibility test. J Antimicrob Chemother 47(6):789–799
Jiang S, Zhang J, Yang Q, Sun D, Pu X, Shen H, Li Q, Wang Z, Lin B (2021) Antimicrobial activity of natural plant compound carvacrol against soft rot disease agent Dickeya zeae. Curr Microbiol 78(9):3453–3463. https://doi.org/10.1007/s00284-021-02609-3
Kang HJ, Hwang IK, Kim KS, Choi HC (2003) Comparative structure and physicochemical properties of Ilpumbyeo, a high-quality japonica rice, and its mutant, Suweon 464. J Agric Food Chem 51(22):6598–6603. https://doi.org/10.1021/jf0344946
Kang CI, Kim SH, Bang JW, Kim HB, Kim NJ, Kim EC, Oh MD, Choe KW (2006) Community-acquired versus nosocomial Klebsiella pneumoniae bacteremia: clinical features, treatment outcomes, and clinical implication of antimicrobial resistance. J Korean Med Sci 21(5):816–822. https://doi.org/10.3346/jkms.2006.21.5.816
Lim YS, Kim WR (2008) The global impact of hepatic fibrosis and end-stage liver disease. Clin Liver Dis. https://doi.org/10.1016/j.cld.2008.07.007
Luana N, Rossana C, Curiel JA, Kaisa P, Marco G, Rizzello CG (2014) Manufacture and characterization of a yogurt-like beverage made with oat flakes fermented by selected lactic acid bacteria. Int J Food Microbiol 18(185):17–26. https://doi.org/10.1016/j.ijfoodmicro.2014.05.004
Lukianov DA, Debabov VG (2018) Obtainment of succinic acid and higher alcohols (C 8–C 10) diesters by biphasic esterification. Appl Biochem Microbiol 54(9):863–868. https://doi.org/10.1134/S0003683818090053
Miyake Y, Fukumoto S, Okada M, Sakaida K, Nakamura Y, Osawa T (2005) Antioxidative catechol lignans converted from sesamin and sesaminol triglucoside by culturing with Aspergillus. J Agric Food Chem. https://doi.org/10.1021/jf048743h
Naczk M, Shahidi F (2006) Phenolics in cereals, fruits and vegetables: occurrence, extraction and analysis. J Pharm Biomed Anal. https://doi.org/10.1016/j.jpba.2006.04.002
Nakano D, Kwak CJ, Fujii K, Ikemura K, Satake A, Ohkita M, Takaoka M, Ono Y, Nakai M, Tomimori N, Kiso Y (2006) Sesamin metabolites induce an endothelial nitric oxide-dependent vasorelaxation through their antioxidative property-independent mechanisms: possible involvement of the metabolites in the antihypertensive effect of sesamin. J Pharmacol Exp Thera 318(1):328–335. https://doi.org/10.1124/jpet.105.100149
Navarini L, Gilli R, Gombac V, Abatangelo A, Bosco M, Toffanin R (1999) Polysaccharides from hot water extracts of roasted Coffea arabica beans: isolation and characterization. Carbohydr Polym 40(1):71–81. https://doi.org/10.1016/S0144-8617(99)00032-6
Omafuvbe BO, Akanbi OO (2009) Microbiological and physico-chemical properties of some commercial Nigerian honey. Afr J Microbiol Res 3(12):891–896
Parvez S, Malik KA, Ah Kang S, Kim HY (2006) Probiotics and their fermented food products are beneficial for health. J Appl Microbiol 100(6):1171–1185. https://doi.org/10.1111/j.1365-2672.2006.02963.x
Pino JA, Moncayo-Molina L, Spengler I, Pérez JC (2021) Chemical composition and antibacterial activity of the leaf essential oil of Eucalyptus globulus Labill. from two highs of the canton Cañar Ecuador. Revista CENIC Ciencias Químicas 52:026–033
Rasor JP, Voss E (2001) Enzyme-catalyzed processes in pharmaceutical industry. Appl Catal A 221(1–2):145–158. https://doi.org/10.1016/S0926-860X(01)00804-3
Scarpino V, Reyneri A, Sulyok M, Krska R, Blandino M (2015) Effect of fungicide application to control Fusarium head blight and 20 Fusarium and Alternaria mycotoxins in winter wheat (Triticum aestivum L.). World Mycotoxin J 8(4):499–510. https://doi.org/10.3920/WMJ2014.1814
Sezer Ç, Güven A, Oral NB, Vatansever L (2013) Detoxification of aflatoxin B_1 by bacteriocins and bacteriocinogenic lactic acid bacteria. Turkish J Vet Anim Sci 37(5):594–601. https://doi.org/10.3906/vet-1301-31
Smid EJ, Kleerebezem M (2014) Production of aroma compounds in lactic fermentations. Annu Rev Food Sci Technol 5:313–326. https://doi.org/10.1146/annurev-food-030713-092339
Song W, Han X, Qian Y, Liu G, Yao G, Zhong Y, Qu Y (2016) Proteomic analysis of the biomass hydrolytic potentials of Penicillium oxalicum lignocellulolytic enzyme system. Biotechnol Biofuels 9(1):1–15. https://doi.org/10.1186/s13068-016-0477-2
Sreeramulu G, Zhu Y, Knol W (2001) Characterization of antimicrobial activity in Kombucha fermentation. Acta Biotechnol 21(1):49–56. https://doi.org/10.1002/1521-3846(200102)21:13.0.CO;2-G
Steinkraus KH, Shapiro KB, Hotchkiss JH, Mortlock RP (1996) Investigations into the antibiotic activity of tea fungus/kombucha beverage. Acta Biotechnol 16(2–3):199–205. https://doi.org/10.1002/abio.370160219
Stoyanova LG, Ustyugova EA, Netrusov AI (2012) Antibacterial metabolites of lactic acid bacteria: their diversity and properties. Appl Biochem Microbiol 48(3):229–243. https://doi.org/10.1134/S0003683812030143
Teplova VV, Isakova EP, Klein OI, Dergachova DI, Gessler NN, Deryabina YI (2018) Natural polyphenols: biological activity, pharmacological potential, means of metabolic engineering. Appl Biochem Microbiol 54(3):221–237. https://doi.org/10.1134/S0003683818030146
Thanusu J, Kanagarajan V, Gopalakrishnan M (2010) Synthesis, spectral characterization, and in vitro antibacterial and antifungal activities of novel 1, 3-thiazine-2-amines comprising morpholine nucleus. J Enzyme Inhib Med Chem 25(6):756–764. https://doi.org/10.3109/14756360903389898
Tian H, Shen Y, Yu H, He Y, Chen C (2017) Effects of 4 probiotic strains in coculture with traditional starters on the flavor profile of yogurt. J Food Sci 82(7):1693–1701. https://doi.org/10.1111/1750-3841.13779
Tlili N, Elfalleh W, Hannachi H, Yahia Y, Khaldi A, Ferchichi A, Nasri N (2013) Screening of natural antioxidants from selected medicinal plants. Int J Food Prop 16(5):1117–1126. https://doi.org/10.1080/10942912.2011.576360
Velićanski AS, Cvetković DD, Markov SL, Tumbas Šaponjac VT, Vulić JJ (2014) Antioxidant and antibacterial activity of the beverage obtained by fermentation of sweetened lemon balm (Melissa offi cinalis L.) tea with symbiotic consortium of bacteria and yeasts. Food Technol Biotechnol. 52(4):420–429. https://doi.org/10.17113/b.52.04.14.3611
Wu T, Wang N, Zhang Y, Xu X (2013) Advances in the study on microbial fermentation and transformation of traditional Chinese medicine. Afr J Microbiol Res 7(17):1644–1650. https://doi.org/10.5897/AJMRx12.012
Yoon KY, Woodams EE, Hang YD (2006) Production of probiotic cabbage juice by lactic acid bacteria. Bioresour Technol 97(12):1427–1430. https://doi.org/10.1016/j.biortech.2005.06.018
You L, Gao Q, Feng M, Yang B, Ren J, Gu L, Cui C, Zhao M (2013) Structural characterisation of polysaccharides from Tricholoma matsutake and their antioxidant and antitumour activities. Food Chem 138(4):2242–2249. https://doi.org/10.1016/j.foodchem.2012.11.140
Zhang Z, Lv G, Pan H, Fan L, Soccol CR, Pandey A (2012) Production of powerful antioxidant supplements via solid-state fermentation of wheat (Triticum aestivum Linn.) by Cordyceps militaris. Food Technol Biotechnol 50(1):32–39
Acknowledgements
We are grateful and provide sincere thanks to honorable Vice Chancellor University of Applied Sciences. Neubrandenburg, Germany for the infrastructure and facilities. This study supported by a grant from the Ministry of Tunisia, Laboratory of Aromatic and Medicinal Plants, Center of Biotechnology (LR15CBBC06) at the Ecopark of Borj-cédria. BP-901, 2050 Hammam-Lif. Tunisia.
Funding
This study supported by University of Tunis EL Manar, University of Applied Sciences, Neubrandenburg, Germany, for the infrastructure and facilities, and Laboratory of Aromatic and Medicinal Plants, Center of Biotechnology (LR15CBBC06) at the Ecopark of Borj-cédria. BP-901, 2050 Hammam-Lif. Tunisia.
Author information
Authors and Affiliations
Contributions
HG and AelH, M-RE, and MST designed the study and performed the experiments. HG and M-R Enriqueta performed the experiment and carried out data analyses. HG and AelH contributed to drafting the manuscript. All authors have read and approved the final version of submitted manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors of this manuscript certify that they have no affiliation with or involvement in any organization or entity with any financial interest. I certify that I am submitting the manuscript on behalf of all the authors.
Ethics approval
This article does not contain any studies with human participants performed by any of the authors.
Consent for publication
All authors have seen the manuscript and approved to submit Archives of Microbiology.
Additional information
Communicated by Erko Stackebrandt.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Gadhoumi, H., Hayouni, E.L.A., Martinez-Rojas, E. et al. Biochemical composition, antimicrobial and antifungal activities assessment of the fermented medicinal plants extract using lactic acid bacteria. Arch Microbiol 204, 374 (2022). https://doi.org/10.1007/s00203-022-02985-9
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00203-022-02985-9