Skip to main content
Log in

Evaluation of antioxidant, antibacterial and cytotoxicity activities of exopolysaccharide from Enterococcus strains isolated from traditional Iranian Kishk

  • Original Paper
  • Published:
Journal of Food Measurement and Characterization Aims and scope Submit manuscript

Abstract

In this study, the antimicrobial effect of exopolysaccharide (EPS) extracted from Enterococcus strains [E. durans K48 (MT437,248), E. faecium R114 (MT437,249) and E. faecium T52 (MT437,250)] isolated from Kishk was applied against some foodborne pathogenic bacteria using well diffusion and microdilution methods. The antioxidant activity of EPS was also evaluated by 1,1-diphenyl-2-picrylhydrazyl (DPPH) scavenging assay and ferric reducing antioxidant power (FRAP) method. The cytotoxicity effect of EPS on human Gingival Fibroblast (HGF) cell line was also assessed. The results obtained by antimicrobial test showed that the most resistant bacteria to the examined EPS was Listeria monocytogenes, and the most susceptible were Staphylococcus aureus and E. faecalis. The results showed that the DPPH inhibitory percentage of EPS (25 mg/mL) from E. durans K48, E. faecium R114, and E. faecium T52 was 53%, 58% and 64%, respectively. EPS from E. faecium T52 displayed the highest reducing power, but statistically, there was no significant difference between the reducing power of EPS T52 and EPS R114 (P ≥ 0.05). The lowest toxicity percentage of EPS k48, EPS T52, and EPS R114 on normal human cell line at a concentration of 0.2 mg/mL was 10%, 15%, and 13%, respectively, which was statistically significant (P < 0.05). The obtained results in the present study indicate that EPS from the examined LAB strains with no in vitro cytotoxicity can be a potential source of natural antioxidant and antibacterial agent to be used in food and pharmaceutical industries.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. A. Tamime et al., Effect of processing conditions and raw materials on the properties of Kishk 1. Compositional and microbiological qualities. LWT-Food Sci. Technol. 33(6), 444–451 (2000)

    Article  CAS  Google Scholar 

  2. M.G. Gadallah, M.F. Hassan, Quality properties of Kishk (a dried fermented cereal-milk mixture) prepared from different raw materials. J. Saudi Soc. Agric. Sci. 18(1), 95–101 (2019)

    Google Scholar 

  3. G.S. Kiran et al., Characterization of an exopolysaccharide from probiont Enterobacter faecalis MSI12 and its effect on the disruption of Candida albicans biofilm. RSC Adv. 5(88), 71573–71585 (2015)

    Article  CAS  Google Scholar 

  4. H. Yildiz, N.J.P.B. Karatas, Microbial exopolysaccharides: resources and bioactive properties. Process Biochem. 72, 41–46 (2018)

    Article  CAS  Google Scholar 

  5. Y.R. Saadat, A.Y. Khosroushahi, J.C.P. Gargari, A comprehensive review of anticancer, immunomodulatory and health beneficial effects of the lactic acid bacteria exopolysaccharides. Carbohydr. Polym. 217, 79–89 (2019)

    Article  CAS  Google Scholar 

  6. S.C. Lourenço, M. Moldão-Martins, V.D. Alves, Antioxidants of natural plant origins: from sources to food industry applications. Molecules 24(22), 4132 (2019)

    Article  PubMed Central  CAS  Google Scholar 

  7. R. Liu, S.A. Mabury, Synthetic phenolic antioxidants: a review of environmental occurrence, fate, human exposure, and toxicity. Environ. Sci. Technol. 54(19), 11706–11719 (2020)

    Article  CAS  PubMed  Google Scholar 

  8. T.M. Abdelghany, Safe food additives: a review. J. Biol. Chem. Res. 32(1), 402–437 (2015)

    Google Scholar 

  9. V.B. Bomfim et al., Partial characterization and antioxidant activity of exopolysaccharides produced by Lactobacillus plantarum CNPC003. LWT-Food Sci. Technol. 127, 109349 (2020)

    Article  CAS  Google Scholar 

  10. N.M. El-Deeb et al., A novel purified Lactobacillus acidophilus 20079 exopolysaccharide, LA-EPS-20079, molecularly regulates both apoptotic and NF-ΚB inflammatory pathways in human colon cancer. Microb. Cell. Fact. 17(1), 29 (2018)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  11. M. Ayyash et al., Exopolysaccharide produced by potential probiotic Enterococcus faecium MS79: characterization, bioactivities and rheological properties influenced by salt and pH. LWT-Food Sci. Technol. 131, 109741 (2020)

    Article  CAS  Google Scholar 

  12. Y. Nami et al., A newly isolated probiotic Enterococcus faecalis strain from vagina microbiota enhances apoptosis of human cancer cells. J. Appl. Microbiol. 117(2), 498–508 (2014)

    Article  CAS  PubMed  Google Scholar 

  13. B. Haghshenas et al., Anti-proliferative effects of Enterococcus strains isolated from fermented dairy products on different cancer cell lines. J. Funct. Foods 11, 363–374 (2014)

    Article  CAS  Google Scholar 

  14. M.G. Allam et al., Lactococcus species for conventional Karish cheese conservation. LWT-Food Sci. Technol. 79, 625–631 (2017)

    Article  CAS  Google Scholar 

  15. Y. Nami et al., Probiotic properties of Enterococcus isolated from artisanal dairy products. Front. Microbiol. 10, 300 (2019)

    Article  PubMed  PubMed Central  Google Scholar 

  16. A. Abushelaibi et al., Characterization of potential probiotic lactic acid bacteria isolated from camel milk. LWT-Food Sci. Technol. 79, 316–325 (2017)

    Article  CAS  Google Scholar 

  17. M. Al-Balawi, F.M. Morsy, Enterococcus faecalis is a better competitor than other lactic acid bacteria in the initial colonization of colon of healthy newborn babies at first week of their life. Front. Microbiol. (2020). https://doi.org/10.3389/fmicb.2020.02017

    Article  PubMed  PubMed Central  Google Scholar 

  18. J. Yu et al., Diversity of lactic acid bacteria associated with traditional fermented dairy products in Mongolia. J. Dairy Sci. 94(7), 3229–3241 (2011)

    Article  CAS  PubMed  Google Scholar 

  19. Y. Lee et al., Identification of lactic acid bacteria in Galchi- and Myeolchi-Jeotgal by 16S rRNA gene sequencing, MALDI-TOF mass spectrometry, and PCR-DGGE. J. Microbiol. Biotechnol. 28(7), 1112–1121 (2018)

    Article  CAS  PubMed  Google Scholar 

  20. D. Jeong et al., Characterization and antibacterial activity of a novel exopolysaccharide produced by Lactobacillus kefiranofaciens DN1 isolated from kefir. Food Control 78, 436–442 (2017)

    Article  CAS  Google Scholar 

  21. J.-Y. Li et al., Exopolysaccharide from Lactobacillus planterum LP6: antioxidation and the effect on oxidative stress. Carbohydr. Polym. 98(1), 1147–1152 (2013)

    Article  CAS  PubMed  Google Scholar 

  22. M. Dubois et al., Colorimetric method for determination of sugars and related substances. Anal. Chem. 28(3), 350–356 (1956)

    Article  CAS  Google Scholar 

  23. M.Y.M. Imran et al., Statistical optimization of exopolysaccharide production by Lactobacillus plantarum NTMI05 and NTMI20. Int. J. Biol. Macromol. 93, 731–745 (2016)

    Article  CAS  PubMed  Google Scholar 

  24. F.R. Cockerill et al., Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria That Grow Aerobically; Approved Standard (Clinical and Laboratory Standards Institute, Wayne, 2012)

    Google Scholar 

  25. I. Wiegand, K. Hilpert, J.N.P. Hancock, Agar and broth dilution methods to determine the minimal inhibitory concentration (MIC) of antimicrobial substances. Nat. Protoc. 3(2), 163 (2008)

    Article  CAS  PubMed  Google Scholar 

  26. Y. Abid et al., Production and structural characterization of exopolysaccharides from newly isolated probiotic lactic acid bacteria. Int. J. Biol. Macromol. 108, 719–728 (2018)

    Article  CAS  PubMed  Google Scholar 

  27. M. Balouiri, M. Sadiki, S.K. Ibnsouda, Methods for in vitro evaluating antimicrobial activity: a review. J. Pharm. Anal. 6(2), 71–79 (2016)

    Article  PubMed  Google Scholar 

  28. M. Sardarodiyan et al., Antioxidant and antimicrobial activities of water-soluble polysaccharide isolated from Balangu seed (Lallemantia royleana) gum. J. Anal. Sci. Technol. 10(1), 17 (2019)

    Article  Google Scholar 

  29. P. Mojibi, F. Tafvizi, M.B. Torbati, Cell-bound exopolysaccharide extract from indigenous probiotic bacteria induce apoptosis in HT–29 cell-line. Iran. J. Pathol. 14(1), 41 (2019)

    Article  PubMed  Google Scholar 

  30. B. Ismail, K.J.B. Nampoothiri, Exposition of antitumour activity of a chemically characterized exopolysaccharide from a probiotic Lactobacillus plantarum MTCC 9510. Biologia 68(6), 1041–1047 (2013)

    Article  CAS  Google Scholar 

  31. F. Zuo et al., Identification and partial characterization of lactic acid bacteria isolated from traditional dairy products produced by herders in the western Tianshan Mountains of China. Lett. Appl. Microbiol. 59(5), 549–556 (2014)

    Article  CAS  PubMed  Google Scholar 

  32. H. Avnİ Kırmacı et al., Identification and characterisation of lactic acid bacteria isolated from traditional Urfa cheese. Int. J. Dairy Technol. 69(2), 301–307 (2016)

    Article  CAS  Google Scholar 

  33. X. Ao et al., Identification of lactic acid bacteria in traditional fermented yak milk and evaluation of their application in fermented milk products. J. Dairy Sci. 95(3), 1073–1084 (2012)

    Article  CAS  PubMed  Google Scholar 

  34. B. Bhat, J.B. Bajaj, Hypocholesterolemic and bioactive potential of exopolysaccharide from a probiotic Enterococcus faecium K1 isolated from kalarei. Bioresour. Technol. 254, 264–267 (2018)

    Article  CAS  PubMed  Google Scholar 

  35. F. Leroy, L. De Vuyst , Advances in production and simplified methods for recovery and quantification of exopolysaccharides for applications in food and health. J. Dairy Sci. 99(4), 3229–3238 (2016)

    Article  CAS  PubMed  Google Scholar 

  36. F. Freitas, V.D. Alves, M.A. Reis, Advances in bacterial exopolysaccharides: from production to biotechnological applications. Trends Biotechnol. 29(8), 388–398 (2011)

    Article  CAS  PubMed  Google Scholar 

  37. P. Kanmani et al., Synthesis and functional characterization of antibiofilm exopolysaccharide produced by Enterococcus faecium MC13 isolated from the gut of fish. Appl. Biochem. Biotechnol. 169(3), 1001–1015 (2013)

    Article  CAS  PubMed  Google Scholar 

  38. P. Kanmani et al., Production and purification of a novel exopolysaccharide from lactic acid bacterium Streptococcus phocae PI80 and its functional characteristics activity in vitro. Bioresour. Technol. 102(7), 4827–4833 (2011)

    Article  CAS  PubMed  Google Scholar 

  39. K. Abdhul et al., Antioxidant activity of exopolysaccharide from probiotic strain Enterococcus faecium (BDU7) from Ngari. Int. J. Biol. Macromol. 70, 450–454 (2014)

    Article  CAS  PubMed  Google Scholar 

  40. P. Venkatesh et al., Physicochemical and biosorption properties of novel exopolysaccharide produced by Enterococcus faecalis. LWT-Food Sci. Technol. 68, 606–614 (2016)

    Article  CAS  Google Scholar 

  41. M.S.R. Rajoka et al., Antibacterial and antioxidant activity of exopolysaccharide mediated silver nanoparticle synthesized by Lactobacillus brevis isolated from Chinese koumiss. Colloids Surf. B Biointerfaces 186, 110734 (2020)

    Article  CAS  Google Scholar 

  42. X. Wang et al., Optimization, partial characterization and antioxidant activity of an exopolysaccharide from Lactobacillus plantarum KX041. Int. J. Biol. Macromol. 103, 1173–1184 (2017)

    Article  CAS  PubMed  Google Scholar 

  43. A.O. Adelekan, T.O. Olurin, A.O. Ezeani, Antioxidant activities of exopolysaccharides produced by lactic acid bacteria isolated from commercial yoghurt samples. Adv. Microbiol. 10(08), 359 (2020)

    Article  CAS  Google Scholar 

  44. B. Adebayo-Tayo, R.J.H. Fashogbon, In vitro antioxidant, antibacterial, in vivo immunomodulatory, antitumor and hematological potential of exopolysaccharide produced by wild type and mutant Lactobacillus delbureckii subsp. bulgaricus. Heliyon 6(2), e03268 (2020)

    Article  PubMed  PubMed Central  Google Scholar 

  45. C.-F. Liu, T.-M. Pan, In vitro effects of lactic acid bacteria on cancer cell viability and antioxidant activity. J. Food Drug Anal. 18(2), 77 (2010)

    Google Scholar 

  46. T.-W. Liang, S.-C. Tseng, S.-L.JMd. Wang, Production and characterization of antioxidant properties of exopolysaccharide(s) from Peanibacillus mucilaginosus TKU032. Mar. Drugs 14(2), 40 (2016)

    Article  PubMed Central  CAS  Google Scholar 

  47. Clinical Laboratory Standard Institute, Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria that Grow Aerobically; M07, 12th edn. (CSLI, Wayen, PA, 2012)

  48. R. Lambert, Susceptibility testing: inoculum size dependency of inhibition using the Colworth MIC technique. J. Appl. Microbiol. 89(2), 275–279 (2000)

    Article  CAS  PubMed  Google Scholar 

  49. J. Zhang et al., Physicochemical characteristics and bioactivities of the exopolysaccharide and its sulphated polymer from Streptococcus thermophilus GST-6. Carbohydr. Polym. 146, 368–375 (2016)

    Article  CAS  PubMed  Google Scholar 

  50. F. Nehal et al., Characterization, high production and antimicrobial activity of exopolysaccharides from Lactococcus lactis F-mou. Microb. Pathog. 132, 10–19 (2019)

    Article  CAS  PubMed  Google Scholar 

  51. A. Hauser, Antibiotic Basics for Clinicians: The ABCs of Choosing the Right Antibacterial Agent, 2nd edn. (Lippincott Williams & Wilkins, Philadelphia, 2018)

    Google Scholar 

  52. A.H. Delcour, Outer membrane permeability and antibiotic resistance. Biochimica et Biophysica Acta-Proteins Proteomics 1794(5), 808–816 (2009)

    Article  CAS  Google Scholar 

  53. M. Galindo-Méndez, Antimicrobial resistance in Escherichia coli, in E. coli Infections: Importance of Early Diagnosis and Efficient Treatment (IntechOpen, London, 2020)

  54. Z. Benattouche, D. Bouhadi, G.B. Raho, Antioxidant and antibacterial activities of exopolysaccharides produced by lactic acid bacteria isolated from yogurt. Int. J. Food Stud. 7(2), 30–37 (2018)

    Article  Google Scholar 

  55. F. He et al., Studies on antibacterial activity and antibacterial mechanism of a novel polysaccharide from Streptomyces virginia H03. Food Control 21(9), 1257–1262 (2010)

    Article  CAS  Google Scholar 

  56. D. Du et al., Effect of complex coordinating tea polysaccharide with cerium on degradation of plasmid DNA and organophosphorous pesticides. J. Chin. Rare Earth Soc. 23(1), 118–121 (2005)

    CAS  Google Scholar 

  57. M.S.R. Rajoka et al., Characterization, the antioxidant and antimicrobial activity of exopolysaccharide isolated from poultry origin Lactobacilli. Probiotics Antimicrob. Proteins 11(4), 1132–1142 (2019)

    Article  CAS  PubMed  Google Scholar 

  58. P. Weissman-Shomer, M. Fry, Chick embryo fibroblasts senescence in vitro: pattern of cell division and life span as a function of cell density. Mech. Ageing Dev. 4, 159–166 (1975)

    Article  CAS  PubMed  Google Scholar 

  59. H.I. EL-Adawi et al., Cytotoxicity assay and antioxidant activities of the lactic acid bacterial strains. Afr. J. Microbiol. Res. 6(8), 1700–1712 (2012)

    Google Scholar 

  60. M.S. Selim et al., Production and characterisation of exopolysaccharide from Streptomyces carpaticus isolated from marine sediments in Egypt and its effect on breast and colon cell lines. J. Genet. Eng. Biotechnol. 16(1), 23–28 (2018)

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

This work was financially supported by a Grant (No. 47333) from Ferdowsi University of Mashhad (Research affairs), Iran.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mohammad Bagher Habibi Najafi.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rahnama Vosough, P., Habibi Najafi, M.B., Edalatian Dovom, M.R. et al. Evaluation of antioxidant, antibacterial and cytotoxicity activities of exopolysaccharide from Enterococcus strains isolated from traditional Iranian Kishk. Food Measure 15, 5221–5230 (2021). https://doi.org/10.1007/s11694-021-01092-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11694-021-01092-5

Keywords

Navigation