Abstract
This study is aimed at evaluating the probiotic potential of three Enterococcus faecium strains (called 29-P2, 168-P6 and 277-S3) isolated from ‘pastırma’, a Turkish traditional dry-cured meat product. For this, key probiotic properties and some functional characteristics of strains were tested in vitro. Antimicrobial activity of 3 E. faecium strains was evaluated against 18 indicator microorganisms consisting of 13 foodborne pathogens and 5 lactic acid bacteria and all strains were found as the producer of antimicrobial substance. Especially one strain 168-P6 showed a remarkable activity spectrum and inhibited all of the used foodborne pathogen indicators. Antimicrobial compounds produced by strains were identified by determining the effect of enzyme, pH and temperature on antimicrobial activity. All strains exhibited tolerance to acidic conditions and a simulated gastric environment. Also, strains exhibited high adhesion capacity. The safety of the strains was assessed by determining hemolytic activity and the resistance to 14 different antibiotics. None of the three strains exhibited hemolytic activity, also strains were found reliable in terms of clinically relevant antibiotics, only one strain 29-P2 was found resistant to vancomycin. In addition, metabolic activities of strains including lactic acid, hydrogen peroxide, exopolysaccharide production and proteolytic activity were determined and amounts of all metabolic products were found low. When evaluated all data obtained, it is believed that the strains have enviable characteristics as a probiotic candidate.
Similar content being viewed by others
References
Ahhmed AM, Kaneko G, Ushio H et al (2013) Changes in physicochemical properties of proteins in Kayserian Pastirma made from the M. semimembranosus muscle of cows during traditional processing. Food Sci Hum Wellness 2:46–55
Ahmadova A, Todorov SD, Choiset Y et al (2013) Evaluation of antimicrobial activity, probiotic properties and safety of wild strain Enterococcus faecium AQ71 isolated from Azerbaijani Motal cheese. Food Control 30:631–641
Akköse A, Aktaş N (2014) Curing and diffusion coefficient study in Pastırma, a Turkish traditional meat product. Meat Sci 96:311–314
Akköse A, Kaban G, Karaoğlu MM, Kaya M (2018) Characteristics of pastırma types produced from water buffalo meat. Kafkas Univ Vet Fak Derg 24(2):179–185
Aspri M, O’Connor PM, Field D et al (2017) Application of bacteriocin-producing Enterococcus faecium isolated from donkey milk, in the bio-control of Listeria monocytogenes in fresh whey cheese. Int Dairy J 73:1–9
Banwo K, Sanni A, Tan H (2012) Technological properties and probiotic potential of Enterococcus faecium strains isolated from cow milk. J Appl Microbiol 114:229–241
Bauer AW, Kirby WMM, Sherris JC, Turck M (1966) Antibiotic susceptibility testing by a standardized single disk method. Am J Clin Pathol 45:493–496
Belgacem ZB, Abriouel H, Omar NB et al (2010) Antimicrobial activity, safety aspects and some technological properties of bacteriocinogenic Enterococcus faecium from artisanal Tunisian fermented meat. Food Control 21:462–470
Bennik MH, Verheul A, Abee T, Naaktgeboren-Stoffels G, Gorris LG, Smid EJ (1997) Interactions of nisin and pediocin pa-1 with closely related lactic acid bacteria that manifest over 100-fold differences in bacteriocin sensitivity. Appl Environ Microbiol 63:3628–3636
Braїek OB, Smaoui S (2019) Enterococci: between emerging pathogens and potential probiotics. Biomed Res Int. https://doi.org/10.1155/2019/5938210
Clinical and Laboratory Standards Institute (2013) Performance standards for antimicrobial susceptibility testing, twentieth informational supplement M100-S23. Wayne, PA, USA
Corcoran BM, Stanton C, Fitzgerald GF, Ross RP (2005) Survival of probiotic lactobacilli in acidic environments is enhanced in the presence of metabolizable sugars. Appl Environ Microbiol 71:3060–3067
Demirci M, Gunduz H (1994) Dairy technology handbook. Hasad, Ankara
Dincer E, Kivanc M (2012) Characterization of lactic acid bacteria from Turkish Pastirma. Ann Microbiol 62:1155–1163
Dündar H (2016) Bacteriocinogenic potential of Enterococcus faecium isolated from wine. Probiot Antimicrob Prot 8:150–160
El-Ghaish S, El-Baz A, Hwanhlem N et al (2015) Bacteriocin production and safety evaluation of non-starter Enterococcus faecium IM1 and Enterococcus hirae IM1 strains isolated from homemade Egyptian dairy products. Eur Food Res Technol. https://doi.org/10.1007/s00217-015-2424-z
Food and Agriculture Organization/World Health Organization (2002) Guidelines for the evaluation of probiotics in food: report of a joint FAO/WHO Working Group on drafting guidelines for the evaluation of probiotics in food. FAO/WHO, London, ON, Canada
Foulquié MorenoSarantinopoulosTsakalidou MRPEL, De Vuyst (2006) The role and application of enterococci in food and health. Int J Food Microbiol 106:1–24
Guo L, Li T, Tang Y, Yang L, Huo G (2015) Probiotic properties of Enterococcus strains isolated from traditional naturally fermented cream in China. Microb Biotechnol 9:737–745
Hadji-Sfaxi I, El-Ghaish S, Ahmadova A et al (2011) Antimicrobial activity and safety of use of Enterococcus faecium PC4.1 isolated from Mongol yogurt. Food Control 22:2020–2027
Hanchi H, Mottawea W, Sebei K, Hammami R (2018) The genus enterococcus: between probiotic potential and safety concerns—an update. Front Microbiol. https://doi.org/10.3389/fmicb.2018.01791
Hosseini SV, Arlindo S, Böhme K, Fernàndez-No C, Calo-Mata P, Barros-Velàzquez J (2009) Molecular and probiotic characterization of bacteriocin-producing Enterococcus faecium strains isolated from nonfermented animal foods. J Appl Microbiol 107:1392–1403
Hugas M, Garriga M, Aymerich MT (2003) Functionality of enterococci in meat products. Int J Food Microbiol 88:223–233
Khan H, Flint S, Yu PL (2010) Enterocins in food preservation. Int J Food Microbiol 141:1–10
Kıvanç SA, Kıvanç M, Yiğit T (2016) Antibiotic susceptibility, antibacterial activity and characterisation of Enterococcus faecium strains isolated from breast milk. Exp Ther Med 12:1732–1740
Nueno-Palop C, Narbad A (2011) Probiotic assessment of Enterococcus faecalis CP58 isolated from human gut. Int J Food Microbiol 145:390–394
Öz E, Kaban G, Barış Ö, Kaya M (2017) Isolation and identification of lactic acid bacteria from pastırma. Food Cont 77:158–162
Patrick WA, Wagner HB (1949) Determination of hydrogen peroxide in small concentrations. Anal Chem 21:1279–1289
Rajagopal SN, Sandine WE (1990) Associative growth and proteolysis of Streptococcus thermophilus and Lactobacillus bulgaricus in skim milk. J Dairy Sci 73:894–899
Rivas FP, Castro MP, Vallejo M, Marguet E, Campos CA (2012) Antibacterial potential of Enterococcus faecium strains isolated from ewes’ milk and cheese. LWT-Food Sci Technol 46:428–436
Ruas-Madiedo P, De Los Reyes-Gavilán CG (2005) Invited review: methods for the screening, isolation, and characterization of exopolysaccharides produced by lactic acid bacteria. J Dairy Sci 88:843–856
Semedo T, Almeida Santos M, Martins P et al (2003) Comparative study using type strains and clinical and food isolates to examine hemolytic activity and occurrence of the cyl operon in Enterococci. J Clin Microbiol 41(6):2569–2576
Shi Y, Zhai M, Li J, Li B (2019) Evaluation of safety and probiotic properties of a strain of Enterococcus faecium isolated from chicken bile. J Food Sci Technol. https://doi.org/10.1007/s13197-019-04089-7
Tagg JR, McGiven AR (1971) Assay system for bacteriocins. Appl Microbiol 21:943
Thirabunyanon M, Boonprasom P, Niamsup P (2009) Probiotic potential of lactic acid bacteria isolated from fermented dairy milks on antiproliferation of colon cancer cells. Biotechnol Lett 31:571–576
Tinrat S, Khuntayaporn P, Thirapanmethee K, Chomnawang MT (2018) In vitro assessment of Enterococcus faecalis MTC 1032 as the potential probiotic in food supplements. J Food Sci Technol 55(7):2384–2394
Zhu WM, Liu W, Wu DQ (2000) Isolation and characterization of a new bacteriocin from Lactobacillus gasseri KT7. J Appl Microbiol 88:877–886
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
No conflict of interest exists in the submission of this manuscript and the manuscript is approved by all authors for publication.
Ethical approval
The paper has been submitted with full responsibility, following the due ethical procedure, also no human participants and/or animals were used.
Financial disclosure
The authors of this manuscript have no financial or personal relationship with other people or organizations that could inappropriately influence or bias the content of the paper.
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
Dinçer, E., Kıvanç, M. In vitro evaluation of probiotic potential of Enterococcus faecium strains isolated from Turkish pastırma. Arch Microbiol 203, 2831–2841 (2021). https://doi.org/10.1007/s00203-021-02273-y
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00203-021-02273-y