Abstract
The current study was carried out to investigate metabolic activities and main probiotic characteristics of two Latilactobacillus sakei strains (8.P1 and 28.P2) isolated from pastırma, a highly seasoned, air-dried cured beef. Both strains showed antimicrobial activity against important foodborne pathogens like Listeria monocytogenes, Staphylococcus aureus, Pseudomonas aeruginosa and so forth. For the characterization of antimicrobial activity, the effect of various enzymes, temperature and pH were tested. The results of the tests demonstrated that the antimicrobial activity of strains was based on the production of protein-structured compounds such as bacteriocin or bacteriocin like peptides. In metabolic activity studies, amounts of the lactic acid, proteolytic activity and hydrogen peroxide produced by the 8.P1 and 28.P2 were found to range between 16.09 and 17.32 mg/mL, 0.24 and 0.04 mg/mL and 0.98 and 0.04 µg/mL, respectively. It was also observed that neither strain could produce exopolysaccharide. Both strains were found susceptible to vancomycin, chloramphenicol, gentamicin, tetracycline, and netilmicin sulfate. When the strains are evaluated with respect to their probiotic potential, 28.P2 could tolerate acidic conditions, but 8.P1 showed sensitivity. The survival rate of the strains in the simulated gastric juice and their adhesion abilities were found suitable to stay alive in the gastrointestinal tract and to proliferate in the intestine. The evaluation of all the features of both strains demonstrated that both strains had the potential to be used as a protective culture. In addition, it was observed that 8.P1 and 28.P2 were more suitable as a starter culture and a probiotic candidate respectively.
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References
Abd-Elghany SM, El-Makhzangy AM, El-Shawaf AEM, El-Mougy RM, Sallam KI (2020) Ensuring the best storage temperature of Egyptian pastrami based on microbiological, physico-chemical and sensory evaluation. J Stored Prod Res 87:101626. https://doi.org/10.1016/j.jspr.2020.101626
Ahire JJ, Jakkamsetty C, Kashikar MS, Lakshmi SG, Madempudi RS (2021) In vitro evaluation of probiotic properties of Lactobacillus plantarum UBLP40 isolated from traditional indigenous fermented food. Probiotics Antimicrob Proteins. https://doi.org/10.1007/s12602-021-09775-7
Aksu M, Erdemir E, Turan E, Sat İG (2020) Effects of red beet extracts on protein and lipid oxidation, colour, microbial, sensory properties and storage stability of Turkish pastırma. J Stored Prod Res 89:101721. https://doi.org/10.1016/j.jspr.2020.101721
Ammor MS, Flórez AB, Mayo B (2007) Antibiotic resistance in non-enterococcal lactic acid bacteria and bifidobacteria. Food Microbiol 24(6):559–570. https://doi.org/10.1016/j.fm.2006.11.001
An H, Zhou H, Huang Y et al (2010) l High-eve expression of heme-dependent cataase gene katA from Lactobacius sakei protects Lactobacius rhamnosus from oxidative stress. Mo Biotechno 45(2):155–160. https://doi.org/10.1007/s12033-010-9254-9
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. https://doi.org/10.1111/jam.12031
Barbieri F, Laghi L, Gardini F, Montanari C, Tabanelli G (2020) Metabolism of Lactobacillus sakei Chr82 in the presence of different amounts of fermentable sugars. Foods 9(6):720. https://doi.org/10.3390/foods9060720
Barbosa MS, Todorov SD, Belguesmia Y et al (2014) Purification and characterization of the bacteriocin produced by Lactobacillus sakei MBSa1 isolated from Brazilian salami. J Appl Microbiol 116(5):1195–1208. https://doi.org/10.1111/jam.12438
Batdorj B, Trinetta V, Dagaarrondo M et al (2007) Isoation, taxonomic identification and hydrogen peroxide production by Lactobacius debrueckii subsp. actis T31 isoated from Mongoian yoghurt: inhibitory activity on food-borne pathogens. J App Microbio 103(3):584–593. https://doi.org/10.1111/j.1365-2672.2007.03279.x
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
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. https://doi.org/10.1128/aem.63.9.3628-3636.1997
Bhat B, Bajaj BK (2019) Hypocholesterolemic potential of probiotics: concept and mechanistic insights. Indian J Exp Biol 57:73–85
Campedei I, Mathur H, Savetti E et al (2019) l Genus-wide assessment of antibiotic resistance in Lactobacius spp. Appl Environ Microbiol. https://doi.org/10.1128/AEM.01738-18
Celik OF, Con AH, Saygin H, Şahin N, Temiz H (2021) Isolation and Identification of lactobacilli from traditional yogurts as potential starter cultures. LWT Food Sci Technol. https://doi.org/10.1016/j.lwt.2021.111774
Champomier-Vergès MC, Chaillou S, Cornet M, Zagorec M (2001) Lactobacillus sakei: recent developments and future prospects. Res Microbiol 152(10):839–848. https://doi.org/10.1016/S0923-2508(01)01267-0
Citti JE, Sandine WE, Elliker PR (1963) Some observation on the hull method for measurement of proteolysis in milk. J Dairy Sci 46:337–345
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. https://doi.org/10.1128/AEM.71.6.3060-3067.2005
Da Silva Cardoso P, Fagundes JM, Couto DS, de Marchi Pires E, Guimarães CED, Ribeiro CDF, Otero DM (2020) From curing to smoking: processes and techniques for the production of pastrami. Braz J Dev. https://doi.org/10.34117/bjdv6n8-538
Demirci M, Gunduz H (1994) Dairy Technology Handbook. Hasad, Ankara
Dertli E, Yilmaz MT, Tatlisu NB, Toker OS, Cankurt H, Sagdic O (2016) Effects of in situ exopolysaccharide production and fermentation conditions on physicochemical, microbiological, textural and microstructural properties of Turkish-type fermented sausage (sucuk). Meat Sci 121:156–165. https://doi.org/10.1016/j.meatsci.2016.06.008
Dincer E, Kivanc M (2012) Characterization of lactic acid bacteria from Turkish Pastirma. Ann Microbiol 62:1155–1163. https://doi.org/10.1007/s13213-011-0355-x
Dušková M, Morávková M, Mrázek J, Florianová M, Vorlová L, Karpíšková R (2021) Assessment of antibiotic resistance in starter and non-starter lactobacilli of food origin. Acta Vet Brno 89(4):401–411. https://doi.org/10.2754/avb202089040401
EFSA (2018) Guidance on the characterisation of microorganisms used as feed additives or as production organisms. EFSA J 16(3):5206. https://doi.org/10.2903/j.efsa.2018.5206
Er S, Koparal AT, Kivanc M (2015) Cytotoxic effects of various lactic acid bacteria on Caco-2 cells. Turk J Biol 39:23–30. https://doi.org/10.3906/biy-1402-62
FAO/WHO (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. London, ON, Canada
Gomes BC, Rodrigues MR, Winkelströter LK, Nomizo A, de Martinis EC (2012) In vitro evaluation of the probiotic potential of bacteriocin producer Lactobacillus sakei 1. J Food Prot 75(6):1083–1089. https://doi.org/10.4315/0362-028X.JFP-11-523
Hill C, Guarner F, Reid G et al (2014) The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastroenterol Hepatol 11(8):506–514. https://doi.org/10.1038/nrgastro.2014.66
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. https://doi.org/10.1111/j.1365-2672.2009.04327.x
Kivanc M, Yilmaz M, Çakir E (2011) Isolation and identification of lactic acid bacteria from boza, and their microbial activity against several reporter strains. Turk J Biol 35(3):313–324. https://doi.org/10.3906/biy-0906-67
Kim H, Shin M, Ryu S, Yun B, Oh S, Park DJ, Kim Y (2021) Evaluation of probiotic characteristics of newly isolated lactic acid bacteria from dry-aged Hanwoo beef. Food Sci Anim Resour 41(3):468. https://doi.org/10.5851/kosfa.2021.e11
Lewus CB, Sun S, Montville TJ (1992) Production of an amylase-sensitive bacteriocin by an atypical Leuconostoc paramesenteroides strain. Appl Environ Microbiol 58(1):143–149. https://doi.org/10.1128/aem.58.1.143-149.1992
Lim S, Moon JH, Shin CM, Jeong D, Kim B (2020) Effect of Lactobacillus sakei, a probiotic derived from kimchi, on body fat in koreans with obesity: a randomized controlled study. Endocrinol Metab 35(2):425–434. https://doi.org/10.3803/EnM.2020.35.2.425
Mogoşanu GD, Grumezescu AM, Bejenaru C, Bejenaru LE (2017) Natural products used for food preservation. In: Grumezescu A (ed) Food Preservation, first edn. Academic Press, Massachusetts, pp 365–411
Montanari C, Barbieri F, Magnani M, Grazia L, Gardini F, Tabanelli G (2018) Phenotypic diversity of Lactobacillus sakei strains. Front Microbiol 9:2003. https://doi.org/10.3389/fmicb.2018.02003
Mulaw G, Sisay Tessema T, Muleta D, Tesfaye A (2019) In vitro evaluation of probiotic properties of lactic acid bacteria isolated from some traditionally fermented Ethiopian food products. Int J Microbiol. https://doi.org/10.1155/2019/7179514
Ouwehand AC, Salminen S (2003) In vitro adhesion assays for probiotics and their in vivo relevance: a review. Microb Ecol Health Dis 15(4):175–184. https://doi.org/10.1080/08910600310019886
Özen M, Dinleyici EC (2015) The history of probiotics: the untold story. Benef Microbes 6(2):159–165. https://doi.org/10.3920/BM2014.0103
Patrick WA, Wagner HB Determination of hydrogen peroxide in small concentrations. Anal Chem 21:1279–1289. https://doi.org/10.1021/ac60034a038
Puebla-Barragan S, Reid G (1949) (2019) Forty-five-year evolution of probiotic therapy. Microb Cell 6(4):184–196. https://doi.org/10.15698/mic2019.04.673
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. https://doi.org/10.3168/jds.S0022-0302(05)72750-8
Sawa N, Koga S, Okamura K, Ishibashi N, Zendo T, Sonomoto K (2013) Identification and characterization of novel multiple bacteriocins produced by Lactobacillus sakei D98. J Appl Microbiol 115(1):61–69. https://doi.org/10.1111/jam.12226
Schillinger U, Lücke FK (1989) Antibacterial activity of Lactobacillus sake isolated from meat. Appl Environ Microbiol 55(8):1901–1906. https://doi.org/10.1128/aem.55.8.1901-1906.1989
Seo SH, Jung M, Kim WJ (2014) Antilisterial and amylase-sensitive bacteriocin producing Enterococcus faecium SH01 from Mukeunji, a Korean over-ripened Kimchi. Food Sci Biotechnol 23(4):1177–1184. https://doi.org/10.1007/s10068-014-0161-x
Tagg JR, McGiven AR (1971) Assay system for bacteriocins. Appl Microbiol 21:943. https://doi.org/10.1128/am.21.5.943-943.1971
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. https://doi.org/10.1007/s10529-008-9902-3
Todorov SD, Vaz-Velho M, de Melo Franco BDG, Holzapfel WH (2013) Partial characterization of bacteriocins produced by three strains of Lactobacillus sakei, isolated from salpicao, a fermented meat product from North-West of Portugal. Food Control 30(1):111–121. https://doi.org/10.1016/j.foodcont.2012.07.022
Topçu KC, Kaya M, Kaban G (2020) Probiotic properties of lactic acid bacteria strains isolated from pastırma. LWT Food Sci Technol 134:110216. https://doi.org/10.1016/j.lwt.2020.110216
Trush EA, Poluektova EA, Beniashvili AG, Shifrin OS, Poluektov YM, Ivashkin VT (2020) The evolution of human probiotics: challenges and prospects. Probiotics Antimicrob Proteins 12(4):1291–1299. https://doi.org/10.1007/s12602-019-09628-4
Won SM, Chen S, Park KW, Yoon JH (2020) Isolation of lactic acid bacteria from kimchi and screening of Lactobacillus sakei ADM14 with anti-adipogenic effect and potential probiotic properties. LWT Food Sci Technol 126:109296. https://doi.org/10.1016/j.lwt.2020.109296
Yüksekdağ ZN, Beyatli Y, Aslim B (2004) Determination of some characteristics coccoid forms of lactic acid bacteria isolated from Turkish kefirs with natural probiotic. LWT-Food Sci Technol 37(6):663–667. https://doi.org/10.1016/j.lwt.2004.02.004
Yuksekdag ZN, Aslım B (2010) Assessment of potential probiotic and starter properties of Pediococcu spp. isolated from Turkish-Type Fermented Sausages (Sucuk). J Microbiol Biotechnol 20:161–168. https://doi.org/10.4014/jmb.0904.04019
Zagorec M, Champomier-Vergès MC (2017) Lactobacillus sakei: a starter for sausage fermentation, a protective culture for meat products. Microorganisms 5(3):56. https://doi.org/10.3390/microorganisms5030056
Zalán Z, Németh E, Baráth Á, Halász A (2005) Influence of growth medium on hydrogen peroxide and bacteriocin production of Lactobacillus strains. Food Technol Biotechnol 43(3):219–225
Zheng J, Wittouck S, Salvetti E et al (2020) A taxonomic note on the genus Lactobacillus: Description of 23 novel genera, emended description of the genus Lactobacillus Beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae. Int J Sys Evol Microbiol 70:2782–2858. https://doi.org/10.1099/ijsem.0.004107
Zhu WM, Liu W, Wu DQ (2000) Isolation and characterization of a new bacteriocin from Lactobacillus gasseri KT7. J Appl Microbiol 88:877–886. https://doi.org/10.1046/j.1365-2672.2000.01027.x
Zonenschain D, Rebecchi A, Morelli L (2009) Erythromycin-and tetracycline‐resistant lactobacilli in Italian fermented dry sausages. J App Microbiol 107(5):1559–1568. https://doi.org/10.1111/j.1365-2672.2009.04338.x
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ED: All analysis were performed. Data evaluation was performed with MK who was a consultant in the study. ED: First draft of the manuscript was written and final version was edited with MK.
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Dincer, E., Kivanc, M. Evaluation of metabolic activities and probiotic characteristics of two Latilactobacillus sakei strains isolated from pastırma. World J Microbiol Biotechnol 38, 237 (2022). https://doi.org/10.1007/s11274-022-03431-0
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DOI: https://doi.org/10.1007/s11274-022-03431-0