DOI QR코드

DOI QR Code

Assessment of Potential Probiotic and Starter Properties of Pediococcus spp. Isolated from Turkish-Type Fermented Sausages (Sucuk)

  • Yuksekdag, Z. Nur (Department of Biology, Faculty of Science and Arts, Gazi University) ;
  • Aslim, Belma (Department of Biology, Faculty of Science and Arts, Gazi University)
  • Published : 2010.01.31

Abstract

In this study, the metabolic activities of five strains of Pediococcus spp., in terms of the quantities they produced of lactic acid, hydrogen peroxide, exopolysaccharides, and proteolytic activity, were determined. Lactic acid levels produced by these strains were found to be in the range of 2.5-5.6 mg/ml. All strains produced hydrogen peroxide. The P. pentosaceus Z13P strain produced the maximum amount (0.25 mg/ml) of proteolytic activity. Exopolysaccharide (EPS) production by the Pediococcus strains during growth in MRS (de Man, Rogosa, and Sharpe) medium was in the range 25-64 mg/l. The susceptibility of 10 different antibiotics against these strains was also tested. All strains were found to be resistant to amoxicillin, gentamicin, and vancomycin. Antimicrobial effects of the Pediococcus spp. on pathogens were also determined by an agar diffusion method. All of the strains were able to inhibit L. monocytogenes. The tolerance of the strains to low pH, their resistance to bile salts of strains, and their abilities to autoaggregate and coaggregate with L. monocytogenes were also evaluated.

Keywords

References

  1. Annuk, H., T. Shchepetova, T. Kullisaar, E. Songisepp, M. Zilmer, and M. Mikelsaar. 2003. Characterization of intestinal lactobacilli as putative probiotic candidates. J. Appl. Microbiol. 94: 403-412. https://doi.org/10.1046/j.1365-2672.2003.01847.x
  2. Arici, M., B. Bilgin, O. Sagdic, and C. Ozdemir. 2004. Some characteristics of Lactobacillus isolates from infant faeces. Food Microbiol. 21: 19-24. https://doi.org/10.1016/S0740-0020(03)00044-3
  3. Aroutcheva, A., D. Gariti, M. Simon, S. Shott, J. Faro, J. A. Simoes, A. Gurguis, and S. Faro. 2001. Defense factors of vaginal lactobacilli. Am. J. Obstet. Gynecol. 185: 375-379. https://doi.org/10.1067/mob.2001.115867
  4. Asahara, T., K. Shimizu, K. Nomoto, T. Hamabata, A. Ozawa, and Y. Takeda. 2004. Probiotic bifidobacteria protect mice from lethal infection with Shiga toxin-producing Escherichia coli O157: H7. Infect. Immun. 72: 2240-2247. https://doi.org/10.1128/IAI.72.4.2240-2247.2004
  5. Aslim, B., Z. N. Yuksekdag, E. Sarikaya, and Y. Beyatli. 2005. Determination of the bacteriocin-like substances produced by some lactic acid bacteria isolated from Turkish dairy products. LWT/Food Sci. Technol. 38: 691-694.
  6. Aslim, B., Y. Beyatli, and Z. N. Yuksekdag. 2006. Productions and monomer compositions of exopolysaccharides by Lactobacillus delbrueckii subsp. bulgaricus and Streptococcus thermophilus strains isolated from traditional home-made yoghurts and raw milk. Int. J. Food Sci. Technol. 41: 973-979. https://doi.org/10.1111/j.1365-2621.2005.01155.x
  7. Aslim, B., D. Onal, and Y. Beyatli. 2007. Factors influencing autoaggregation and aggregation of Lactobacillus delbrueckii subsp. bulgaricus isolated from handmade yogurt. J. Food Protect. 70: 223-227.
  8. Beyatli, Y., B. Aslim, D. Onal, and H. Bozkurt. 2007. Determination of some characteristic properties of lactic acid bacteria isolated from traditional home-made yogurts. Deut. Lebensm. Rundsh. 103: 517-522.
  9. Boonmee, M., N. Leksawasdi, W. Bridge, and P. L. Rogers. 2003. Batch and continuous culture of Lactococcus lactis NZ133: Experimental data and model development. Biochem. Eng. J. 14: 127-135. https://doi.org/10.1016/S1369-703X(02)00171-7
  10. Charteris, W. P., P. M. Kelly, L. Morelli, and J. K. Collins. 1998. Development and application of an in vivo methodology to determine the transit tolerance of potentially probiotic Lactobacillus and Bifidobacterium species in the upper human gastrointestinal tract. J. Appl. Microbiol. 84: 759-768. https://doi.org/10.1046/j.1365-2672.1998.00407.x
  11. Chou, L. S. and B. Weimer. 1999. Isolation and characterization of acid- and bile-tolerant isolates from strains of Lactobacillus acidophilus. J. Dairy Sci. 82: 23-31. https://doi.org/10.3168/jds.S0022-0302(99)75204-5
  12. Citti, J., W. E. Sandine, and P. R. Elliker. 1963. Some observations on the Hull method for measurement of proteolysis in milk. J. Dairy Sci. 46: 337. https://doi.org/10.3168/jds.S0022-0302(63)89042-6
  13. Clinical and Laboratory Standards Institute. 2005. Document M- 100-S9. Performance Standards for Antimicrobial Susceptibility Testing. 12th Informational Supplement. M100-S12 CLSI: Wayne Pennsylvania.
  14. Con, A. H. and H. Y. Gokalp. 2000. Production of bacteriocin-like metabolites by lactic acid cultures isolated from sucuk samples. Meat Sci. 55: 89-96. https://doi.org/10.1016/S0309-1740(99)00129-1
  15. Con, A. H., H. Y. Gokalp, and M. Kaya. 2001. Antagonistic effect on Listeria monocytogenes and L. innocua of a bacteriocin-like metabolite produced by lactic acid bacteria isolated from sucuk. Meat Sci. 59: 437-441. https://doi.org/10.1016/S0309-1740(01)00099-7
  16. Del Re, B., B. Sgorbati, M. Miglioli, and D. Palenzona. 2000. Adhesion, autoaggregation and hydrophobicity of 13 strains of Bifidobacterium longum. Lett. Appl. Microbiol. 31: 438-442. https://doi.org/10.1046/j.1365-2672.2000.00845.x
  17. Demirci, M. and H. Gunduz. 1994. Dairy Technology Handbook. Hasad Press, Turkey. pp. 184.
  18. du Toit, M., C. M. Franz, L. M. Dicks, U. Schillinger, P. Harberer, B. Warlies, F. Ahrens, and W. H. Holzapfel. 1998. Characterization and selection of probiotic lactobacilli for a preliminary minipig feeding trial and their effect on serum cholesterol levels, faeces pH and faeces moisture content. Int. J. Food Microbiol. 40: 93-104. https://doi.org/10.1016/S0168-1605(98)00024-5
  19. Dubois, M., K. A. Gilles, J. K. Hamilton, P. A. Peters, and F. Smith. 1956. Colorimetric method for determination of sugars and related substances. Anal. Chem. 28: 350-356. https://doi.org/10.1021/ac60111a017
  20. Erkkila, S. and E. Petaja. 2000. Screening of commercial meat starter cultures at low pH and in the presence of bile salts for potential probiotic use. Meat Sci. 55: 297-300. https://doi.org/10.1016/S0309-1740(99)00156-4
  21. Erkkila, S., M. Venalainen, S. Hielm, E. Petaja, E. Puolanne, and T. Mattila-Sandholm. 2000. Survival of Escherichia coli O157:H7 in dry sausage fermented by probiotic lactic acid bacteria. J. Sci. Food Agric. 80: 2101-2104. https://doi.org/10.1002/1097-0010(200011)80:14<2101::AID-JSFA756>3.0.CO;2-3
  22. Erkkila, S., M. L. Suihko, S. Eerola, E. Petaja, and T. Mattila-Sandholm. 2001. Dry fermented sausages by Lactobacillus rhamnosus strains. Int. J. Food Microbiol. 64: 205-210. https://doi.org/10.1016/S0168-1605(00)00457-8
  23. Erkkila, S., E. Petaja, S. Eerola, L. Lilleberg, T. Mattila-Sandholm, and M. L. Suihko. 2001. Flavour profiles of dry sausages fermented by selected novel meat starter cultures. Meat Sci. 58: 111-116. https://doi.org/10.1016/S0309-1740(00)00135-2
  24. Frengova, G. I., E. D. Simova, D. M. Beshkova, and Z. I. Simov. 2000. Production and monomer composition of exopolysaccharides by yogurt starter cultures. Can. J. Microbiol. 46: 1123-1127. https://doi.org/10.1139/w00-103
  25. Gill, H. S. 1998. Stimulation of the system by lactic cultures. Int. Dairy J. 8: 535-544. https://doi.org/10.1016/S0958-6946(98)00074-0
  26. Gotcheva, V., E. Hristozova, T. Hristozova, M. Guo, Z. Roshkova, and A. Angelov. 2002. Assessment of potential probiotic properties of lactic acid bacteria and yeast strains. Food Biotechnol. 16: 211-225. https://doi.org/10.1081/FBT-120016668
  27. Harrigan, W. and M. McCance. 1990. Laboratory Methods in Food and Dairy Microbiology, 8th Ed. Academic Press, London, U.K.
  28. Helander, I. M., A. von Wright, and T. M. Mattila-Sandholm. 1997. Potential of lactic acid bacteria and novel antimicrobials against Gram-negative bacteria. Trends Food Sci. Technol. 8: 146-150. https://doi.org/10.1016/S0924-2244(97)01030-3
  29. Herreros, M. A., H. Sandoval, L. Gonzalez, J. M. Csatro, J. M. Fresno, and M. E. Tornadijo. 2005. Antimicrobial activity and antibiotic resistance of lactic acid bacteria isolated from Armada cheese (a Spanish goats' milk cheese). Food Microbiol. 22: 455-459. https://doi.org/10.1016/j.fm.2004.11.007
  30. Huang, H. Y., S. Y. Huang, P. Y. Chen, V. A. E. King, Y. P. Lin, and J. H. Tsen. 2007. Basic characteristics of Sporolactobacillus inulinus BCRC 14647 for potential probiotic properties. Curr. Microbiol. 54: 396-404. https://doi.org/10.1007/s00284-006-0496-5
  31. Hummel, A. S., C. Hertel, W. H. Holzapfel, and C. M. A. P. Franz. 2007. Antibiotic resistances of starter and probiotic strains of lactic acid bacteria. Appl. Environ. Microbiol. 73: 730-739. https://doi.org/10.1128/AEM.02105-06
  32. Incze, K. 1998. Dry fermented sausages. Meat Sci. 49: 169-177. https://doi.org/10.1016/S0309-1740(98)90046-8
  33. Kim, W., J. Ren, and W. Dunn. 1999. Differentiation of Lactococcus lactis subspecies lactis and subspecies cremoris strains by their adaptive response to stress. FEMS Microbiol. Lett. 171: 57-65. https://doi.org/10.1111/j.1574-6968.1999.tb13412.x
  34. Kos, B., J. Suskoviae, S. Vukoviae, M. Simpraga, J. Frece, and S. Matosiae. 2003. Adhesion and aggregation ability of probiotic strain Lactobacillus acidophilus M92. J. Appl. Microbiol. 94: 981-987. https://doi.org/10.1046/j.1365-2672.2003.01915.x
  35. Kumar, C. G. and S. K. Anand. 1998. Significance of microbial biofilms in food industry: A review. Int. J. Food Microbiol. 42: 9-27. https://doi.org/10.1016/S0168-1605(98)00060-9
  36. Leroy, F., J. Verluyten, and L. De Vuyst. 2006. Functional meat starter cultures for improved sausage fermentation. Int. J. Food Microbiol. 106: 270-285. https://doi.org/10.1016/j.ijfoodmicro.2005.06.027
  37. Moreira, M., A. Bevilacqua, and G. Antoni. 2003. Manufacture of Quartirolo cheese using exopolysaccharide-producing starter cultures. Milchwissenchaft 58: 301-304.
  38. Ouwehand, A. C., S. Salminen, and E. Isolauri. 2002. Probiotics: An overview of benefical effects. Antonie Von Leeuwenhoek 82: 279-289. https://doi.org/10.1023/A:1020620607611
  39. Pailin, T., D. H. Kang, K. Schmidt, and D. Y. C. Fung. 2001. Detection of extracellular bound proteinase in EPS producing lactic acid bacteria cultures on milk agar. Lett. Appl. Microbiol. 33: 45-49. https://doi.org/10.1046/j.1472-765X.2001.00954.x
  40. Patrick, W. A. and H. B. Wagner. 1949. Determination of hydrogen peroxide in small concentrations. Anal. Chem. 21: 1279-1280. https://doi.org/10.1021/ac60034a038
  41. Pennacchia, C., D. Ercolini, G. Blaiotta, O. Pepe, G. Mauriello, and F. Villani. 2004. Selection of Lactobacillus strains from fermented sausages for their potential use as probiotic. Meat Sci. 67: 309-317. https://doi.org/10.1016/j.meatsci.2003.11.003
  42. Pepe, O., F. Villani, D. Oliviero, T. Greco, and S. Coppala. 2003. Effects of proteolytic starter cultures as leavening agents of pizza dough. Int. J. Food Microbiol. 84: 319-326. https://doi.org/10.1016/S0168-1605(02)00473-7
  43. Reinheimer, J. A., M. R. Demkow, and M. C. Condioti. 1990. Inhibition of coliform bacteria by lactic cultures. Aust. J. Dairy Technol. May: 5-9.
  44. Rojo-Bezares, B., Y. Saenz, M. Zarazaga, C. Torres, and F. Ruiz-Larrea. 2007. Antimicrobial activity of nisin against Oenococcus oeni and other wine bacteria. Int. J. Food Microbiol. 116: 32-36. https://doi.org/10.1016/j.ijfoodmicro.2006.12.020
  45. Salazar-Lindo, E., P. Miranda-Langschwager, M. Campos-Sanchez, E. Chea-Woo, and R. B. Sack. 2004. Lactobacillus casei strain GG in the treatment of infants with acute watery diarrhea: A randomized, double-blind, placebo controlled clinical trial. BMC Pediatr. 4: 18-26. https://doi.org/10.1186/1471-2431-4-18
  46. Temmerman, R., B. Pot, G. Huys, and J. Swings. 2003. Identification and antibiotic susceptibility of bacterial isolates from probiotic products. Int. J. Food Microbiol. 81: 1-10. https://doi.org/10.1016/S0168-1605(02)00162-9
  47. Toksoy, A. 1996. A study of some metabolic and antimicrobial activities of Lactobacillus plantarum and Pediococcus pentosaceus strains. Ph. D. Thesis. Gazi University Institute of Science and Technology. pp. 118.
  48. Torino, M. I., M. P. Taranto, F. Sesma, and G. Font de Valdez. 2001. Heterofermentative pattern and exopolysaccharide production by Lactobacillus helveticus 15807 in response to environmental pH. J. Appl. Microbiol. 91: 846-852. https://doi.org/10.1046/j.1365-2672.2001.01450.x
  49. Ekmekci, H., B. Aslim, and D. Onal Darilmaz. 2009. Some factors affecting the autoaggregation ability of vaginal Lactobacilli isolated from Turkish women. Arch. Biol. Sci. 61: 407-412. https://doi.org/10.2298/ABS0903407E
  50. Villar, M., A. P. de Ruiz Holgado, J. Sanchez, R. E. Trucco, and G. Oliver. 1985. Isolation and characterization of Pediococcus halophilus from salted anchovies (Engraulis anchoita). Appl. Environ. Microbiol. 49: 664-666.
  51. Walling, E., M. Dols-Lafargue, and A. Lonvaud-Funel. 2005. Glucose fermentation kinetics and exopolysaccharide production by ropy Pediococcus damnosus IOEB8801. Food Microbiol. 22: 71-78. https://doi.org/10.1016/j.fm.2004.04.003
  52. Wood, B. J. B. and W. H. Holzapfel. 1995. The Genera of Lactic Acid Bacteria, Vol. 2. Blackie Academic and Professional, Glasgow.
  53. Xanthopoulos, V., E. Litopoulou-Tzanetaki, and N. Tzanetakis. 2000. Characterization of Lactobacillus isolates from infant faeces as dietary adjuncts. Food Microbiol. 17: 205-215. https://doi.org/10.1006/fmic.1999.0300
  54. Yaman, A., H. Y. Gokalp, and A. H. Con. 1998. Some characteristics of lactic acid bacteria present in commercial sucuk samples. Meat Sci. 49: 387-397. https://doi.org/10.1016/S0309-1740(98)00004-7
  55. Yuksekdag, Z. N., Y. Beyatli, and B. Aslim. 2004. Metabolic activities Lactobacillus spp. strains isolated from kefir. Nahrung/Food 48: 218-220. https://doi.org/10.1002/food.200300414
  56. Yuksekdag, Z. N., Y. Beyatli, and B. Aslim. 2004. Determination of some characteristics coccoid forms of lactic acid bacteria isolated from Turkish kefirs with natural probiotic. LWT/Food Sci. Technol. 37: 663-667.

Cited by

  1. 백합(Meretrix meretrix)식해에서 분리한 Pediococcus pentosaceus SH-10의 생균제적 특성 vol.44, pp.6, 2010, https://doi.org/10.5657/kfas.2011.0605
  2. Evaluation of the Probiotic Potential of Bacillus polyfermenticus CJ6 Isolated from Meju, a Korean Soybean Fermentation Starter vol.22, pp.11, 2010, https://doi.org/10.4014/jmb.1205.05049
  3. In vitro study of potentially probiotic lactic acid bacteria strains isolated from kimchi vol.63, pp.4, 2010, https://doi.org/10.1007/s13213-013-0599-8
  4. Selection of γ‐aminobutyric acid‐producing lactic acid bacteria and their potential as probiotics for use as starter cultures in Thai fermented sausages (Nham) vol.48, pp.7, 2013, https://doi.org/10.1111/ijfs.12098
  5. Yeasts from autochthonal cheese starters: technological and functional properties vol.115, pp.2, 2010, https://doi.org/10.1111/jam.12228
  6. 김치 종류에 따른 유산균의 생물학적 및 기능적 특성 vol.42, pp.1, 2010, https://doi.org/10.3746/jkfn.2013.42.1.089
  7. Probiotic Potential of Pediococcus pentosaceus CRAG3: A New Isolate from Fermented Cucumber vol.6, pp.1, 2010, https://doi.org/10.1007/s12602-013-9149-8
  8. Dairy propionibacterium strains with potential as biopreservatives against foodborne pathogens and their tolerance-resistance properties vol.238, pp.1, 2014, https://doi.org/10.1007/s00217-013-2066-y
  9. In vitro evaluation of the suitability potential probiotic of lactobacilli isolates from the gastrointestinal tract of chicken vol.239, pp.2, 2014, https://doi.org/10.1007/s00217-014-2224-x
  10. Sugar-coated: exopolysaccharide producing lactic acid bacteria for food and human health applications vol.6, pp.3, 2010, https://doi.org/10.1039/c4fo00529e
  11. Determination of Antibiotic Resistance and Biogenic Amine Production of Lactic Acid Bacteria Isolated from Fermented Turkish Sausage (Sucuk) vol.35, pp.2, 2015, https://doi.org/10.1111/jfs.12177
  12. In vitro study of probiotic properties of Lactobacillus plantarum F22 isolated from chhang – A traditional fermented beverage of Himachal Pradesh, India vol.14, pp.1, 2010, https://doi.org/10.1016/j.jgeb.2016.08.001
  13. Selection of indigenous Lactobacillus paracasei CD4 and Lactobacillus gastricus BTM 7 as probiotic: assessment of traits combined with principal component analysis vol.122, pp.5, 2010, https://doi.org/10.1111/jam.13426
  14. Antibiotic susceptibility profile of Pediococcus spp. from diverse sources vol.8, pp.12, 2010, https://doi.org/10.1007/s13205-018-1514-6
  15. Antibiotic resistance in vancomycin‐resistant lactic acid bacteria (VRLAB) isolated from foods of animal origin vol.44, pp.6, 2010, https://doi.org/10.1111/jfpp.14468
  16. Characterization of Lactobacillus plantarum strains isolated from Turkish pastırma and possibility to use of food industry vol.40, pp.2, 2020, https://doi.org/10.1590/fst.05819
  17. 잠재적 사료첨가제로서 Pediococcus acidilactici SRCM102607의 생균제 특성 및 면역활성 효과 vol.30, pp.10, 2010, https://doi.org/10.5352/jls.2020.30.10.896
  18. Autochthonous Probiotics in Meat Products: Selection, Identification, and Their Use as Starter Culture vol.8, pp.11, 2010, https://doi.org/10.3390/microorganisms8111833
  19. Evaluation of GABA Production and Probiotic Activities of Enterococcus faecium BS5 vol.13, pp.4, 2010, https://doi.org/10.1007/s12602-021-09759-7
  20. Probiotic properties of Lactobacillus casei – MYSRD 108 and Lactobacillus plantarum-MYSRD 71 with potential antimicrobial activity against Salmonella paratyphi vol.32, pp.None, 2021, https://doi.org/10.1016/j.btre.2021.e00672
  21. Pediococcus pentosaceus, a future additive or probiotic candidate vol.20, pp.1, 2021, https://doi.org/10.1186/s12934-021-01537-y