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Bacteriocinogenic bacteria isolated from Civil, Kashar and White cheeses in Erzurum, Turkey

Year 2019, Volume: 66 Issue: 2, 147 - 153, 05.04.2019

Hayrunnisa Özlü , Mustafa Atasever

https://doi.org/10.33988/auvfd.547483

Abstract

This study was carried out in order to identify the bacteriocinogenic lactic acid bacteria (LAB) isolated from civil, kashar and white cheeses produced by traditional methods in Erzurum, Turkey. LAB were isolated from 80 samples of cheese collected from the markets of Erzurum. Antimicrobial activities of the isolates were determined using agar spot and well diffusion methods. LAB that showing antimicrobial activity were characterized phenotypically and genotypically, and the bacteriocin-producing strains were determined. The susceptibilities of bacteriocins to different temperatures, pH and enzymes were tested. While 48.29% of the 381 LAB isolated from cheese samples had antimicrobial activity, only 4.35% of them were determined producing bacteriocin. While 168 of 184 isolates which were showing antimicrobial activity were identified by phenotypical methods at a genus level, and 11 of were at a species level, 135 of 184 isolates were identified by genotypical methods at a genus level, and 26 of were at a species level. Lb. plantarum (24.36%) and Lb. brevis (23.08%) in lactobacilli, E. faecium (38.89%) and E. durans (20.37%) in enterococci, and Lc. lactis subsp. lactis (100%) in lactococci were identified as the dominant species. All bacteriocin producing exhibited antimicrobial activity against Micrococcus luteus. It has been determined that bacteriocin producing Lc. lactis subsp. lactis and Lb. pentosus strains have inhibition impact on Staphylococcus aureus and Listeria monocytogenes. It has been concluded that the bacteriocin-producing isolates, due to not losing their activities in a wide range of pH and different temperature-time values, could be used as a bio-protective culture in food production and storage.

Keywords

Bacteriocin Civil cheese Kashar cheese VITEK 2 16S rDNA

References

  • Aymerich M, Garriga M, Monfort J, et al. (2000): Bacteriocin-producing lactobacilli in Spanish-style fermented sausages: characterization of bacteriocins. Food Microbiol, 17, 33-45.
  • Badis A, Guetarni D, Moussa Boudjema B, et al. (2004): Identification and technological properties of lactic acid bacteria isolated from raw goat milk of four Algerian races. Food Microbiol, 21, 579-588.
  • Beasley SS, Saris E (2004): Nisin-producing Lactococcus lactis strains isolated from human milk. Appl Environ Microbiol, 70, 5051-3.
  • Ben Omar N, Abriouel H, Lucas R, et al. (2006): Isolation of bacteriocinogenic Lactobacillus plantarum strains from ben saalga, a traditional fermented gruel from Burkina Faso. Int J Food Microbiol, 112, 44-50.
  • Beresford TP, Fitzsimons NA, Brennan NL, et al. (2001): Recent advances in cheese microbiology. Int Dairy J, 11, 259-274.
  • Bintsis T (2018): Lactic acid bacteria: Their applications in foods. J Bacteriol Mycol, 6 (2), 89–94.
  • Bintsis T, Papademas P (2002): Microbiological quality of white-brined cheeses: A review. Int J Dairy Technol, 55, 113-120.
  • Bonade A, Murelli F, Vescovo M, et al. (2001): Partial characterization of a bacteriocin produced by Lactobacillus helveticus. Lett Appl Microbiol, 33, 153-8.
  • Caridi A (2003): Identification and first characterization of lactic acid bacteria isolated from the artisanal ovine cheese Pecorino del Poro. Int J Dairy Technol, 56, 105-110.
  • Çayır Üstündağ H, Yalçın H (2017): Bacteriocins and used in foods. MAKÜ Sag Bil Enst Derg, 5 (1), 53-65.
  • Çon AH, Gökalp HY (2000): Laktik asit bakterilerinin antimikrobiyal metabolitleri ve etki şekilleri. Türk Mikrobiyol Cem Derg, 30, 180-190.
  • Deasy BM, Rea MC, Fitzgerald GF, et al. (2000): A rapid PCR based method to distinguish between Lactococcus and Enterococcus. Syst Appl Microbiol, 23, 510-522.
  • Dinçer E, Kıvanç M, Karaca H (2010): Biyokoruyucu olarak laktik asit bakterileri ve bakteriyosinler. Gıda, 35: 55-62.
  • Drosinos EH, Paramithiotis S, Kolovos G, et al. (2007): Phenotypic and technological diversity of lactic acid bacteria and staphylococci isolated from traditionally fermented sausages in southern Greece. Food Microbiol, 24, 260-270.
  • Edwards U, Rogall T, Blocker H, et al. (1989): Isolation and direct complete nucleotide determination of entire genes. Characterization of a gene coding for 16S ribosomal RNA. Nucleic Acids Res, 17, 7843-53.
  • Englen MD, Kelley LC (2000): A rapid DNA isolation procedure for the identification of Campylobacter jejuni by the polymerase chain reaction. Lett Appl Microbiol, 31, 421-426.
  • Franz CMAP, Du Toit M, von Holy A, et al. (1997): Production of nisin-like bacteriocins by Lactococcus lactis strains isolated from vegetables. J Basic Microb, 37, 187- 196.
  • González L, Sandoval H, Sacristán N, et al. (2007): Identification of lactic acid bacteria isolated from Genestoso cheese throughout ripening and study of their antimicrobial activity. Food Control, 18, 716-722.
  • Gunay-Esiyok O, Akcelik N, Akcelik M (2014): Identification of genomic heterogeneity among Lactococcus lactis strains by plasmid profiling, PFGE and 16S rDNA sequence analysis. Pol J Microbiol, 63, 157-66.
  • Gürsoy O, Kınık Ö (2006): Peynir teknolojisinde enterokoklar –I: Biyokimyasal özellikleri ve peynir teknolojisindeki önemleri. Ege Üniv Ziraat Fak Derg, 43, 79-90.
  • Hernández D, Cardell E, Zárate V (2005): Antimicrobial activity of lactic acid bacteria isolated from Tenerife cheese: initial characterization of plantaricin TF711, a bacteriocin-like substance produced by Lactobacillus plantarum TF711. J Appl Microbiol, 99, 77-84.
  • Kandler O, Weiss N (1986): Regular, nonsporing Gram positive rods. Genus Lactobacillus. 1208–1234. In: PHA Sneath, NS Mair, ME Sharpe, JG Holt (Ed), Bergey’s Manual of Systematic Bacteriology. Williams and Wilkins, Baltimore.
  • Kántor A, Kluz M, Puchalski C, et al. (2016): Identification of lactic acid bacteria isolated from wine using real-time PCR. J Environ Sci Heal B, 51(1), 52-56.
  • Kıran F, Osmanoğlu Ö (2011). Laktik asit bakterilerinin (LAB) identifikasyonunda/tiplendirme-sinde kullanılan moleküler yöntemler. Erciyes Üniv Fen Bil Enst Derg, 27, 62-74.
  • Kunene NF, Geornaras I, von Holy A, et al. (2000). Characterization and determination of origin of lactic acid bacteria from a sorghum-based fermented weaning food by analysis of soluble proteins and amplified fragment length polymorphism fingerprinting. Appl Environ Microb, 66, 1084-1092.
  • Morandi S, Cremonesi P, Povolo M, et al. (2012). Enterococcus lactis sp. nov., from Italian raw milk cheeses. Int J Syst Evol Micr, 62, 1992-1996.
  • Papamanoli E, Tzanetakis N, Litopoulou-Tzanetaki E, et al. (2003): Characterization of lactic acid bacteria isolated from a Greek dry-fermented sausage in respect of their technological and probiotic properties. Meat Sci, 65, 859-867.
  • Rodriguez E, Gonzalez B, Gaya P, et al. (2000): Diversity of bacteriocins produced by lactic acid bacteria isolated from raw milk. Int Dairy J, 10, 7-15.
  • Salminen J-P, Roslin T, Karonen M, et al. (2004): Seasonal variation in the content of hydrolyzable tannins, flavonoid glycosides, and proanthocyanidins in oak leaves. J Chem Ecol, 30, 1693-1711.
  • Sanchez I, Palop L, Ballesteros C (2000): Biochemical characterization of lactic acid bacteria isolated from spontaneous fermentation of 'Almagro' eggplants. Int J Food Microbiol, 59, 9-17.
  • Schillinger U, Lucke FK (1989): Antibacterial activity of Lactobacillus-Sake isolated from meat. Appl Environ Microbiol, 55, 1901-1906.
  • Simova ED, Beshkova DB, Dimitrov ZP (2009). Characterization and antimicrobial spectrum of bacteriocins produced by lactic acid bacteria isolated from traditional Bulgarian dairy products. J Appl Microbiol, 106, 692-701.
  • Temmerman R, Huys G, Swings J (2004): Identification of lactic acid bacteria: culture-dependent and culture- independent methods. Trends Food Sci Technol, 15, 348- 359.
  • Tuma S, Kucerova K, Plockova M (2008). Isolation of anticlostridially active Lactobacilli from semi-hard cheese. Czech J Food Sci, 26, 324-332.
  • Tuncer Y (2009): Phenotypic and Genotypic Characterization of Nisin-Producing Lactococcus Lactis Subsp Lactis Yb23 Isolated from Raw Milk in Turkey. Biotechnol Biotec Eq, 23, 1504-1508.
  • Turantaş F (2003): Fermente gıdalar. 447-457. In: A Ünlütürk, F Turantaş (Ed.), Gıda Mikrobiyolojisi. Meta Basım Matbaacılık Hizmetleri, İzmir.
  • van Belkum MJ, Hayema BJ, Geis A, et al. (1989): Cloning of two bacteriocin genes from a lactococcal bacteriocin plasmid. Appl Environ Microb, 55, 1187-1191.
  • Yang E, Fan L, Jiang Y, et al. (2012): Antimicrobial activity of bacteriocin-producing lactic acid bacteria isolated from cheeses and yogurts. AMB Express, 2, 1-12.

Erzurum ilindeki Civil, Kaşar ve Beyaz peynirlerden izole edilen bakteriyosinogenik bakteriler

Year 2019, Volume: 66 Issue: 2, 147 - 153, 05.04.2019

Hayrunnisa Özlü , Mustafa Atasever

https://doi.org/10.33988/auvfd.547483

Abstract

Bu çalışma, Erzurum ilinde geleneksel yöntemlerle üretilen beyaz, civil ve kaşar peynirlerinden izole edilen bakteriyosinogenik laktik asit bakterilerinin (LAB) belirlemesi amacıyla yapıldı. Erzurum piyasasından toplanan 80 peynir örneğinden LAB izole edildi. İzolatların antimikrobiyal aktiviteleri agar spot ve kuyu difüzyon yöntemleri kullanılarak belirlendi. Antimikrobiyel aktivite gösteren LAB fenotipik ve genotipik olarak tanımlandı ve bakteriyosin üreten suşlar tespit edildi. Bakteriyosinlerin farklı sıcaklık, pH ve enzimlere karşı duyarlılıkları test edildi. Peynir örneklerinden izole edilen 381 izolatın %48.29’u antimikrobiyal etkiye sahipken bunlardan yanlızca %4.35’inin bakteriyosin ürettiği tespit edildi. Antimikrobiyal aktivite gösteren 184 izolattan 168 tanesi cins ve 11 tanesi tür düzeyinde fenotipik yöntemlerle tanımlanırken, 184 izolattan 135 tanesi cins ve 26 tanesi tür düzeyinde genotipik yöntemle belirlenmiştir. Laktobasillerde Lb. plantarum (%24.36) ve Lb. brevis (%23.08), enterokoklarda E. faecium (%38.89) ve E. durans (%20.37), laktokoklarda ise Lc. lactis subsp. lactis (%100) baskın türler olarak tespit edildi. Bakteriyosin üreten izolatların tamamı M. luteus’a karşı antimikrobiyel aktivite gösterdi. Bakteriyosin üreten Lc. lactis subsp. lactis ve Lb. pentosus suşlarının S. aureus ve L. monocytogenes üzerine inhibe edici etkisinin olduğu belirlendi. Bakteriyosin üreten izolatların geniş bir pH aralığında ve farklı ısı-zaman değerlerinde aktivitelerini kaybetmemelerinden dolayı gıda üretimi ve muhafazasında biyokoruyucu kültür olarak kullanılabileceği sonucuna varıldı.

Keywords

Bakteriyosin Civil peynir Kaşar peyniri VITEK 2 16S rDNA

References

  • Aymerich M, Garriga M, Monfort J, et al. (2000): Bacteriocin-producing lactobacilli in Spanish-style fermented sausages: characterization of bacteriocins. Food Microbiol, 17, 33-45.
  • Badis A, Guetarni D, Moussa Boudjema B, et al. (2004): Identification and technological properties of lactic acid bacteria isolated from raw goat milk of four Algerian races. Food Microbiol, 21, 579-588.
  • Beasley SS, Saris E (2004): Nisin-producing Lactococcus lactis strains isolated from human milk. Appl Environ Microbiol, 70, 5051-3.
  • Ben Omar N, Abriouel H, Lucas R, et al. (2006): Isolation of bacteriocinogenic Lactobacillus plantarum strains from ben saalga, a traditional fermented gruel from Burkina Faso. Int J Food Microbiol, 112, 44-50.
  • Beresford TP, Fitzsimons NA, Brennan NL, et al. (2001): Recent advances in cheese microbiology. Int Dairy J, 11, 259-274.
  • Bintsis T (2018): Lactic acid bacteria: Their applications in foods. J Bacteriol Mycol, 6 (2), 89–94.
  • Bintsis T, Papademas P (2002): Microbiological quality of white-brined cheeses: A review. Int J Dairy Technol, 55, 113-120.
  • Bonade A, Murelli F, Vescovo M, et al. (2001): Partial characterization of a bacteriocin produced by Lactobacillus helveticus. Lett Appl Microbiol, 33, 153-8.
  • Caridi A (2003): Identification and first characterization of lactic acid bacteria isolated from the artisanal ovine cheese Pecorino del Poro. Int J Dairy Technol, 56, 105-110.
  • Çayır Üstündağ H, Yalçın H (2017): Bacteriocins and used in foods. MAKÜ Sag Bil Enst Derg, 5 (1), 53-65.
  • Çon AH, Gökalp HY (2000): Laktik asit bakterilerinin antimikrobiyal metabolitleri ve etki şekilleri. Türk Mikrobiyol Cem Derg, 30, 180-190.
  • Deasy BM, Rea MC, Fitzgerald GF, et al. (2000): A rapid PCR based method to distinguish between Lactococcus and Enterococcus. Syst Appl Microbiol, 23, 510-522.
  • Dinçer E, Kıvanç M, Karaca H (2010): Biyokoruyucu olarak laktik asit bakterileri ve bakteriyosinler. Gıda, 35: 55-62.
  • Drosinos EH, Paramithiotis S, Kolovos G, et al. (2007): Phenotypic and technological diversity of lactic acid bacteria and staphylococci isolated from traditionally fermented sausages in southern Greece. Food Microbiol, 24, 260-270.
  • Edwards U, Rogall T, Blocker H, et al. (1989): Isolation and direct complete nucleotide determination of entire genes. Characterization of a gene coding for 16S ribosomal RNA. Nucleic Acids Res, 17, 7843-53.
  • Englen MD, Kelley LC (2000): A rapid DNA isolation procedure for the identification of Campylobacter jejuni by the polymerase chain reaction. Lett Appl Microbiol, 31, 421-426.
  • Franz CMAP, Du Toit M, von Holy A, et al. (1997): Production of nisin-like bacteriocins by Lactococcus lactis strains isolated from vegetables. J Basic Microb, 37, 187- 196.
  • González L, Sandoval H, Sacristán N, et al. (2007): Identification of lactic acid bacteria isolated from Genestoso cheese throughout ripening and study of their antimicrobial activity. Food Control, 18, 716-722.
  • Gunay-Esiyok O, Akcelik N, Akcelik M (2014): Identification of genomic heterogeneity among Lactococcus lactis strains by plasmid profiling, PFGE and 16S rDNA sequence analysis. Pol J Microbiol, 63, 157-66.
  • Gürsoy O, Kınık Ö (2006): Peynir teknolojisinde enterokoklar –I: Biyokimyasal özellikleri ve peynir teknolojisindeki önemleri. Ege Üniv Ziraat Fak Derg, 43, 79-90.
  • Hernández D, Cardell E, Zárate V (2005): Antimicrobial activity of lactic acid bacteria isolated from Tenerife cheese: initial characterization of plantaricin TF711, a bacteriocin-like substance produced by Lactobacillus plantarum TF711. J Appl Microbiol, 99, 77-84.
  • Kandler O, Weiss N (1986): Regular, nonsporing Gram positive rods. Genus Lactobacillus. 1208–1234. In: PHA Sneath, NS Mair, ME Sharpe, JG Holt (Ed), Bergey’s Manual of Systematic Bacteriology. Williams and Wilkins, Baltimore.
  • Kántor A, Kluz M, Puchalski C, et al. (2016): Identification of lactic acid bacteria isolated from wine using real-time PCR. J Environ Sci Heal B, 51(1), 52-56.
  • Kıran F, Osmanoğlu Ö (2011). Laktik asit bakterilerinin (LAB) identifikasyonunda/tiplendirme-sinde kullanılan moleküler yöntemler. Erciyes Üniv Fen Bil Enst Derg, 27, 62-74.
  • Kunene NF, Geornaras I, von Holy A, et al. (2000). Characterization and determination of origin of lactic acid bacteria from a sorghum-based fermented weaning food by analysis of soluble proteins and amplified fragment length polymorphism fingerprinting. Appl Environ Microb, 66, 1084-1092.
  • Morandi S, Cremonesi P, Povolo M, et al. (2012). Enterococcus lactis sp. nov., from Italian raw milk cheeses. Int J Syst Evol Micr, 62, 1992-1996.
  • Papamanoli E, Tzanetakis N, Litopoulou-Tzanetaki E, et al. (2003): Characterization of lactic acid bacteria isolated from a Greek dry-fermented sausage in respect of their technological and probiotic properties. Meat Sci, 65, 859-867.
  • Rodriguez E, Gonzalez B, Gaya P, et al. (2000): Diversity of bacteriocins produced by lactic acid bacteria isolated from raw milk. Int Dairy J, 10, 7-15.
  • Salminen J-P, Roslin T, Karonen M, et al. (2004): Seasonal variation in the content of hydrolyzable tannins, flavonoid glycosides, and proanthocyanidins in oak leaves. J Chem Ecol, 30, 1693-1711.
  • Sanchez I, Palop L, Ballesteros C (2000): Biochemical characterization of lactic acid bacteria isolated from spontaneous fermentation of 'Almagro' eggplants. Int J Food Microbiol, 59, 9-17.
  • Schillinger U, Lucke FK (1989): Antibacterial activity of Lactobacillus-Sake isolated from meat. Appl Environ Microbiol, 55, 1901-1906.
  • Simova ED, Beshkova DB, Dimitrov ZP (2009). Characterization and antimicrobial spectrum of bacteriocins produced by lactic acid bacteria isolated from traditional Bulgarian dairy products. J Appl Microbiol, 106, 692-701.
  • Temmerman R, Huys G, Swings J (2004): Identification of lactic acid bacteria: culture-dependent and culture- independent methods. Trends Food Sci Technol, 15, 348- 359.
  • Tuma S, Kucerova K, Plockova M (2008). Isolation of anticlostridially active Lactobacilli from semi-hard cheese. Czech J Food Sci, 26, 324-332.
  • Tuncer Y (2009): Phenotypic and Genotypic Characterization of Nisin-Producing Lactococcus Lactis Subsp Lactis Yb23 Isolated from Raw Milk in Turkey. Biotechnol Biotec Eq, 23, 1504-1508.
  • Turantaş F (2003): Fermente gıdalar. 447-457. In: A Ünlütürk, F Turantaş (Ed.), Gıda Mikrobiyolojisi. Meta Basım Matbaacılık Hizmetleri, İzmir.
  • van Belkum MJ, Hayema BJ, Geis A, et al. (1989): Cloning of two bacteriocin genes from a lactococcal bacteriocin plasmid. Appl Environ Microb, 55, 1187-1191.
  • Yang E, Fan L, Jiang Y, et al. (2012): Antimicrobial activity of bacteriocin-producing lactic acid bacteria isolated from cheeses and yogurts. AMB Express, 2, 1-12.
There are 38 citations in total.

Details

Primary Language English
Subjects Veterinary Surgery
Journal Section Research Article
Authors

Hayrunnisa Özlü

Mustafa Atasever

Publication Date April 5, 2019
Published in Issue Year 2019Volume: 66 Issue: 2

Cite

APA Özlü, H., & Atasever, M. (2019). Bacteriocinogenic bacteria isolated from Civil, Kashar and White cheeses in Erzurum, Turkey. Ankara Üniversitesi Veteriner Fakültesi Dergisi, 66(2), 147-153. https://doi.org/10.33988/auvfd.547483
AMA Özlü H, Atasever M. Bacteriocinogenic bacteria isolated from Civil, Kashar and White cheeses in Erzurum, Turkey. Ankara Univ Vet Fak Derg. April 2019;66(2):147-153. doi:10.33988/auvfd.547483
Chicago Özlü, Hayrunnisa, and Mustafa Atasever. “Bacteriocinogenic Bacteria Isolated from Civil, Kashar and White Cheeses in Erzurum, Turkey”. Ankara Üniversitesi Veteriner Fakültesi Dergisi 66, no. 2 (April 2019): 147-53. https://doi.org/10.33988/auvfd.547483.
EndNote Özlü H, Atasever M (April 1, 2019) Bacteriocinogenic bacteria isolated from Civil, Kashar and White cheeses in Erzurum, Turkey. Ankara Üniversitesi Veteriner Fakültesi Dergisi 66 2 147–153.
IEEE H. Özlü and M. Atasever, “Bacteriocinogenic bacteria isolated from Civil, Kashar and White cheeses in Erzurum, Turkey”, Ankara Univ Vet Fak Derg, vol. 66, no. 2, pp. 147–153, 2019, doi: 10.33988/auvfd.547483.
ISNAD Özlü, Hayrunnisa - Atasever, Mustafa. “Bacteriocinogenic Bacteria Isolated from Civil, Kashar and White Cheeses in Erzurum, Turkey”. Ankara Üniversitesi Veteriner Fakültesi Dergisi 66/2 (April 2019), 147-153. https://doi.org/10.33988/auvfd.547483.
JAMA Özlü H, Atasever M. Bacteriocinogenic bacteria isolated from Civil, Kashar and White cheeses in Erzurum, Turkey. Ankara Univ Vet Fak Derg. 2019;66:147–153.
MLA Özlü, Hayrunnisa and Mustafa Atasever. “Bacteriocinogenic Bacteria Isolated from Civil, Kashar and White Cheeses in Erzurum, Turkey”. Ankara Üniversitesi Veteriner Fakültesi Dergisi, vol. 66, no. 2, 2019, pp. 147-53, doi:10.33988/auvfd.547483.
Vancouver Özlü H, Atasever M. Bacteriocinogenic bacteria isolated from Civil, Kashar and White cheeses in Erzurum, Turkey. Ankara Univ Vet Fak Derg. 2019;66(2):147-53.