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Mycobiota of Konya mold-ripened (Kuflu) Tulum cheese and the diversity of Penicillium roqueforti isolates

Year 2021, Volume: 68 Issue: 4, 349 - 354, 27.09.2021
https://doi.org/10.33988/auvfd.778788

Abstract

Konya Kuflu Tulum cheese is a well-known variety of Turkish mold-ripened cheeses produced by cutting the mature Tulum cheese into pieces to allow the filamentous fungi to grow on its surface in the cool and humid atmosphere in cellars or caves. The aim of the present study was to determine the fungal flora of Kuflu cheese using 54 filamentous fungi and 8 yeasts that were isolated from 26 cheese samples. Internal transcribed spacer (ITS) sequencing indicated that 53 of the mold isolates were Penicillium roqueforti and 1 was Cladosporium cladosporioides. The yeasts were identified as Pichia membranifaciens, Candida zeylanoides, Debaryomyces hansenii, and Geotrichum candidum. Morphological examination of the P. roqueforti isolates on various media revealed similar phenotypes among all but two isolates; however, (GTG)5 fingerprinting analysis indicated that the isolated P. roqueforti strains were highly similar in all but one case, which displayed a different pattern. To our knowledge, this study represents the first to conduct molecular methods for identification of fungi associated with Konya Kuflu Tulum cheese. In addition, the morphological and genetic diversities of the Turkey-originated P. roqueforti isolates are presented. 

Supporting Institution

The Scientific and Technological Research Council of Turkey (TUBITAK)

Project Number

Grant no. 119O314

Thanks

This study is produced from the master’s thesis of Meryem Seri and part of the work has been presented in the 2nd International Eurasian Mycology Congress (Konya, Turkey, 2019) and 1st International / 11th National Food Engineering Congress (Konya, Turkey, 2019) as poster presentation.

References

  • Álvarez-Martín P, Flórez AB, López-Díaz TM, et al (2007): Phenotypic and molecular identification of yeast species associated with Spanish blue-veined Cabrales cheese. Int Dairy J, 17, 961-967.
  • Albenzio M, Corbo M, Rehman S, et al (2001): Microbiological and biochemical characteristics of Canestrato Pugliese cheese made from raw milk, pasteurized milk or by heating the curd in hot whey. Int J Food Microbiol, 67, 35-48.
  • Belén Flórez A, Álvarez-Martín P, López-Díaz TM, et al (2007): Morphotypic and molecular identification of filamentous fungi from Spanish blue-veined Cabrales cheese, and typing of Penicillium roqueforti and Geotrichum candidum isolates. Int Dairy J, 17, 350-357.
  • Boysen M, Skouboe P, Frisvad J, et al (1996): Reclassification of the Penicillium roqueforti group into three species on the basis of molecular genetic and biochemical profiles. Microbiology, 142, 541-549.
  • Cantor MD, van den Tempel T, Hansen TK, et al (2004): Blue cheese. 175-198. In: Fox PF, McSweeney PLH, Cogan TM, Guinee TP (Eds), Cheese: Chemistry, Physics and Microbiology, Academic Press, London.
  • Demirer MA (1974): A study of molds isolated from certain cheeses and their ability to produce aflatoxins. Ankara Univ Vet Fak Derg, 21, 180-198.
  • Dumas E, Feurtey A, Rodríguez de la Vega RC, et al (2020): Independent domestication events in the blue-cheese fungus Penicillium roqueforti. Mol Ecol, 29, 2639-2660.
  • Frisvad JC, Samson RA (2004): Polyphasic taxonomy of Penicillium subgenus Penicillium. A guide to identification of food and air-borne terverticillate Penicillia and their mycotoxins. Stud Mycol, 49, C174.
  • Geisen R, Cantor M, Hansen T, et al (2001): Characterization of Penicillium roqueforti strains used as cheese starter cultures by RAPD typing. Int J Food Microbiol, 65, 183-191.
  • Glass NL, Donaldson GC (1995): Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Appl Environ Microbiol, 61, 1323-1330.
  • Gillot G, Jany J-L, Coton M, et al (2015): Insights into Penicillium roqueforti morphological and genetic diversity. PloS One, 10, e0129849.
  • Gillot G, Jany J-L, Poirier E, et al (2017): Functional diversity within the Penicillium roqueforti species. Int J Food Microbiol, 241, 141-150.
  • Gripon JC (1993): Mould-Ripened Cheeses. 111-136. In: PF Fox (Ed), Cheese: Chemistry, Physics and Microbiology, Springer, Boston.
  • Guley Z, Uysal H, Kilic S (2015): Lactic acid bacteria flora of Konya kuflu cheese: a traditional cheese from Konya province in Turkey. J Microbiol Biotechnol Food Sci, 04, 238-242.
  • Harrigan W (1998): Laboratory Methods in Food Microbiology. Academic Press, San Diego.
  • Hayaloglu AA, Kirbag S (2007): Microbial quality and presence of moulds in Kuflu cheese. Int J Food Microbiol, 115, 376-380.
  • Healy M, Huong J, Bittner T, et al (2005): Microbial DNA typing by automated repetitive-sequence-based PCR. J Clin Microbiol, 43, 199-207.
  • Kimura M (1980): A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol, 16, 111-120.
  • Kumar S, Stecher G, Li M, et al (2018): MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol, 35, 1547-1549.
  • Metin B (2018): Filamentous Fungi in Cheese Production. 257-275. In: Ş Öztürkoğlu Budak, HC Akal (Eds). Microbial Cultures and Enzymes in Dairy Technology. IGI Global, Hershey.
  • Ozmen Togay S, Capece A, Sıesto G, et al (2020): Molecular characterization of yeasts isolated from traditional Turkish cheeses. Food Sci Technol, 40, 871-876.
  • Ozturkoglu Budak S, Figge MJ, Houbraken J, et al (2016): The diversity and evolution of microbiota in traditional Turkish Divle Cave cheese during ripening. Int Dairy J, 58, 50-53.
  • Özkalp B, Durak Y (1998): Investigation of mold flora in moldy cheeses of Konya and its vicinity. Turk J Biol, 22, 341-346.
  • Redondo C, Cubero J, Melgarejo P (2009): Characterization of Penicillium Species by Ribosomal DNA Sequencing and BOX, ERIC and REP-PCR Analysis. Mycopathologia, 168, 11.
  • Ridgway R (1912): Color standards and color nomenclature. The author, Washington, D.C.
  • Ropars J, López-Villavicencio M, Dupont J, et al (2014): Induction of sexual reproduction and genetic diversity in the cheese fungus Penicillium roqueforti. Evol Appl, 7, 433-441.
  • Tekinşen KK, Cebirbay MA, Elmalı M (2009): Moldy cheese of Konya. Akademik Gıda, 7, 31-35.
  • Turin, Riva, Galbiati, et al (2000): Fast, simple and highly sensitive double-rounded polymerase chain reaction assay to detect medically relevant fungi in dermatological specimens. Eur J Clin Invest, 30, 511-518.
  • Ünsal A (1997): Süt Uyuyunca - Türkiye Peynirleri. Yapı Kredi Yayınları, İstanbul.
  • Van den Tempel T, Jakobsen M (2000): The technological characteristics of Debaryomyces hansenii and Yarrowia lipolytica and their potential as starter cultures for production of Danablu. Int Dairy J, 10, 263-270.
  • Versalovic J, Schneider M, Bruijn FJ, et al (1994): Genomic fingerprinting of bacteria using repetitive sequence-based polymerase chain reaction. Methods Mol Cell Biol, 5, 25-40.
  • Visagie CM, Houbraken J, Frisvad JC, et al (2014): Identification and nomenclature of the genus Penicillium. Stud Mycol, 78, 343-371.
  • Yalcin S, Senses S, Ozbas Y (2012): Identification and enzymatic characterization of the yeasts isolated from Erzincan tulum cheese. Mljekarstvo, 62, 53-61.
Year 2021, Volume: 68 Issue: 4, 349 - 354, 27.09.2021
https://doi.org/10.33988/auvfd.778788

Abstract

Project Number

Grant no. 119O314

References

  • Álvarez-Martín P, Flórez AB, López-Díaz TM, et al (2007): Phenotypic and molecular identification of yeast species associated with Spanish blue-veined Cabrales cheese. Int Dairy J, 17, 961-967.
  • Albenzio M, Corbo M, Rehman S, et al (2001): Microbiological and biochemical characteristics of Canestrato Pugliese cheese made from raw milk, pasteurized milk or by heating the curd in hot whey. Int J Food Microbiol, 67, 35-48.
  • Belén Flórez A, Álvarez-Martín P, López-Díaz TM, et al (2007): Morphotypic and molecular identification of filamentous fungi from Spanish blue-veined Cabrales cheese, and typing of Penicillium roqueforti and Geotrichum candidum isolates. Int Dairy J, 17, 350-357.
  • Boysen M, Skouboe P, Frisvad J, et al (1996): Reclassification of the Penicillium roqueforti group into three species on the basis of molecular genetic and biochemical profiles. Microbiology, 142, 541-549.
  • Cantor MD, van den Tempel T, Hansen TK, et al (2004): Blue cheese. 175-198. In: Fox PF, McSweeney PLH, Cogan TM, Guinee TP (Eds), Cheese: Chemistry, Physics and Microbiology, Academic Press, London.
  • Demirer MA (1974): A study of molds isolated from certain cheeses and their ability to produce aflatoxins. Ankara Univ Vet Fak Derg, 21, 180-198.
  • Dumas E, Feurtey A, Rodríguez de la Vega RC, et al (2020): Independent domestication events in the blue-cheese fungus Penicillium roqueforti. Mol Ecol, 29, 2639-2660.
  • Frisvad JC, Samson RA (2004): Polyphasic taxonomy of Penicillium subgenus Penicillium. A guide to identification of food and air-borne terverticillate Penicillia and their mycotoxins. Stud Mycol, 49, C174.
  • Geisen R, Cantor M, Hansen T, et al (2001): Characterization of Penicillium roqueforti strains used as cheese starter cultures by RAPD typing. Int J Food Microbiol, 65, 183-191.
  • Glass NL, Donaldson GC (1995): Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Appl Environ Microbiol, 61, 1323-1330.
  • Gillot G, Jany J-L, Coton M, et al (2015): Insights into Penicillium roqueforti morphological and genetic diversity. PloS One, 10, e0129849.
  • Gillot G, Jany J-L, Poirier E, et al (2017): Functional diversity within the Penicillium roqueforti species. Int J Food Microbiol, 241, 141-150.
  • Gripon JC (1993): Mould-Ripened Cheeses. 111-136. In: PF Fox (Ed), Cheese: Chemistry, Physics and Microbiology, Springer, Boston.
  • Guley Z, Uysal H, Kilic S (2015): Lactic acid bacteria flora of Konya kuflu cheese: a traditional cheese from Konya province in Turkey. J Microbiol Biotechnol Food Sci, 04, 238-242.
  • Harrigan W (1998): Laboratory Methods in Food Microbiology. Academic Press, San Diego.
  • Hayaloglu AA, Kirbag S (2007): Microbial quality and presence of moulds in Kuflu cheese. Int J Food Microbiol, 115, 376-380.
  • Healy M, Huong J, Bittner T, et al (2005): Microbial DNA typing by automated repetitive-sequence-based PCR. J Clin Microbiol, 43, 199-207.
  • Kimura M (1980): A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol, 16, 111-120.
  • Kumar S, Stecher G, Li M, et al (2018): MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol, 35, 1547-1549.
  • Metin B (2018): Filamentous Fungi in Cheese Production. 257-275. In: Ş Öztürkoğlu Budak, HC Akal (Eds). Microbial Cultures and Enzymes in Dairy Technology. IGI Global, Hershey.
  • Ozmen Togay S, Capece A, Sıesto G, et al (2020): Molecular characterization of yeasts isolated from traditional Turkish cheeses. Food Sci Technol, 40, 871-876.
  • Ozturkoglu Budak S, Figge MJ, Houbraken J, et al (2016): The diversity and evolution of microbiota in traditional Turkish Divle Cave cheese during ripening. Int Dairy J, 58, 50-53.
  • Özkalp B, Durak Y (1998): Investigation of mold flora in moldy cheeses of Konya and its vicinity. Turk J Biol, 22, 341-346.
  • Redondo C, Cubero J, Melgarejo P (2009): Characterization of Penicillium Species by Ribosomal DNA Sequencing and BOX, ERIC and REP-PCR Analysis. Mycopathologia, 168, 11.
  • Ridgway R (1912): Color standards and color nomenclature. The author, Washington, D.C.
  • Ropars J, López-Villavicencio M, Dupont J, et al (2014): Induction of sexual reproduction and genetic diversity in the cheese fungus Penicillium roqueforti. Evol Appl, 7, 433-441.
  • Tekinşen KK, Cebirbay MA, Elmalı M (2009): Moldy cheese of Konya. Akademik Gıda, 7, 31-35.
  • Turin, Riva, Galbiati, et al (2000): Fast, simple and highly sensitive double-rounded polymerase chain reaction assay to detect medically relevant fungi in dermatological specimens. Eur J Clin Invest, 30, 511-518.
  • Ünsal A (1997): Süt Uyuyunca - Türkiye Peynirleri. Yapı Kredi Yayınları, İstanbul.
  • Van den Tempel T, Jakobsen M (2000): The technological characteristics of Debaryomyces hansenii and Yarrowia lipolytica and their potential as starter cultures for production of Danablu. Int Dairy J, 10, 263-270.
  • Versalovic J, Schneider M, Bruijn FJ, et al (1994): Genomic fingerprinting of bacteria using repetitive sequence-based polymerase chain reaction. Methods Mol Cell Biol, 5, 25-40.
  • Visagie CM, Houbraken J, Frisvad JC, et al (2014): Identification and nomenclature of the genus Penicillium. Stud Mycol, 78, 343-371.
  • Yalcin S, Senses S, Ozbas Y (2012): Identification and enzymatic characterization of the yeasts isolated from Erzincan tulum cheese. Mljekarstvo, 62, 53-61.
There are 33 citations in total.

Details

Primary Language English
Subjects Veterinary Surgery
Journal Section Research Article
Authors

Meryem Seri 0000-0001-6871-1608

Banu Metin 0000-0002-3203-0058

Project Number Grant no. 119O314
Publication Date September 27, 2021
Published in Issue Year 2021Volume: 68 Issue: 4

Cite

APA Seri, M., & Metin, B. (2021). Mycobiota of Konya mold-ripened (Kuflu) Tulum cheese and the diversity of Penicillium roqueforti isolates. Ankara Üniversitesi Veteriner Fakültesi Dergisi, 68(4), 349-354. https://doi.org/10.33988/auvfd.778788
AMA Seri M, Metin B. Mycobiota of Konya mold-ripened (Kuflu) Tulum cheese and the diversity of Penicillium roqueforti isolates. Ankara Univ Vet Fak Derg. September 2021;68(4):349-354. doi:10.33988/auvfd.778788
Chicago Seri, Meryem, and Banu Metin. “Mycobiota of Konya Mold-Ripened (Kuflu) Tulum Cheese and the Diversity of Penicillium Roqueforti Isolates”. Ankara Üniversitesi Veteriner Fakültesi Dergisi 68, no. 4 (September 2021): 349-54. https://doi.org/10.33988/auvfd.778788.
EndNote Seri M, Metin B (September 1, 2021) Mycobiota of Konya mold-ripened (Kuflu) Tulum cheese and the diversity of Penicillium roqueforti isolates. Ankara Üniversitesi Veteriner Fakültesi Dergisi 68 4 349–354.
IEEE M. Seri and B. Metin, “Mycobiota of Konya mold-ripened (Kuflu) Tulum cheese and the diversity of Penicillium roqueforti isolates”, Ankara Univ Vet Fak Derg, vol. 68, no. 4, pp. 349–354, 2021, doi: 10.33988/auvfd.778788.
ISNAD Seri, Meryem - Metin, Banu. “Mycobiota of Konya Mold-Ripened (Kuflu) Tulum Cheese and the Diversity of Penicillium Roqueforti Isolates”. Ankara Üniversitesi Veteriner Fakültesi Dergisi 68/4 (September 2021), 349-354. https://doi.org/10.33988/auvfd.778788.
JAMA Seri M, Metin B. Mycobiota of Konya mold-ripened (Kuflu) Tulum cheese and the diversity of Penicillium roqueforti isolates. Ankara Univ Vet Fak Derg. 2021;68:349–354.
MLA Seri, Meryem and Banu Metin. “Mycobiota of Konya Mold-Ripened (Kuflu) Tulum Cheese and the Diversity of Penicillium Roqueforti Isolates”. Ankara Üniversitesi Veteriner Fakültesi Dergisi, vol. 68, no. 4, 2021, pp. 349-54, doi:10.33988/auvfd.778788.
Vancouver Seri M, Metin B. Mycobiota of Konya mold-ripened (Kuflu) Tulum cheese and the diversity of Penicillium roqueforti isolates. Ankara Univ Vet Fak Derg. 2021;68(4):349-54.