Filamentous Fungi Associated with the Golot Cheese of the Rize-Ardesen Highlands in Turkey

Year 2020, Issue: 19, 435 - 441, 31.08.2020

Banu Metin

https://doi.org/10.31590/ejosat.715639

Cited By: 2

Abstract

The aim of this study was to identify using molecular methods the filamentous fungi associated with the Golot cheese produced in Ardesen, Rize Province, East Black Sea region, Turkey. Sixteen fungi were isolated from seven cheese samples and subjected to sequencing analysis using different fungal DNA barcodes. The first marker used, internal transcribed spacer (ITS), allowed identification of Geotrichum candidum and Penicillium roqueforti. The other isolates, defined as Penicillium and Cladosporium, could be identified only at the genus level using ITS; therefore, the beta-tubulin (benA) gene and the microsatellite PC4 markers were used to define the remaining Penicillium isolates as P. biforme and P. solitum. The Cladosporium isolate was identified as C. macrocarpum by analysis using benA and translation elongation factor 1-α (tef1) genes. The most common species associated with Golot cheeses were determined to be P. biforme (56%) and G. candidum (25%). Previously unknown sequences of P. solitum PC4 and C. macrocarpum tef1, and a longer version of C. macrocarpum benA were submitted to GenBank.

Keywords

Golot cheese, Mycobiota, Fungal identification markers, Penicillium, Cladosporium

Supporting Institution

The Scientific and Technological Research Council of Turkey (TUBITAK) to B. M.

Project Number

Grant no. 119O314

Thanks

The author thanks Havva Balcan for providing the cheese samples.

Türkiye'de Rize-Ardeşen Yaylalarının Golot Peyniri ile İlişkili Filamentli Funguslar

Abstract

Bu çalışmanın amacı, Doğu Karadeniz Bölgesi, Rize İli, Ardeşen'de üretilen Golot peyniri ile ilişkili filamentli fungusların moleküler yöntemler kullanılarak belirlenmesidir. Yedi peynir örneğinden on altı fungus izole edilmiş ve farklı fungal DNA barkodları kullanılarak dizilim belirleme analizine tabi tutulmuştur. Kullanılan ilk markör olan internal transcribed spacer bölgesi (ITS), Geotrichum candidum ve Penicillium roqueforti'nin identifikasyonuna olanak vermiştir. Diğer izolatlar, ITS kullanılarak sadece cins düzeyinde Penicillium ve Cladosporium olarak tanımlanabilmiştir; bu nedenle, beta-tubulin (benA) geni ve mikrosatellit PC4 markörleri, kalan Penicillium izolatlarını P. biforme ve P. solitum olarak tanımlamak için kullanılmıştır. Cladosporium izolatı, benA ve translation elongation factor 1-α (tef1) genleri kullanılarak analiz edilerek C. macrocarpum olarak tanımlanmıştır. Golot peynirleriyle ilişkili en yaygın türlerin P. biforme (%56) ve G. candidum (%25) olduğu belirlenmiştir. Daha önce bilinmeyen P. solitum PC4 ve C. macrocarpum tef1 dizilimleri ve daha uzun bir C. macrocarpum benA versiyonu GenBank'a sunulmuştur.

Keywords

Golot peyniri, Mikobiyota, Fungal identifikasyon markörleri, Penicllium, Cladosporium

Project Number

Grant no. 119O314

References

• Anelli, P., Haidukowski, M., Epifani, F., Cimmarusti, M. T., Moretti, A., Logrieco, A., & Susca, A. (2019). Fungal mycobiota and mycotoxin risk for traditional artisan Italian cave cheese. Food Microbiology, 78, 62-72.
• Amrouche, T., Mounier, J., Pawtowski, A., Thomas, F., & Picot, A. (2020). Microbiota associated with dromedary camel milk from Algerian Sahara. Current Microbiology, 77(1), 24-31.
• Bachmann, H.P., Bobst, C., Butikofer, U., Casey, M.G., Dalla Torre, M., Frohlich-Wyder, M.T., Furst, M. (2005). Occurrence and significance of Fusarium domesticum alias Anticollanti on smear-ripened cheeses. LWT- Food Science and Technology, 38(4), 399-407.
• Balcan, H. (2017). Personal communication, Rize-Ardesen village.
• Batra, N., Kaur, H., Mohindra, S., Singh, S., Shamanth, A. S., & Rudramurthy, S. M. (2019). Cladosporium sphaerospermum causing brain abscess, a saprophyte turning pathogen: Case and review of published reports. Journal de Mycologie Medicale, 29(2), 180-184.
• Bensch, K., Groenewald, J. Z., Meijer, M., Dijksterhuis, J., Jurjević, Ž., Andersen, B., ... & Samson, R. A. (2018). Cladosporium species in indoor environments. Studies in Mycology, 89, 177-301.
• Bensch, K., Braun, U., Groenewald, J. Z., & Crous, P. W. (2012). The genus Cladosporium. Studies in Mycology, 72, 1-401.
• Boutrou, R., & Guéguen, M. (2005). Interests in Geotrichum candidum for cheese technology. International journal of food microbiology, 102(1), 1-20.
• Caglar, A., Turkoglu, H., Ceylan, Z. G., Dayisoyl, K. S. (1998). Golot peynirinin uretim teknigi ve bilesimi uzerine arastirmalar (Studies on the production technique and composition of Golot cheese). V. Sut ve Sut Urunleri Sempozyumu - Geleneksel Sut Urunleri (No 621, pp. 65-78). Ankara: Milli Produktivite Merkezi Yayinlari.
• Cakmakci, S. (2011). Turkiye Peynirleri (Cheeses of Turkey). In Hayaloglu A. A. & Ozer B. (eds) Peynir Biliminin Temelleri (pp. 598-600). Izmir: Sidas Medya.
• Chabalier, C., Ratomahenina, R., Galzy, P., & Dieu, B. (1995). Remarks on the appearance of “violine” on Cantal cheese. Acta Microbiologica et Immunologica Hungarica, 42(2), 199–202.
• Costanzo, N., Rodolfi, M., Musarella, R., Ceniti, C., Santoro, A., Britti, D., & Casalinuovo, F. (2018). Microbial quality evaluation of grated cheese samples collected at retail level in Calabria (Italy). Journal of Food Safety, 38(6), e12530.
• Cuétara, M. S., Alhambra, A., Moragues, M. D., González-Elorza, E., Pontón, J., & del Palacio, A. (2009). Detection of (1→ 3)-β-D-glucan as an adjunct to diagnosis in a mixed population with uncommon proven invasive fungal diseases or with an unusual clinical presentation. Clinical and Vaccine Immunology, 16(3), 423-426.
• Decontardi, S., Soares, C., Lima, N., & Battilani, P. (2018). Polyphasic identification of Penicillia and Aspergilli isolated from Italian grana cheese. Food Microbiology, 73, 137-149.
• Fabian, S. J., Maust, M. D., & Panaccione, D. G. (2018). Ergot alkaloid synthesis capacity of Penicillium camemberti. Applied and Environmental Microbiology, 84(19), e01583-18.
• Fox, P. F., Law, J., McSweeney, P. L. H., & Wallace, J. (1993). Biochemistry of cheese ripening. In Fox P.F. (eds) Cheese: Chemistry, Physics and Microbiology (pp. 389-438). Boston, MA: Springer.
• Frisvad, J. C., & Samson, R. A. (2004). Polyphasic taxonomy of Penicillium subgenus Penicillium. A guide to identification of food and air-borne terverticillate Penicillia and their mycotoxins. Studies in mycology, 49(1), 1-174.
• Frisvad, J. C., Smedsgaard, J., Larsen, T. O., & Samson, R. A. (2004). Mycotoxins, drugs and other extrolites produced by species in Penicillium subgenus Penicillium. Studies in Mycology, 49(201), e41.
• Garnier, L., Valence, F., & Mounier, J. (2017). Diversity and control of spoilage fungi in dairy products: An update. Microorganisms, 5(3), 42.
• Giraud, F., Giraud, T., Aguileta, G., Fournier, E., Samson, R., Cruaud, C., ... & Dupont, J. (2010). Microsatellite loci to recognize species for the cheese starter and contaminating strains associated with cheese manufacturing. International Journal of Food Microbiology, 137(2-3), 204-213.
• Glass, N. L., & Donaldson, G. C. (1995). Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Applied and Environmental Microbiology, 61(4), 1323-1330.
• Gripon J. C. (1993). Mould-ripened cheeses. In: Fox P.F. (eds) Cheese: Chemistry, Physics and Microbiology (pp. 111-136). Boston, MA: Springer.
• Gu, Y., Liu, Y., Cao, S., Huang, X., Zuo, Z., Yu, S., ... & Wu, R. (2016). Suppressive subtractive hybridization reveals different gene expression between high and low virulence strains of Cladosporium cladosporioides. Microbial Pathogenesis, 100, 276-284.
• Harrigan, W. F. (1998). Laboratory Methods in Food Microbiology (pp. 263-269). San Diego, CA: Academic Press.
• Hymery, N., Vasseur, V., Coton, M., Mounier, J., Jany, J., Barbier, G. and Coton, E. (2014). Filamentous fungi and mycotoxins in cheese: A review. Comprehensive Reviews in Food Science and Food Safety, 13, 437-456.
• Hocking, A. D., & Faedo, M. (1992). Fungi causing thread mould spoilage of vacuum packaged Cheddar cheese during maturation. International Journal of Food Microbiology, 16(2), 123-130.
• Kamber, U., & Terzi, G. (2008). The traditional cheeses of Turkey: Middle and Eastern Black sea region. Food Reviews International, 24(1), 95-118.
• Kumar, S., Stecher, G., Li, M., Knyaz, C., & Tamura, K. (2018). MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution, 35(6), 1547-1549.
• Lalueza, A., López-Medrano, F., Del Palacio, A., Alhambra, A., Alvarez, E., Ramos, A., ... & Aguado, J. M. (2011). Cladosporium macrocarpum brain abscess after endoscopic ultrasound-guided celiac plexus block. Endoscopy, 43(S 02), E9-E10.
• Lund, F., Filtenborg, O., & Frisvad, J. C. (1995). Associated mycoflora of cheese. Food Microbiology, 12, 173-180.
• Marcellino, N., & Benson, D. R. (2013). The good, the bad, and the ugly: Tales of mold‐ripened cheese. Microbiology Spectrum, 1(1).
• Martín, J. F., & Liras, P. (2017). Secondary metabolites in cheese fungi. In: Merillon, J. M., Ramawat, K. G. (Eds.), Reference Series in Phytochemistry: Fungal Metabolites (pp. 293-315). Cham, Switzerland: Springer.
• Merla, C., Andreoli, G., Garino, C., Vicari, N., Tosi, G., Guglielminetti, M. L., ... & Fabbi, M. (2018). Monitoring of ochratoxin A and ochratoxin-producing fungi in traditional salami manufactured in Northern Italy. Mycotoxin Research, 34(2), 107-116.
• Marín, P., Palmero, D., & Jurado, M. (2015). Occurrence of moulds associated with ovine raw milk and cheeses of the Spanish region of Castilla La Mancha. International Journal of Dairy Technology, 68(4), 565-572.
• McSweeney, P. L. (2004). Biochemistry of cheese ripening. International Journal of Dairy Technology, 57(2‐3), 127-144.
• Metin, B. (2018). Filamentous fungi in cheese production. In Ş. Öztürkoğlu Budak, & H. Akal (Eds.), Microbial Cultures and Enzymes in Dairy Technology (pp. 257-275). Hershey, PA: IGI Global.
• Panelli, S., Buffoni, J. N., Bonacina, C., & Feligini, M. (2012). Identification of moulds from the Taleggio cheese environment by the use of DNA barcodes. Food Control, 28(2), 385-391.
• Peterson, S. W. (2004). Multilocus DNA sequence analysis shows that Penicillium biourgeianum is a distinct species closely related to P. brevicompactum and P. olsonii. Mycological Research, 108(4), 434-440.
• Pitt, J. I., & Hocking, A. D. (2009). Fungi and Food Spoilage (pp. 78-79). New York: Springer.
• Pleadin, J., Zadravec, M., Brnić, D., Perković, I., Škrivanko, M., & Kovačević, D. (2017). Moulds and mycotoxins detected in the regional speciality fermented sausage ‘slavonski kulen’during a 1-year production period. Food Additives & Contaminants: Part A, 34(2), 282-290.
• Ramos-Pereira, J., Mareze, J., Patrinou, E., Santos, J. A., & López-Díaz, T. M. (2019). Polyphasic identification of Penicillium spp. isolated from Spanish semi-hard ripened cheeses. Food Microbiology, 84, 103253.
• Ratomahenina, R., Chabalier, C., & Galzy, P. (1994). Concerning Sporendonema casei Desmazieres. Latte, 19(6), 616–617.
• Ropars, J., Cruaud, C., Lacoste, S., & Dupont, J. (2012). A taxonomic and ecological overview of cheese fungi. International Journal of Food Microbiology, 155(3), 199–210.
• Scaramuzza, N., Diaferia, C., & Berni, E. (2015). Monitoring the mycobiota of three plants manufacturing Culatello (a typical Italian meat product). International Journal of Food Microbiology, 203, 78-85.
• Schoch, C. L., Seifert, K. A., Huhndorf, S., Robert, V., Spouge, J. L., Levesque, C. A., ... & Fungal Barcoding Consortium. (2012). Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proceedings of the National Academy of Sciences, 109(16), 6241-6246.
• Schubert, K., Groenewald, J. Z., Braun, U., Dijksterhuis, J., Starink, M., Hill, C. F., ... & Crous, P. W. (2007). Biodiversity in the Cladosporium herbarum complex (Davidiellaceae, Capnodiales), with standardisation of methods for Cladosporium taxonomy and diagnostics. Studies in Mycology, 58, 105-156.
• Spinnler, H. E., & Gripon, J. C. (2004). Surface mould-ripened cheeses. In P. F. Fox, P. L. H. McSweeney, T. M. Cogan, & T. P. Guinee (Eds.), Cheese: Chemistry, Physics and Microbiology (Vol. 2, pp. 157–174). Amsterdam: Elsevier Academic Press.
• Tamura, K., & Nei, M. (1993). Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution, 10(3), 512-526.
• Turin, L., Riva, F., Galbiati, G., & Cainelli, T. (2000). Fast, simple and highly sensitive double-rounded polymerase chain reaction assay to detect medically relevant fungi in dermatological specimens. European Journal of Clinical Investigation, 30(6), 511-518.
• Unsal, A. (1997). Sut uyuyunca - Turkiye peynirleri (When the milk sleeps - Cheeses of Turkey) (pp. 154-156). Istanbul: Yapi Kredi Yayinlari.
• Werner, H., Nielsen, E. W., Ardö, Y., Rage, A., & Antila, V. (1999). North European varieties of cheese. In P. F. Fox (Ed.), Cheese: Chemistry, Physics and Microbiology (pp. 245–262). Boston, MA: Springer.
• White, T. J., Bruns, T. D., Lee, S. B. and Taylor, J. W. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis, M. A., Gelfand, D. H., Sninsky, J. J. and White, T. J. (Eds.), PCR Protocols: A Guide to Methods and Applications (pp. 315-322). New York: Academic Press.
• Yazici, F. and Dervisoglu, M. (2002) Proteolysis in Golot cheese. Acta Alimentaria, 31 (3), 307-313.