TAXONOMY, MORPHOLOGICAL, GENETIC AND METABOLIC CHARACTERISTICS OF PENICILLIUM ROQUEFORTI AS A CHEESE MOLD

Abstract

Penicillium roqueforti is a filamentous fungus used as secondary starter culture in mold-ripening of cheese. In facilities using starter cultures, P. roqueforti is added directly in milk or introduced by spraying on the cheese curd. If a commercial starter is not used, the fungus can spontaneously grow on cheese through contamination from the environment. In recent years, studies on morphological, metabolic, and genetic characteristics of P. roqueforti have been conducted. New findings have been reported on the adaptation of P. roqueforti that originates from caves or cellars, to cheese matrix and the domestication process that has been going on for centuries. In addition, this species was found to be able to reproduce sexually, which is of great biotechnological importance. In this review, taxonomic, morphological, genetic, and metabolic features of P. roqueforti are presented, the use of these characteristics in cheese production and the biotechnological potential of P. roqueforti is emphasized.

Keywords

• Penicillium roqueforti
• mold-ripened cheeses
• starter culture
• taxonomy
• genetic characteristics

PEYNİR KÜFÜ OLARAK PENICILLIUM ROQUEFORTI’NİN TAKSONOMİSİ, MORFOLOJİK, GENETİK VE METABOLİK ÖZELLİKLERİ

Abstract

Filamentli bir fungus olan Penicillium roqueforti, küflü peynirlerin olgunlaştırılmasında sekonder starter olarak kullanılmaktadır. Starter kültür olarak kullanılan işletmelerde, P. roqueforti direkt olarak süt içine katılabildiği gibi, peynir pıhtısı üzerine püskürtülerek de inoküle edilmektedir. Ticari starter kültür kullanılmadığında ise ortamdan bulaşarak peynirde spontan olarak gelişebilir. Son yıllarda, P. roqueforti’nin morfolojik, metabolik ve genetik özellikleri ile ilgili çalışmalar yapılmıştır. Mağara ya da mahzen ortamından gelen P. roqueforti’nin peynir matriksine adaptasyonu ve yüzyıllar süren evcilleşme süreci hakkında yeni bulgular ortaya çıkmıştır. Ayrıca, P. roqueforti’nin eşeyli üreme yapabildiği tespit edilmiştir ki, bunun biyoteknolojik açıdan büyük önemi söz konusudur. Bu derlemede, gıda endüstrisi için değerli bir tür olan P. roqueforti’nin taksonomik, morfolojik, genetik ve metabolik özellikleri sunulmuş, bu özelliklerin küflü peynir üretiminde kullanımı değerlendirilmiş ve P. roqueforti’nin biyoteknolojik potansiyeli vurgulanmıştır.

Keywords

• Penicillium roqueforti
• küflü peynir
• starter kültür
• taksonomi
• genetik özellikler

References

1. Anonim, (2015). “Geotrichum candidum”, http://microbialfoods.org/geotrichum-candidum-mold-transition/ , Son Erişim tarihi: 14.07.2020
2. Bodinaku, I., Shaffer, J., Connors, A.B., Steenwyk, J.L., Biango-Daniels, M.N., Kastman, E.K., Rokas, A., Robbat, A., Wolfe, B.E. (2019). Rapid Phenotypic and Metabolomic Domestication of Wild Penicillium Molds on Cheese. ASM MBio, 10(5): e02445-19. https://doi.org/10.1101/647172
3. Brown, D.W., Butchko, R.A.E., Proctor, R.H., (2011). Identification of genes and gene clusters involved in mycotoxin synthesis. Ed.: De Saeger, S., Woodhead Publishing, 2nd edition, Cambridge, UK, 333-348 p.
4. Cleere, M., (2017). Pigment Biosynthesis Genes in the Blue Cheese Fungus Penicillium roqueforti, PhD thesis, University of Nottingham, Nottingham, UK, 93 p.
5. Cheeseman, K., Ropars, J., Renault, P., Dupont, J., Gouzy, J., Branca, A., Abraham, A.L., Ceppi, M., Conseiller, E., Debuchy, R., Malagnac, F., Goarin, A., Silar, P., Lacoste, S., Sallet, E., Bensimon, A., Giraud, T., Brygoo, Y., (2014). Multiple recent horizontal transfers of a large genomic region in cheese making fungi. Nature Communications, 5: 2876. https://doi.org/10.1038/ncomms3876
6. Çakmakçı, S., (2011). Türkiye Peynirleri. Peynir Biliminin Temelleri, Ed.: Hayaloğlu, A.A. ve Özer, B., 1.Baskı, Sidas Medya LTD.ŞTİ., İzmir.
7. Çakmakçı, S., Çetin, B., Gürses, M., Dağdemir, E., Hayaloğlu, A.A., (2012). Morphological, molecular and mycotoxigenic identification of dominant filamentous fungi from Moldy Civil Cheese. J. Food Prot., 75 (11): 2045-2049. https://doi.org/10.4315/0362-028X.JFP-12-107
8. Del-Cid, A., Gil-Duran, C., Vaca, I., Rojas-Aedo, J.F., Garcia-Rico, R.O., Levican, G., Chavez, R., (2016). Identification and functional analysis of the mycophenolic acid gene cluster of Penicillium roqueforti. PLoS One, 11(1): e0147047. https://doi.org/10.1371/journal.pone.0147047

9. Dumas, E., Feurtey, A., Rodríguez de la Vega, R.C., Le Prieur, S., Snirc, A., Coton, M., Thierry, A., Coton, E., Le Piver, M., Roueyre, D., Ropars, J., Branca, A., Giraud, T. (2020). Independent domestication events in the blue‐cheese fungus Penicillium roqueforti. Molecular Ecology, 00: 1– 22. https://doi.org/10.1101/451773
10. Fernandez-Bodega, M.A., Mauriz, E., Gomez, A., Martin, J.F., (2009). Proteolytic activity, mycotoxins and andrastin A in Penicillium roqueforti strains isolated from Cabrales, Valdeon and Bejes-Tresviso local varieties of blue-veined cheeses. Int. J. of Food Microbiol., 136(1): 18-25. https://doi.org/10.1016/j.ijfoodmicro.2009.09.014
11. Frisvad, C.F., 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: 1-174.
12. Fox, P.F., Guinee, T.P., Cogan, T.M., McSweeney, P.L.H., (2016a). Principal families of cheeses: Blue veined cheeses (Chapter 3). In: Fundamentals of Cheese Science, 2rd edition, Springer, New York, pp. 54-57.
13. Fox, P.F., Guinee, T.P., Cogan, T.M., McSweeney, P.L.H., (2016b). Cheese Flavour (Chapter 13). In: Fundamentals of Cheese Science, 2rd edition, Springer, New York, pp. 443-472.
14. Fox, P.F., Guinee, T.P., Cogan, T.M., McSweeney, P.L.H., (2016c). Microbiology of Cheese Ripening (Chapter 11). In: Fundamentals of Cheese Science, 2rd edition, Springer, New York, pp. 333-351.
15. Fox, P.F., Guinee, T.P., Cogan, T.M., McSweeney, P.L.H., (2016d). Biochemistry of Cheese Ripening (Chapter 12). In: Fundamentals of Cheese Science, 2rd edition, Springer, New York, pp. 391-439.
16. Fontaine, K., Hymery, N., Lacroix, M.Z., Puel, S., Puel, O., Rigalma, K., Gaydou, V., Coton, E., Mounier, J., (2015). Influence of intraspesific variability and abiotic factors mycotoxin production in Penicillium roqueforti. Int. J. of Food Microbiol., 215: 187-193. https://doi.org/10.1016/j.ijfoodmicro.2015.07.021
17. Garcia-Estrada, C., Martin, J.F., (2016). Biosynthetic gene clusters for relevant secondary metabolites produced by Penicillium roqueforti in blue cheeses. Appl. Microbiol. Biotechnol., 100: 8303-8313. https://doi.org/10.1007/s00253-016-7788-x
18. Geisen, R., Cantor, M.D., Hansen, T.K., Holzapfel, W.H., Jakobsen, M., (2001). Characterization of Penicillium roqueforti strains used as cheese starter cultures by RAPD typing. Int. J. of Food Microbiol., 65(3): 183-191. https://doi.org/10.1016/s0168-1605(00)00514-6
19. Gibbons, J.G., Rinker, D.C., (2015). The genomics of microbial domestication in the fermented food environment. Curr. Opin. Genet. Dev., 35: 1-8. https://doi.org/10.1016/j.gde.2015.07.003
20. Gillot, G., Jany, J.L., Coton, M., Le Floch, G., Debaets, S., Ropars, J., Lopez- Villavicencio, M., Dupont, J., Branca, A., Giraud, T., Coton, E., (2015). Insights into Penicillium roqueforti: Morphological and genetic diversity. PLoS One, 10(6): e0129849 (1-21). https://doi.org/10.1371/journal.pone.0129849
21. Gillot, G., Jany, J.C., Poirier, E., Maillard, M.B., Debaets, S., Thierry, A., Coton, E., Coton, M., (2017a). Functional diversity within the Penicillium roqueforti species. Int. J. of Food Microbiol., 241: 141-150. https://doi.org/10.1016/j.ijfoodmicro.2016.10.001
22. Gillot, G., Jany, J.L., Dominguez-Santos, R., Poirier, E., Debaets, S., Hidalgo, P.I., Ullan, R.V., Coton, E., Coton, M. (2017b). Genetic basis for mycophenolic acid production and strain-dependent production variability in Penicillium roqueforti. Food Microbiology, 62: 239-250. https://doi.org/10.1016/j.fm.2016.10.013
23. 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. Int. J. of Food Microbiol., 137 (2-3): 204-213. https://doi.org/10.1016/j.ijfoodmicro.2009.11.014
24. Guevara-Suarez, M., García, D., Cano-Lira, J.F., Guarro, J., Gené, J. (2020). Species diversity in Penicillium and Talaromyces from herbivore dung, and the proposal of two new genera of penicillium-like fungi in Aspergillaceae. Fungal Syst. Evol., 5: 39-75. https://doi.org/10.3114/fuse.2020.05.03
25. Gürkan, H., Yılmaztekin, M., Çakmakçı, S., Hayaloğlu, A., (2018). Volatile compounds and biogenic amines during the ripening of mold-ripened Civil cheese manufactured using three different strains of Penicillium roqueforti. J. Food Saf., 38e12568. https://doi.org/10.1111/jfs.12568
26. Houbraken, J., Frisvad, J.C., Samson, R.A., (2010). Sex in Penicillium series Roqueforti. IMA Fungus, 1(2): 171-180. https://doi.org/10.5598/imafungus.2010.01.02.10
27. Hymery, N., Vasseur, V., Coton, M., Mounier, J., Jany, J.L., Barbier, G., Coton, E., (2014). Filamentous fungi and mycotoxins in cheese: A review. Comprehensive Reviews in Food Science and Food Safety, 13(4): 437-456. https://doi.org/10.1111/1541-4337.12069
28. Kırtıl, H.E. (2018). Küflü peynirlerden izole edilen küflerin moleküler tanımlanması ve karakterizasyonu. Yıldız Teknik Üniversitesi, Fen Bilimleri Enstitüsü, Gıda Mühendisliği Anabilim Dalı, Yüksek lisans tezi, İstanbul, 131 s.
29. Kosalkova, K., Dominguez-Santos, R., Coton, M., Coton, E., Garcia-Estrada, C., Liras, P., Martin, J.F., (2015). A natural short pathway synthesizes roquefortine C but not meleagrin in three different Penicillium roqueforti strains. Appl. Microbiol. Biotechnol., 99: 7601-7612. https://doi.org/10.1007/s00253-015-6676-0
30. López-Villavicencio, M., Aguileta, G., Giraud, T., de Vienne, D.M., Lacoste, S., Couloux, A., Dupont, J. (2010). Sex in Penicillium: Combined phylogenetic and experimental approaches, Fungal Genetics and Biology, 47(8): 693-706. https://doi.org/10.1016/j.fgb.2010.05.002
31. Martin, J.F. and Coton M., (2017). Blue Cheese: Microbiota and Fungal Metabolites. In: Fermented Foods in Health and Disease Prevention, Ed.: Frias, J., Martinez-Villaluenga, C., Penas, E., 1.Baskı, Academic Press.
32. Metin, B., (2018). Filamentous Fungi in Cheese Production. In: Microbial Cultures and Enzymes in Dairy Technology, Ed.: Öztürkoğlu Budak, Ş., Akal, H.C. 1st edition, IGI Global.
33. Mioso, R., Toledo Marante, F., Herrera Bravo de Laguna, I., (2015). Penicillium roqueforti: a multifunctional cell factory of high value-added molecules. J. Appl. Microbiol. 118: 781e791. https://doi.org/10.1111/jam.12706
34. Monnet, C., Landaud, S. Bonnarme, P., Swennen, D. (2014). Growth and adaptation of microorganisms on the cheese surface. FEMS Microbiology Letters, 362: 1-9. https://doi.org/10.1093/femsle/fnu025
35. MycoBank, (2020). Taxa descriptions: Penicillium roqueforti Thom, http://www.mycobank.org/BioloMICS.aspx?TableKey=14682616000000063&Rec=15208&Fields=All, Son Erişim Tarihi: 3.07.2020
36. Öztürkoğlu Budak, S., Figge, M.R., Houbraken, J., Vries, R.P. (2016). The diversity and evolution of microbiota in traditional Turkish Divle Cave cheese during ripening. International Dairy Journal, 58: 50-53. https://doi.org/10.1016/j.idairyj.2015.09.011
37. Petyaev, I.M., Bashmakov, Y.K., (2012). Could cheese be the missing piece in the French paradox puzzle?. Med. Hypotheses, 79, 746-749. https://doi.org/10.1016/j.mehy.2012.08.018
38. Perrone, G., Susca, A., (2017). Penicillium species and their associated mycotoxins. In: Mycotoxigenic Fungi: Methods and Protocols. Ed.: Moretti, A. ve Susca, A.., Humana Press Springer Protocols, 1st edition, New York.
39. Renaud, S., de Lorgeril, M., (1992). Wine, alcohol, platelets, and the French paradox for coronary heart disease. Lancet, 339: 1523-1526. https://doi.org/10.1016/0140-6736(92)91277-f
40. Ropars, J., Dupont, J., Fontanillas, E., Rodriguez de la Vega, R.C., Malagnac, F., Coton, M., Giraud, T., L_opez-Villavicencio, M., (2012). Sex in cheese: evidence for sexuality in the fungus Penicillium roqueforti. PLoS One, 7(11): 7e49665. https://doi.org/10.1371/journal.pone.0049665
41. Ropars, J., Lopez-Villavicencio, M., Dupont, J., Snirc, A., Gillot, G., Coton, M., Jany, J.-L., Coton, E., Giraud, T., (2014). Induction of sexual reproduction and genetic diversity in the cheese fungus Penicillium roqueforti. Evol. Appl., 7(4): 433-441. https://doi.org/10.1111/eva.12140
42. Ropars, J., de la Vega, R.C.R., Lopez-Villavicencio, M., Gouzy, J., Sallet, E., Dumas, E., Lacoste, S., Debuchy, R., Dupont, J., Branca, A., Giraud, T., (2015). Adaptive horizontal gene transfers between multiple cheesee-associated fungi. Curr. Biol., 25(19): 2562-2569. https://doi.org/10.1016/j.cub.2015.08.025
43. Ropars, J., De la Vega, R.R., Villavicencio, M.L., Branca, A. (2016a). Diversity and mechanisms of genomic adaptation in Penicillium. In: Aspergillus and Penicillium in the Post-Genomic Era, Ed.; DeVries, R.G., Andersen, M.R., Caister Academic Press: Lyngby, Denmark, pp. 27–42.
44. Ropars, J., Lo, Y.-C., Dumas, E., Snirc, A., Begerow, D., Rollnik, T., Lacoste, S., Dupont, J., Giraud, T., L_opez-Villavicencio, M., (2016b). Fertility depression among cheese-making Penicillium roqueforti strains suggests degeneration during domestication. Evolution 70: 2099e2109. https://doi.org/10.1111/evo.13015
45. Ropars, J., Lopez-Villavicencio, M., Snirc, A., Lacoste, S., Giraud, T., (2017). Blue cheese-making has shaped the population genetic structure of the mould Penicillium roqueforti. PLoS One, 12(3): e0171387. https://doi.org/10.1371/journal.pone.0171387
46. Schaack, S., Gilbert, C., Feschotte, C. (2010). Promiscuous DNA: horizontal transfer of transposable elements and why it matters for eukaryotic evolution. Trends Ecol. Evol., 25(9): 537–546. https://doi.org/10.1016/j.tree.2010.06.001
47. Seri, M. (2020). Konya küflü peynirinden izole edilen küflerin moleküler identifikasyonu ve Penicillium roqueforti izolatlarının morfolojik karakterizasyonu. İstanbul Sabahattin Zaim Üniversitesi, Fen Bilimleri Enstitüsü, Gıda Mühendisliği Anabilim Dalı, Yüksek lisans tezi, İstanbul, 102 s.
48. Şengün, I.Y., Yaman, D.B., Gönül, S.A., (2008). Mycotoxins and mould contamination in cheese: a review. World Mycotoxin Journal, 1(3): 291-298. https://doi.org/10.3920/WMJ2008.x041
49. Visagie, C.M., Houbraken, J., Frisvad, J.C., Hong, S.B., Klaassen, C.H.W., Perrone, G., Seifert, K.A., Varga, J., Yaguchi, T., Samson, R.A., (2014). Identification and nomenclature of the genus Penicillium. Studies in Mycology, 78: 343-371. https://doi.org/10.1016/j.simyco.2014.09.001
50. Yalman, M., Tepeli, S.Ö., Demirel Zorba, N.N. (2016). Türkiye’de geleneksel yöntemlerle üretilen peynirlerin küf florası. Türk Tarım – Gıda Bilim ve Teknoloji Dergisi, 4(11): 926-933.