Abstract
To generate a comprehensive profile of viable fungi (yeasts and molds) on cheese as it is purchased by consumers, 44 types of cheese were obtained from a local grocery store from 1 to 4 times each (depending on availability) and sampled. Pure cultures were obtained and identified by DNA sequence of the ITS region, as well as growth characteristics and colony morphology. The yeast Debaryomyces hansenii was the most abundant fungus, present in 79 % of all cheeses and 63 % of all samples. Penicillium roqueforti was the most common mold, isolated from a variety of cheeses in addition to the blue cheeses. Eighteen other fungal species were isolated, ten from only one sample each. Most fungi isolated have been documented from dairy products; a few raise potential food safety concerns (i.e. Aspergillus flavus, isolated from a single sample and capable of producing aflatoxins; and Candida parapsilosis, an emerging human pathogen isolated from three cheeses). With the exception of D. hansenii (present in most cheese) and P. roqueforti (a necessary component of blue cheese), no strong correlation was observed between cheese type, manufacturer, or sampling time with the yeast or mold species composition.
Similar content being viewed by others
References
Abarca ML, Bragulat MR, Castellá G, Cabañes FJ (1994) Ochratoxin A production by strains of Aspergillus niger var. niger. Appl Environ Microbiol 60:2650–2652
Atanassova M, Choiset Y, Dalgalarrondo M, Chobert JM, Dousset X, Ivanova I (2003) Isolation and partial biochemical characterization of a proteinaceous anti-bacteria and anti-yeast compound produced by Lactobacillus paracasei subsp. paracasei strain M3. Int J Food Microbiol 87:63–73
Beresford TP, Fitzsimons N, Brennan NL, Cogan TM (2001) Recent advances in cheese microbiology. Int Dairy J 11:259–274
Bintsis T, Papademas P (2002) Microbiological quality of white-brined cheeses: a review. Int J Dairy Tech 55:113–120
Borelli BM, Ferreira EG, Lacerda ICA, Franco GR, Rosa CA (2006) Yeast populations associated with the artisanal cheese produced in the region of Serra da Canastra, Brazil. World J Microbiol Biotechnol 22:1115–1119
Bourdichon F, Casaregola S, Farrokh C, Frisvad JC, Gerds ML, Hammes WP et al (2012) Food fermentations: microorganisms with technological beneficial use. Int J Food Microbiol 154:87–97
Boysen M, Skouboe P, Frisvad J, Rossen L (1996) Reclassification of the Penicillium roqueforti group into three species on the basis of molecular genetic and biochemical profiles. Microbiology 142:541–549
Breuer U, Harms H (2006) Debaryomyces hansenii— an extremophilic yeast with biotechnological potential. Yeast 23:415–437
Creppy EE (2002) Update of survey, regulation and toxic effects of mycotoxins in Europe. Toxicol Lett 127:19–28
De Freitas I, Pinon N, Berdagué J, Tournayre P, Lortal S, Thierry A (2008) Kluyveromyces lactis but not Pichia fermentans used as adjunct culture modifies the olfactory profiles of cantalet cheese. J Dairy Sci 91:531–543
El-Sharoud WM, Belloch C, Peris D, Querol A (2009) Molecular identification of yeasts associated with traditional Egyptian dairy products. J Food Sci 74:M1–M6
Fox PF, McSweeney PLH (2004) Cheese: an overview. In: Fox PF, McSweeney PLH, Cogan TM, Guinee TP (eds) Cheese: chemistry, physics and microbiology, vol 1, 3rd edn. Elsevier Academic Press, Amsterdam, pp 1–18
Gadaga TH, Mutukumira AN, Narvhus JA (2000) Enumeration and identification of yeasts isolated from Zimbabwean traditional fermented milk. Int Dairy J 10:459–466
Gardes M, Bruns TD (1993) ITS primers with enhances specifocity for basidiomycetes - application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118
Gori K, Sorensen LM, Petersen MA, Jespersen L, Arneborg N (2012) Debaryomyces hansenii strains differ in their production of flavor compounds in a cheese-surface model. MicrobiologyOpen 1:161–168
Haasum I, Nielsen PV (1998) Physiological characterization of common fungi associated with cheese. J Food Sci 63:157–161
Harju S, Fedosyuk H, Peterson KR (2004) Rapid isolation of yeast genomic DNA: Bust n’ grab. BMC Biotechnol 4:8
Hayaloglu AA, Kirbag S (2007) Microbial quality and presence of moulds in Kuflu cheese. Int J Food Microbiol 115:376–380
Hocking AD, Faedo M (1992) Fungi causing thread mold spoilage of vacuum packaged Cheddar cheese during maturation. Int J Food Microbiol 16:123–130
Houbraken J, Frisvad JC, Samson RA (2010) Sex in Penicillium series roqueforti. IMA Fungus 1:171–180
Irlinger F, Mounier J (2009) Microbial interactions in cheese: implications for cheese quality and safety. Curr Opin Biotechnol 20:142–148
Jacques N, Casaregola S (2008) Safety assessment of dairy microorganisms: the hemiascomycetous yeasts. Int J Food Microbiol 126:321–326
Jakobsen M, Narvhus J (1996) Yeasts and their possible beneficial and negative effects on the quality of dairy products. Int Dairy J 6:755–768
Kindstedt PS (2013) The basics of cheesemaking. Microbiol Spectr 1:CM-0002–CM-0012
Kõljag U, Nilsson RH, Abarenkov K, Tedersoo L, Taylor AFS, Bahram M et al (2013) Towards a unified paradigm for sequence-based identification of fungi. Mol Ecol 22:5271–5277
Kure CF, Wasteson Y, Brendehaug J, Skaar I (2001) Mould contaminants on Jarlsberg and Norvegia cheese blocks from four factories. Int J Food Microbiol 70:21–27
Larsen TO, Gareis M, Frisvad JC (2002) Cell cytotoxicity and mycotoxin and secondary metabolite production by common Penicillia on cheese agar. J Agric Food Chem 50:6148–6152
Lavoie K, Touchette M, St-Gelais D, Labrie S (2012) Characterization of the fungal microflora in raw milk and specialty cheeses of the province of Quebec. Dairy Sci Technol 92:455–468
Lie JL, Marth EH (1967) Formation of aflatoxin in cheddar cheese by Aspergillus flavus and Aspergillus parasiticus. J Dairy Sci 50:1708–1710
Lund F, Filtenborg O, Frisvad JC (1995) Associated mycoflora of cheese. Food Microbiol 12:173–180
Lund F, Nielsen AB, Skouboe P (2003) Distribution of Penicillium commune isolates in cheese dairies mapped using secondary metabolite profiles, morphotypes, RAPD and AFLP fingerprinting. Food Microbiol 20:725–734
Marcellino N, Benson (2013) The good, the bad and the ugly: tales of mold-ripened cheese. Microbiol Spectr 1:CM-0005–CM-0012
Moran G, Coleman D, Sullivan D (2012) An introduction to the medically important Candida species. In: Calderone RA, Clancy CJ (eds) Candida and candidiasis, 2nd edn. ASM Press, New York, pp 11–25
Mounier J, Goerges S, Gelsomino R, Vancanneyt M, Vandemeulebroecke K, Hoste B et al (2006) Sources of the adventitious microflora of a smear-ripened cheese. J Appl Microbiol 101:668–681
Mounier J, Monnet C, Vallaeys T, Arditi R, Sarthou AS, Helias A, Irlinger F (2008) Microbial interactions within a cheese microbial community. Appl Environ Microbiol 74:172–181
Nielsen KF, Dalsgaard PW, Smedsgaard J, Larsen TO (2005) Andrastins A-D, Penicillium roqueforti metabolites consistently produced in blue-mold-ripened cheese. J Agric Food Chem 53:2908–2913
O’Brien NM, O’Connor TP, O’Callaghan JO, Dobson ADW (2004) Toxins in cheese. In: Fox PE, McSweeney PLH, Cogan TM, Guinee TP (eds) Cheese: Chemistry, Physics and Microbiology, vol 1, 3rd edn. Elsevier Academic Press, Amsterdam, pp 562–571
Ogier JC, Son O, Gruss A, Tailliez P, Delacroix-Buchet A (2002) Identification of the bacterial microflora in dairy products by temporal temperature gradient gel electrophoresis. Appl Environ Microbiol 68:3691–3701
Pereira-Dias S, Potes ME, Marinho A, Malfeito-Ferreira M, Loureiro V (2000) Characterisation of yeast flora isolated from an artisanal Portuguese ewes’ cheese. Int J Food Microbiol 60:55–63
Pitkin JW, Panaccione DG, Walton JD (1996) A putative cyclic peptide efflux pump encoded by the TOXA gene of the plant-pathogenic fungus Cochliobolus carbonum. Microbiology 142:1557–1565
Pitt JI, Cruickshank RH, Leistner L (1986) Penicillium commune, P. camembertii, the origin of white cheese moulds, and the production of cyclopiazonic acid. Food Microbiol 3:363–371
Pitt JI, Hocking AD (2009) Fungi and food spoilage, 3rd edn. Springer, New York, p 519
Sengun IY, Yaman DB, Gonul SA (2008) Mycotoxins and mould contamination in cheese: a review. World Mycotoxin J 1:291–298
Suzzi G, Schirone M, Martuscelli M, Gatti M, Fornasari ME, Neviana E (2003) Yeasts associated with Manteca. FEMS Yeast Res 3:159–166
Swearingen PA, O’Sullivan DJ, Warthesen JJ (2001) Isolation, characterization, and influence of native, nonstarter lactic acid bacteria on cheddar cheese quality. J Dairy Sci 84:50–59
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729
Torkar KG, Teger SG (2006) The presence of some pathogen micro organisms, yeasts and moulds in cheese samples produced at small dairy-processing plants. Acta Agric Slov 88:37–51
Trofa D, Gacser A, Nosanchuk JD (2008) Candida parapsilosis, an emerging fungal pathogen. Clin Microbiol Rev 21:606–625
Tsai WJ, Liewen MB, Bullerman LB (1988) Toxicity and sorbate sensitivity of molds isolated from surplus commodity cheeses. J Food Prot 51:457–462
Vasdinyei R, Deák T (2003) Characterization of yeast isolates originating from hungarian dairy products using traditional and molecular identification techniques. Int J Food Microbiol 86:123–130
Wanderley L, Bianchin A, Arruda Teo CRP, Meneghello Fuentefria A (2013) Occurrence and pathogenicity of Candida spp. in unpasteurized cheese. Braz J Biosci 11:145–148
Welthagen JJ, Viljoen BC (1998) Yeast profile in gouda cheese during processing and ripening. Int J Food Microbiol 41:185–194
White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, San Diego, pp 315–322
Wolfe BE, Button JE, Santarelli M, Dutton RJ (2014) Cheese rind communities provide tractable systems for in situ and in vitro studies of microbial diversity. Cell 158:422–433
Wyder M-T, Puhan Z (1999) Investigation in the yeast flora in smear ripened cheeses. Milchwissenschaft 54:330–333
Acknowledgments
This work was supported by the USDA National Institute of Food and Agriculture Hatch Project NEB-31-136. We thank Dr. Robert Hutkins for reviewing this manuscript.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Banjara, N., Suhr, M.J. & Hallen-Adams, H.E. Diversity of Yeast and Mold Species from a Variety of Cheese Types. Curr Microbiol 70, 792–800 (2015). https://doi.org/10.1007/s00284-015-0790-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00284-015-0790-1