Skip to main content
Log in

Diversity of Yeast and Mold Species from a Variety of Cheese Types

  • Published:
Current Microbiology Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. 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

    PubMed Central  CAS  PubMed  Google Scholar 

  2. 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

    Article  CAS  PubMed  Google Scholar 

  3. Beresford TP, Fitzsimons N, Brennan NL, Cogan TM (2001) Recent advances in cheese microbiology. Int Dairy J 11:259–274

    Article  CAS  Google Scholar 

  4. Bintsis T, Papademas P (2002) Microbiological quality of white-brined cheeses: a review. Int J Dairy Tech 55:113–120

    Article  Google Scholar 

  5. 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

    Article  CAS  Google Scholar 

  6. 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

    Article  CAS  PubMed  Google Scholar 

  7. 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

    Article  CAS  PubMed  Google Scholar 

  8. Breuer U, Harms H (2006) Debaryomyces hansenii— an extremophilic yeast with biotechnological potential. Yeast 23:415–437

    Article  CAS  PubMed  Google Scholar 

  9. Creppy EE (2002) Update of survey, regulation and toxic effects of mycotoxins in Europe. Toxicol Lett 127:19–28

    Article  CAS  PubMed  Google Scholar 

  10. 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

    Article  PubMed  Google Scholar 

  11. 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

    Article  Google Scholar 

  12. 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

    Chapter  Google Scholar 

  13. Gadaga TH, Mutukumira AN, Narvhus JA (2000) Enumeration and identification of yeasts isolated from Zimbabwean traditional fermented milk. Int Dairy J 10:459–466

    Article  Google Scholar 

  14. 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

    Article  CAS  PubMed  Google Scholar 

  15. 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  16. Haasum I, Nielsen PV (1998) Physiological characterization of common fungi associated with cheese. J Food Sci 63:157–161

    Article  CAS  Google Scholar 

  17. Harju S, Fedosyuk H, Peterson KR (2004) Rapid isolation of yeast genomic DNA: Bust n’ grab. BMC Biotechnol 4:8

    Article  PubMed Central  PubMed  Google Scholar 

  18. Hayaloglu AA, Kirbag S (2007) Microbial quality and presence of moulds in Kuflu cheese. Int J Food Microbiol 115:376–380

    Article  CAS  PubMed  Google Scholar 

  19. Hocking AD, Faedo M (1992) Fungi causing thread mold spoilage of vacuum packaged Cheddar cheese during maturation. Int J Food Microbiol 16:123–130

    Article  CAS  PubMed  Google Scholar 

  20. Houbraken J, Frisvad JC, Samson RA (2010) Sex in Penicillium series roqueforti. IMA Fungus 1:171–180

    Article  PubMed Central  PubMed  Google Scholar 

  21. Irlinger F, Mounier J (2009) Microbial interactions in cheese: implications for cheese quality and safety. Curr Opin Biotechnol 20:142–148

    Article  CAS  PubMed  Google Scholar 

  22. Jacques N, Casaregola S (2008) Safety assessment of dairy microorganisms: the hemiascomycetous yeasts. Int J Food Microbiol 126:321–326

    Article  CAS  PubMed  Google Scholar 

  23. 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

    Article  Google Scholar 

  24. Kindstedt PS (2013) The basics of cheesemaking. Microbiol Spectr 1:CM-0002–CM-0012

    Article  Google Scholar 

  25. 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

    Article  Google Scholar 

  26. 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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  28. 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  29. Lie JL, Marth EH (1967) Formation of aflatoxin in cheddar cheese by Aspergillus flavus and Aspergillus parasiticus. J Dairy Sci 50:1708–1710

    Article  CAS  PubMed  Google Scholar 

  30. Lund F, Filtenborg O, Frisvad JC (1995) Associated mycoflora of cheese. Food Microbiol 12:173–180

    Article  Google Scholar 

  31. 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

    Article  CAS  Google Scholar 

  32. Marcellino N, Benson (2013) The good, the bad and the ugly: tales of mold-ripened cheese. Microbiol Spectr 1:CM-0005–CM-0012

    Google Scholar 

  33. 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

    Google Scholar 

  34. 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

    Article  CAS  PubMed  Google Scholar 

  35. 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  36. 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

    Article  CAS  PubMed  Google Scholar 

  37. 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

    Google Scholar 

  38. 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  39. 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

    Article  CAS  PubMed  Google Scholar 

  40. 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

    Article  CAS  PubMed  Google Scholar 

  41. 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

    Article  CAS  Google Scholar 

  42. Pitt JI, Hocking AD (2009) Fungi and food spoilage, 3rd edn. Springer, New York, p 519

    Book  Google Scholar 

  43. Sengun IY, Yaman DB, Gonul SA (2008) Mycotoxins and mould contamination in cheese: a review. World Mycotoxin J 1:291–298

    Article  CAS  Google Scholar 

  44. Suzzi G, Schirone M, Martuscelli M, Gatti M, Fornasari ME, Neviana E (2003) Yeasts associated with Manteca. FEMS Yeast Res 3:159–166

    Article  CAS  PubMed  Google Scholar 

  45. 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

    Article  CAS  PubMed  Google Scholar 

  46. 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  47. 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

    Google Scholar 

  48. Trofa D, Gacser A, Nosanchuk JD (2008) Candida parapsilosis, an emerging fungal pathogen. Clin Microbiol Rev 21:606–625

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  49. Tsai WJ, Liewen MB, Bullerman LB (1988) Toxicity and sorbate sensitivity of molds isolated from surplus commodity cheeses. J Food Prot 51:457–462

    Google Scholar 

  50. 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

    Article  CAS  PubMed  Google Scholar 

  51. 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

    Google Scholar 

  52. Welthagen JJ, Viljoen BC (1998) Yeast profile in gouda cheese during processing and ripening. Int J Food Microbiol 41:185–194

    Article  CAS  PubMed  Google Scholar 

  53. 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

    Chapter  Google Scholar 

  54. 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

    Article  CAS  PubMed  Google Scholar 

  55. Wyder M-T, Puhan Z (1999) Investigation in the yeast flora in smear ripened cheeses. Milchwissenschaft 54:330–333

    CAS  Google Scholar 

Download references

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

Authors

Corresponding author

Correspondence to Heather E. Hallen-Adams.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00284-015-0790-1

Keywords

Navigation