Applied Microbiology and Biotechnology

, Volume 76, Issue 5, pp 1161–1171 | Cite as

Production of volatile aroma compounds by bacterial strains isolated from different surface-ripened French cheeses

  • Pawinee Deetae
  • Pascal Bonnarme
  • Henry E. SpinnlerEmail author
  • Sandra Helinck
Applied Microbial and Cell Physiology


Twelve bacterial strains belonging to eight taxonomic groups: Brevibacterium linens, Microbacterium foliorum, Arthrobacter arilaitensis, Staphylococcus cohnii, Staphylococcus equorum, Brachybacterium sp., Proteus vulgaris and Psychrobacter sp., isolated from different surface-ripened French cheeses, were investigated for their abilities to generate volatile aroma compounds. Out of 104 volatile compounds, 54 volatile compounds (identified using dynamic headspace technique coupled with gas chromatography-mass spectrometry [GC-MS]) appeared to be produced by the different bacteria on a casamino acid medium. Four out of eight species used in this study: B. linens, M. foliorum, P. vulgaris and Psychrobacter sp. showed a high flavouring potential. Among these four bacterial species, P. vulgaris had the greatest capacity to produce not only the widest varieties but also the highest quantities of volatile compounds having low olfactive thresholds such as sulphur compounds. Branched aldehydes, alcohols and esters were produced in large amounts by P. vulgaris and Psychrobacter sp. showing their capacity to breakdown the branched amino acids. This investigation shows that some common but rarely mentioned bacteria present on the surface of ripened cheeses could play a major role in cheese flavour formation and could be used to produce cheese flavours.


Flavour compounds Ripened cheese Bacteria Sulphur compounds Proteus vulgaris Psychrobacter sp. 



P. Deetae is grateful to the Royal Thai government for a Ph.D. scholarship. A. Helias is gratefully acknowledged for the statistical analysis technique and Chandanie Hunter for reviewing the English language.


  1. Ansede JH, Friedman R, Yoch DC (2001) Phylogenetic analysis of culturable dimethyl sulfide-producing bacteria from a spartina-dominated salt marsh and estuarine water. Appl Environ Microbiol 67:1210–1217CrossRefGoogle Scholar
  2. Ardo Y (2006) Flavour formation by amino acid catabolism. Biotechnol Adv 24:238–242CrossRefGoogle Scholar
  3. Arfi K, Spinnler HE, Tache R, Bonnarme P (2002) Production of volatile compounds by cheese-ripening yeasts: requirement for a methanethiol donor for S-methyl thioacetate synthesis by Kluyveromyces lactis. Appl Microbiol Biotechnol 58:503–510CrossRefGoogle Scholar
  4. Arfi K, Amarita F, Spinnler HE, Bonnarme P (2003) Catabolism of volatile sulfur compounds precursors by Brevibacterium linens and Geotrichum candidum, two microorganisms of the cheese ecosystem. J Biotechnol 105:245–253CrossRefGoogle Scholar
  5. Barbieri G, Bolzoni L, Careri M, Manglia A, Parolari G, Spagnoli S, Virgili R (1994) Study of the volatile fraction of Parmesan cheese. J Agric Food Chem 42:1170–1176CrossRefGoogle Scholar
  6. Beresford TP, Fitzsimons NA, Brennan NL, Cogan TM (2001) Recent advances in cheese microbiology. Int Dairy J 11:259–274CrossRefGoogle Scholar
  7. Bockelmann W, Willems KP, Neve H, Heller KH (2005) Cultures for the ripening of smear cheeses. Int Dairy J 15:719–732CrossRefGoogle Scholar
  8. Bonnarme P, Psoni L, Spinnler HE (2000) Diversity of l-methionine catabolism pathways in cheese-ripening bacteria. Appl Environ Microbiol 66:5514–5517CrossRefGoogle Scholar
  9. Bosset JO, Liardon R (1984) The aroma composition of Gruyère cheese. II. The neutral volatile components. Lebensm-Wiss Technol 17:359–362Google Scholar
  10. Bowman JP, Cavanagh J, Austin JJ, Sanderson K (1996) Novel Psychrobacter species from Antarctic ornithogenic soil. Int J Syst Bacteriol 46:841–848CrossRefGoogle Scholar
  11. Buzzini P, Romano S, Turchetti B, Vaughan A, Pagnoni UM, Davoli P (2005) Production of volatile organic sulfur compounds (VOSCs) by basidiomycetous yeasts. FEMS Yeast Res 5:379–385CrossRefGoogle Scholar
  12. Casey J, Dobb R (1992) Microbial routes to aromatic aldehydes. Enzyme Microb Technol 14:739–747CrossRefGoogle Scholar
  13. Cuer A, Dauphin G, Kergomard A, Dumont JP, Adda J (1979) Production of S-methylthioacetate by Brevibacterium linens. Appl Environ Microbiol 38:332–334Google Scholar
  14. Curioni PMG, Bosset JO (2002) Key odorants in various cheese types as determined by gas chromatography-olfactometry. Int Dairy J 12:959–984CrossRefGoogle Scholar
  15. Demarigny Y, Berger C, Desmasures N, Gueguen M, Spinnler HE (2000) Flavour sulphides are produced from methionine by two different pathways by Geotrichum candidum. J Dairy Res 67:371–380CrossRefGoogle Scholar
  16. Dumont JP, Degas C, Adda J (1976) L’arôme du Camembert: autre composé mineurs mis en évidence. Lait 535–536:243–251Google Scholar
  17. Feurer C, Irlinger F, Spinnler HE, Glaser P, Vallaeys T (2004) Assessment of the rind microbial diversity in a farmhouse-produced vs a pasteurized industrially produced soft red-smear cheese using both cultivation and rDNA-based methods. J Appl Microbiol 97:546–556CrossRefGoogle Scholar
  18. Gallois A, Langlois D (1990) New results in the volatile odorous compounds of French cheese. Lait 70:89–106CrossRefGoogle Scholar
  19. Gonzàles de Llano D, Rodriguez A, Cuesta P (1996) Effect of lactic starter cultures on the organic acid composition of milk and cheese during ripening-analysis by HPLC. J Appl Bacteriol 80:570–576Google Scholar
  20. Helinck S, Spinnler HE, Parayre S, Dame-Cahagne M, Bonnarme P (2000) Enzymatic versus spontaneous S-methyl thioester synthesis in Geotrichum candidum. FEMS Microbiol Lett 193:237–241CrossRefGoogle Scholar
  21. Irlinger F, Bergère J (1999) Use of conventional biochemical tests and analyses of ribotype patterns for classification of micrococci isolated from dairy products. J Dairy Res 66:91–103CrossRefGoogle Scholar
  22. Irlinger F, Morvan A, El-Solh N, Bergère J (1997) Taxonomic characterization of coagulase-negative staphylococci in ripening flora from traditional French cheeses. Syst Appl Microbiol 20:319–328Google Scholar
  23. Jollivet N, Bézenger M-C, Vayssier Y, Belin J-M (1992) Production of volatile compounds in liquid cultures by six strains of coryneform bacteria. Appl Microbiol Biotechnol 36:790–794CrossRefGoogle Scholar
  24. Kagkli DM, Tache R, Cogan TM, Hill C, Casaregola S, Bonnarme P (2006) Kluyveromyces lactis and Saccharomyces cerevisiae, two potent deacidifying and volatile-sulphur-aroma-producing microorganisms of the cheese ecosystem. Appl Microbiol Biotechnol 73:434–442CrossRefGoogle Scholar
  25. Kondjoyan N, Berdagué JL (1996) A compilation of relative retention indices for the analysis of aromatic compounds. Edition du Laboratoire Flaveur. Station de recherche sur la viande, INRA de Theix, Saint Genes Champanelle, France, pp 234Google Scholar
  26. Lamberet G, Auberger B, Bergère JL (1997) Aptitude of cheese bacteria for volatile S-methyl thioester synthesis I. Effect of substrates and pH on their formation by Brevibacterium linens GC171. Appl Microbiol Biotechnol 47:279–283CrossRefGoogle Scholar
  27. Moio L, Dekimpe J, Etievant PX, Addeo F (1993) Volatile flavour compounds of water buffalo mozzarella cheese. Ital J Food Sci 5:57–68Google Scholar
  28. Molimard P, Spinnler HE (1996) Review: compounds involved in the flavor of surface mold-ripened cheeses: origins and properties. J Dairy Sci 79:169–184CrossRefGoogle Scholar
  29. Moller JK, Hinrichsen LL, Andersen HJ (1998) Formation of amino acid (l-leucine, l-phenylalanine) derived volatile flavour compounds by Moraxella phenylpyruvica and Staphylococcus xylosus in cured meat model systems. Int J Food Microbiol 42:101–117CrossRefGoogle Scholar
  30. Monnet C, Correia K, Sarthou AS, Irlinger F (2006) Quantitative detection of Corynebacterium casei in cheese by real-time PCR. Appl Environ Microbiol 72:6972–6979CrossRefGoogle Scholar
  31. Morales P, Fernandez-Garcia E, Nunez M (2005) Production of volatile compounds in cheese by Pseudomonas fragi strains of dairy origin. J Food Prot 68:1399–1407Google Scholar
  32. Prado B, Jara A, Moral AD, Sanchez E (2001) Numerical taxonomy of microorganisms isolated from goat cheese made in Chile. Curr Microbiol 43:396–399CrossRefGoogle Scholar
  33. Reps A (1993) Bacteria surface-ripened cheeses. In: Fox PF (ed) Cheese: chemistry, physics and microbiology, 2nd edn. Chapman & Hall, London, pp 137–172Google Scholar
  34. Roje S (2006) S-Adenosyl-l-methionine: beyond the universal methyl group donor. Phytochemistry 67:1686–1698CrossRefGoogle Scholar
  35. Rychlik M, Bosset JO (2001) Flavour and off-flavour compounds of Swiss Gruyère cheese. Identification of key odorants by quantitative instrumental and sensory studies. Int Dairy J 11:903–910CrossRefGoogle Scholar
  36. Thierry A, Maillard MB, Yvon M (2002) Conversion of l-leucine to isovaleric acid by Propionibacterium freudenreichii TL 34 and ITGP23. Appl Environ Microbiol 68:608–615CrossRefGoogle Scholar
  37. Urbach G (1993) Relation between cheese flavour and chemical composition. Int Dairy J 3:389–422CrossRefGoogle Scholar
  38. Valdes-Stauber N, Scherer S, Seiler H (1997) Identification of yeasts and coryneform bacteria from the surface microflora of brick cheeses. Int J Food Microbiol 34:115–129CrossRefGoogle Scholar
  39. Welsh FW, Murray WD, Williams RE (1989) Microbiological and enzymatic production of flavor and fragrance chemicals. Crit Rev Biotechnol 9:105–169Google Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Pawinee Deetae
    • 1
  • Pascal Bonnarme
    • 1
  • Henry E. Spinnler
    • 1
    Email author
  • Sandra Helinck
    • 1
  1. 1.UMR782 Génie et Microbiologie des Procédés AlimentairesAgroParisTech-INRAThiverval-GrignonFrance

Personalised recommendations