Skip to main content
SpringerLink
Log in

Production of volatile organic compounds (VOCs) by yeasts isolated from the ascocarps of black (Tuber melanosporum Vitt.) and white (Tuber magnatum Pico) truffles

  • Original Paper
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

Twenty-nine yeast strains were isolated from the ascocarps of black and white truffles (Tuber melanosporum Vitt. and Tuber magnatum Pico, respectively), and identified using a polyphasic approach. According to the conventional taxonomic methods, MSP-PCR fingerprinting and sequencing of the D1/D2 domain of 26S rDNA, the strains were identified as Candida saitoana, Debaryomyces hansenii, Cryptococcus sp., Rhodotorula mucilaginosa, and Trichosporon moniliiforme. All isolates assimilated l-methionine as a sole nitrogen source and produced the volatile organic compounds (VOCs), 2-methyl butanol, 3-methyl butanol, methanethiol, S-methyl thioacetate, dimethyl sulfide, dimethyl disulfide, dimethyl trisulfide, dihydro-2-methyl-3(2H)-thiophenone and 3-(methylthio)-1-propanol (MTP). ANOVA analysis of data showed significant (P<0.01) differences in VOCs produced by different yeasts, with MTP as the major component (produced at concentrations ranging from 19.8 to 225.6 mg/l). In addition, since some molecules produced by the isolates of this study are also characteristic of truffle complex aroma, it is possible to hypothesize a complementary role of yeasts associated with this ecosystem in contributing to final Tuber spp. aroma through the independent synthesis of yeast-specific volatile constituents.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Ahmed AA, Mohamed MA, Hami MA (1981) Lybian truffles Terfezia boudieri Chatin: chemical composition and toxicity. J Food Sci 46:927–929

    Article  CAS  Google Scholar 

  • Al-Delaimy KS (1977) Protein and amino acid composition of truffle. Can Inst Food Sci Technol J 10:211–222

    Google Scholar 

  • Aoki T, Uchida K (1991) Enhanced formation of 3-(methylthio)-1-propanol in a salt-tolerant yeast, Zygosaccharomyces rouxii, due to deficiency of S-adenosylmethionine synthase. Agric Biol Chem 55:2113–2116

    CAS  Google Scholar 

  • Arfi K, Tâche R, Spinnler HE, Bonnarme P (2003) Dual influence of the carbon source and l-methionine on the synthesis of sulfur compounds in the cheese-ripening yeast Geotrichum candidum. Appl Microbiol Biotechnol 61:359–365

    PubMed  CAS  Google Scholar 

  • Bacilio-Jimenez M, Aguilar-Flores S, Ventura-Zapata E, Pérez-Campos E, Bouquelet S, Zenteno E (2003) Chemical characterization of root exudates from rice (Oryza sativa) and their effect on the chemotactic response of endophytic bacteria. Plant Soil 249:271–277

    Article  CAS  Google Scholar 

  • Berger C, Khan JA, Molimard P, Martin N, Spinnler HE (1999) Production of sulfur flavours by ten strains of Geotrichum candidum. Appl Environm Microbiol 65:5510–5514

    CAS  Google Scholar 

  • Bokhary HA, Parvez S (1993) Chemical composition of desert truffles Terfezia claveryi. J Food Comp Anal 6:285–293

    Article  CAS  Google Scholar 

  • Bonnarme P, Arfi K, Dury C, Helinck S, Yvon M, Spinnler HE (2001a) Sulfur compound production by Geotrichum candidum from l-methionine: importance of the transaminase step. FEMS Microbiol Lett 205:247–252

    Article  PubMed  CAS  Google Scholar 

  • Bonnarme P, Lapadatescu C, Yvon M, Spinnler HE (2001b) l-methionine: degradation potentiality of cheese-ripening microorganisms. J Dairy Res 68:663–674

    Article  PubMed  CAS  Google Scholar 

  • Buzzini P, Martini A, Cappelli F, Pagnoni UM, Davoli P (2003a) A study on volatile organic compounds (VOCs) produced by tropical ascomycetous yeasts. Antonie van Leeuwenhoek 84:301–311

    Article  PubMed  CAS  Google Scholar 

  • Buzzini P, Martini A, Pagnoni UM, Davoli P (2003b) Production of flavored volatile organic compounds (VOCs) by Candida oleophila GK10. Optimization using factorial design and response surface analysis. Enzyme Microb Technol 33:668–675

    Article  CAS  Google Scholar 

  • 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 5:379–385

    Article  PubMed  CAS  Google Scholar 

  • Chin HW, Lindsay RC (1994) Ascorbate and transition-metal mediation of methanethiol oxidation to dimethyl disulfide and dimethyl trisulfide. Food Chem 49:387–392

    Article  CAS  Google Scholar 

  • Cheetham PJS (1997) Combining the technical push and business pull for natural flavours. Adv Biochem Eng Biotechnol 55:1–49

    CAS  Google Scholar 

  • Coli R, Maurizi Coli A, Granetti B, Damiani P (1990) Chemical composition and nutritive value of black truffle (Tuber melanosporum Vitt.) and white truffle (Tuber magnatum Pico) collected in Umbria (Italy). Proc II Int Congr on Truffles, Spoleto (Italy), CM MMS, Perugia (Italy), pp511–516

  • Dakora FD, Phillips DA (2002) Root exudates as mediators of mineral acquisition in low nutrient environments. Plant Soil 245:35–47

    Article  CAS  Google Scholar 

  • Diriye FU, Scorzetti G, Martini A (1993) Methods for the separation of yeast cells from the surfaces of processed frozen foods. Int J Food Microbiol 19:27–30

    Article  PubMed  CAS  Google Scholar 

  • Duponnois R, Garbaye J (1990) Some mechanisms involved in growth stimulation of ectomycorrhizal fungi by bacteria. Can J Bot 68:2148–2152

    Google Scholar 

  • Endrizzi A, Pagot Y, Le Clainche A, Nicaud JM, Belin JM (1996) Production of lactones and peroxisomal beta-oxidation in yeasts. Crit Rev Biotechnol 16:301–329

    Article  PubMed  CAS  Google Scholar 

  • Frey-Klett P, Churin JL, Pierrat JC, Garbaye J (1999) Dose effect in the dual inoculation of an ectomycorrhizal fungus and a mycorrhiza helper bacterium in two forest nurseries. Soil Biol Biochem 31:1555–1562

    Article  CAS  Google Scholar 

  • Garbaye J (1994) Helper bacteria: a new dimension to the mycorrhizal symbiosis. New Phytol 128:197–210

    Article  Google Scholar 

  • Garbaye J, Bowen GD (1989) Stimulation of ectomycorrhizal infection of Pinus radiata by microorganisms associated with the mantle of ectomycorrhizas. New Phytol 112:383–388

    Article  Google Scholar 

  • 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 193:237–241

    Article  PubMed  CAS  Google Scholar 

  • Jaeger CH III, Lindow SE, Miller W, Clark E, Firestone MK (1999) Mapping of sugar and amino acid availability in soil around roots with bacterial sensors of sucrose and tryptophan. Appl Environm Microbiol 65:2585–2690

    Google Scholar 

  • Lipson DA, Raab TK, Schmidt SK, Monson RK (2001) An empirical model of amino acid transformation in an alpine soil. Soil Biol Biochem 33:189–198

    Article  CAS  Google Scholar 

  • Marletto F (1969) La microflora della rizosfera delle tartufaie. I. I blastomiceti dei tartufi e della rizosfera delle tartufaie. Allionia 15:155–171

    Google Scholar 

  • Martin N, Berger C, Le Du C, Spinnler HE (2001) Aroma compounds production in cheese curd by co-culturing with selected yeasts and bacteria. J Dairy Sci 84:2125–2135

    Article  PubMed  CAS  Google Scholar 

  • Mestres M, Busto O, Guasch J (2000) Analysis of organic sulfur compounds in wine aroma. J Chromatrogr 881:569–581

    Article  CAS  Google Scholar 

  • Meyer W, Mitchell TG, Freedman EZ, Vilgalys R (1993) Hybridization probes for conventional DNA fingerprinting used as single primers in the polymerase chain reaction to distinguish strains of Cryptococcus neoformans. J Clin Microbiol 31:2274–2280

    PubMed  CAS  Google Scholar 

  • Moreira N, Mendes F, Pereira O, Guedes de Pinho P, Hogg T, Vasconcelos I (2002) Volatile sulphur compounds in wines related to yeast metabolism and nitrogen composition of grape musts. Anal Chim Acta 458:157–167

    Article  CAS  Google Scholar 

  • Murcia MA, Martinez-Tomé M, Vera A, Morte A, Gutierrez A, Honrubia M, Jimenez AM (2003) Effect of industrial processing on dessert truffles Terfezia claveryi Chatin and Picoa juniperii Vittadini: proximate composition and fatty acids. J Sci Food Agric 83:535–541

    Article  CAS  Google Scholar 

  • Ozino Marletto O, Sartoris A (1978) Studi sull’ecologia del Tuber melanosporum. V. La blastoflora delle aree bruciate nell’Italia centrale. Allionia 23:91–94

    Google Scholar 

  • Pelusio F, Nilsson T, Montanarella L, Tilio R, Larsen B, Facchetti S, Madsen JO (1995) Headspace solid-phase microextraction analysis of volatile organic sulfur compounds in black and white truffle aroma. J Agric Food Chem 43:2138–2143

    Article  CAS  Google Scholar 

  • Phaff HJ, Starmer WT (1987) Yeasts associated with plants, insects and soils. In: Rose AH, Harrison JS (eds) The Yeasts. Academic , London, pp.123–180

    Google Scholar 

  • Read D (1991) Mycorrhizas in ecosystems. Experimentia 47:376–391

    Article  Google Scholar 

  • Rojas V, Gil JG, Pinaga F, Manzanares P (2001) Studies on acetate ester production by non-Saccharomyces wine yeasts. Int J Food Microbiol 70:283–289

    Article  PubMed  CAS  Google Scholar 

  • Romano P, Suzzi G, Domizio P, Fatichenti F (1997) Secondary products formation as a tool for discriminating non-Saccharomyces wine strains. Antonie van Leeuwenhoek 71:239–242

    Article  PubMed  CAS  Google Scholar 

  • Rovira AD (1969) Plant root exudates. Bot Rev 35:35–57

    CAS  Google Scholar 

  • Sampaio JP, Gadanho M, Santos S, Duarte F, Pais C, Fonseca A, Fell JW (2001) Polyphasic taxonomy of the basisdiomycetous yeast genus Rhodosporidium: Rhodosporidium kratochvilovae and related anamorphic species. Int J Syst Evol Microbiol 51:687–697

    PubMed  CAS  Google Scholar 

  • Schreier P, Drawert F, Junker A, Barton H, Leupold G (1976) Biosynthesis of aroma compounds by microorganisms. II. Formation of sulfur compounds from methionine by Saccharomyces cerevisiae. Zeitschrift fuer Lebensmittel-Untersuchung und Forschung 162:279–284

    Article  CAS  Google Scholar 

  • Spinnler HE, Berger C, Lapadatescu C, Bonnarme P (2001) Production of sulfur compounds by several yeasts of technological interest for cheese ripening. Int Dairy J 11:245–252

    Article  CAS  Google Scholar 

  • Torner MJ, Martinez-Anaya MA, Antuna B, Benedito de Barber C (1992) Headspace flavour compounds produced by yeasts and lactobacilli during fermentation of preferments and bread doughs. Int J Food Microbiol 15:145–152

    Article  PubMed  CAS  Google Scholar 

  • Wache Y, Aguedo M, Choquet A, Gatfield IL, Nicaud JM, Belin JM (2001) Role of beta-oxidation enzymes in gamma-decalactone production by the yeast Yarrowia lipolytica. Appl Environ Microbiol 67:5700–5704

    Article  PubMed  CAS  Google Scholar 

  • Yang Mei C (2001) Truffles in Southwest China. Proc V Int Congr on Truffles, Aix-en-Provance (France), FFT IPSO, Marseille (France), pp248–249

  • Yarrow D (1998) Methods for the isolation, maintenance and identification of yeasts. In: CP Kurtzman JW Fell (eds), The yeasts. A taxonomic study. Elsevier, Amsterdam, pp 77–100

    Google Scholar 

  • Zacchi L, Vaughan-Martini A, Angelini P (2003) Yeast distribution in a truffle-field ecosystem. Ann Microbiol 53:275–282

    Google Scholar 

Download references

Acknowledgements

Authors are grateful to Prof. I. Spencer-Martins and to Dr. Gabriella Giménez Jurado of the Centro de Recursos Microbiológicos (CREM), Secção Autónoma de Biotecnologia, Faculdade de Ciências e Tecnologia, Universidade Nova de Lisboa (Portugal) for the their technical assistance in the course of molecular identification, and to M. Milito for her appreciable work in the course of this study.

Author information

Authors and Affiliations

  1. Dipartimento di Biologia Vegetale e Biotecnologie Agroambientali, Sezione di Microbiologia Applicata, Università di Perugia, Borgo XX Giugno 74, 06121, Perugia, Italy

    Pietro Buzzini, Chiara Gasparetti, Benedetta Turchetti, Ann Vaughan-Martini & Alessandro Martini

  2. Dipartimento di Chimica, Università di Modena e Reggio Emilia, via Campi 183, 41100, Modena, Italy

    Maria Rita Cramarossa, Ugo Maria Pagnoni & Luca Forti

Authors
  1. Pietro Buzzini
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chiara Gasparetti
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Benedetta Turchetti
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Maria Rita Cramarossa
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ann Vaughan-Martini
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Alessandro Martini
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ugo Maria Pagnoni
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Luca Forti
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Pietro Buzzini.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Buzzini, P., Gasparetti, C., Turchetti, B. et al. Production of volatile organic compounds (VOCs) by yeasts isolated from the ascocarps of black (Tuber melanosporum Vitt.) and white (Tuber magnatum Pico) truffles. Arch Microbiol 184, 187–193 (2005). https://doi.org/10.1007/s00203-005-0043-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00203-005-0043-y

Keywords

Search

Navigation