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Survey of viable airborne fungi in wine cellars of Tokaj, Hungary

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Abstract

The composition of fungal biota and air quality of five traditional subterranean wine cellars and one store building of a modern wine production facility were examined in the Tokaj wine region (northeastern Hungary). Air samples were collected with SAS IAQ sampler onto PDA, MEA and RBA. Strains representing morphotypes were isolated from colonies formed on agar plates from either air or surface samples. The internal transcribed spacer (ITS) region of the rRNA gene cluster was amplified with primers ITS1 and ITS4. Altogether 90 morphotypes were isolated, 48 and 12 strains (43 species) from the air and surfaces, respectively. The number of spore-forming species generated high diversity of indoor fungi and differences between the cellars’ fungal compositions; however, their dominant species were proved to be the same. Among the isolated strains Penicillium spp. were the most frequent. The walls of cellars were covered by colonies of Zasmidium (Cladosporium) cellare often referred to as a noble mold. Even so, this mold has been found only at a small concentration in the air samples (10–30 CFU/m3). The walls of the modern store were free of molds. Diversity of fungi of the examined wine cellars was influenced by environmental conditions to a certain degree, such as elevation (height above sea level), age, reconstruction time of cellars, indoor ethanol concentration and the number of chimneys. The location of cellars poorly influenced the concentration of fungi of the air inside cellars, contrary to outdoors where the air of the municipal area contained more CFUs than that of rural spaces.

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References

  • Askew, D. J., & Laing, M. D. (1993). An adapted selective medium for the quantitative isolation of Trichoderma species. Plant Pathology, 42(5), 686–690.

    Article  Google Scholar 

  • Boatto, V., Defrancesco, E., & Trestini, S. (2011). The price premium for wine quality signals: does retailers’ information provision matter? British Food Journal, 113(4–5), 669–679.

    Article  Google Scholar 

  • Cañas, I., & Ocaña, S. M. (2005). Study of the thermal behaviour of traditional wine cellars: the case of the area of “Tierras Sorianas del Cid” (Spain). Renewable Energy, 30(1), 43–55.

    Article  Google Scholar 

  • Clemenz, A., Sterflinger, K., Kneifel, W., & Mandl, K. (2008). Airborne fungal microflora of selected types of wine-cellars in Austria. Mitteilungen Klosterneuburg, 58, 17–22.

    Google Scholar 

  • Day, J. H., & Ellis, A. K. (2001). Allergenic microorganisms and hypersensitivity. In B. Flannigan, R. A. Samson, & J. D. Miller (Eds.), Microorganisms in Home and Indoor Work Environments. Diversity, Health Impacts, Investigation and Control. Boca Raton, London, New York: CRC Press, Taylor & Francis Group.

    Google Scholar 

  • Douwes, J., Thorne, P., Pearce, N., & Heederik, D. (2003). Bioaerosol health effects and exposure assessment: progress and prospects. Annals of Occupational Hygiene, 47, 187–200.

    CAS  Google Scholar 

  • Ewaze, J. O., Summerbell, R. C., & Scott, J. A. (2008). Ethanol physiology in the warehouse-staining fungus. Baudoinia compniacensis. Mycological Research, 112(11), 1373–1380.

    Article  CAS  Google Scholar 

  • Fiedler, K., Schütz, E., & Geh, S. (2001). Detection of microbial volatile organic compounds (MVOCs) produced by moulds on various materials. International Journal of Hygiene and Environmental Health, 204(2–3), 111–121.

    Article  CAS  Google Scholar 

  • Flannigan, B., Samson, R. A., & Miller, J. D. (2011). Microorganisms in home and indoor work environments. Diversity, health impacts, investigation and control (2nd ed.). Boca Raton, London, New York: CRC Press, Taylor & Francis Group.

    Google Scholar 

  • Fung, F., & Hughson, W. G. (2003). Health effects of indoor fungal bioaerosol exposure. Applied Occupational and Environmental Hygiene, 18(7), 535–544.

    Article  Google Scholar 

  • Gašinec, J., Rákay, Š., Rákay, Š., & Šimčak, M. (2012). Geodetic survey of tuff wine cellars in Vel’ka Tŕňa. Acta Montanistica Slovaca, 17(3), 189–194.

    Google Scholar 

  • Goodwin, S. B., McCorison, C. B., Cavaletto, J. R., Culley, D. E., LaButti, K., Baker, S. E., et al. (2016). The mitochondrial genome of the ethanol-metabolizing, wine cellar mold Zasmidium cellare is the smallest for a filamentous ascomycete. Fungal Biology, 120(8), 961–974.

    Article  CAS  Google Scholar 

  • Goto, S., Takayama, K., & Shinohara, T. (1989). Occurence of molds in wine storage cellars. Journal of Fermentation and Bioengineering, 68(4), 230–232.

    Article  Google Scholar 

  • Haas, D., Galler, H., Habib, J., Melkes, A., Schlacher, R., Buzina, W., et al. (2010). Concentrations of viable airborne fungal spores and trichloroanisole in wine cellars. International Journal of Food Microbiology, 144(1), 126–132.

    Article  CAS  Google Scholar 

  • Klich, M. A. (2002). Identification of common Aspergillus species. Utrecht: Centraalbureau voor Schimmelcultures.

    Google Scholar 

  • La Guerche, S., Chamont, S., Blancard, D., Dubourdieu, D., & Darriet, P. (2005). Origin of (−)-geosmin on grapes: on the complementary action of two fungi, Botrytis cinerea and Penicillium expansum. Antonie van Leeuwenhoek, 88(2), 131–139.

    Article  Google Scholar 

  • Macher, J. M. (1989). Positive-hole correction of multiple-jet impactors for collecting viable microorganisms. The American Industrial Hygiene Association Journal, 50(11), 561–568.

    Article  CAS  Google Scholar 

  • Magyar, I., & Bene, Z. (2006). Morphological and taxonomic study on mycobiota of noble rotted grapes in the Tokaj wine district. Acta Alimentaria, 35(2), 237–246.

    Article  Google Scholar 

  • Magyar, D., Eszéki, E. R., Oros, G., Szécsi, Á., Kredics, L., Hatvani, L., et al. (2011). The air spora of an orchid greenhouse. Aerobiologia, 27(2), 121–134.

    Article  Google Scholar 

  • Magyar, D., & Oros, G. (2012). Application of the Principal Component Analysis to disclose factors influencing on the composition of fungal consortia deteriorating remained fruit stalks on sour cherry trees. In P. Sanguansat (Ed.), Principal Component Analysis - Multidisciplinary Applications (pp. 89–110). Rijeka: InTech.

    Google Scholar 

  • Magyar, I., & Tóth, T. (2011). Comparative evaluation of some oenological properties in wine strains of Candida stellata, Candida zemplinina, Saccharomyces uvarum and Saccharomyces cerevisiae. Food Microbiology, 28(1), 94–100.

    Article  CAS  Google Scholar 

  • Magyar, D., Vass, M., & Li, D. W. (2016). Dispersal strategies of microfungi. In Biology of Microfungi (pp. 315–371). Springer International Publishing.

  • Makra, L., Vitányi, B., Gál, A., Mika, J., Matyasovszky, I., & Hirsch, T. (2009). Wine quantity and quality variations in relation to climatic factors in the Tokaj (Hungary) winegrowing region. American Journal of Enology and Viticulture, 60(3), 312–321.

    Google Scholar 

  • Malaktou, E., Philokyprou, M., Michael, A., & Savvides, A. (2016). Thermal assessment of traditional, partially subterranean dwellings in coastal and mountainous regions in the Mediterranean climate. The case of Cyprus. Journal of Sustainable Architecture and Civil Engineering, 16(3), 82–96.

    Article  Google Scholar 

  • Mason, E. W. (1937). Annotated account of fungi received at the Imperial Mycological Institute. (List II, Fasc.3-General part) Kew Surrey: IMI.

  • Mazarrón, F. R., & Cañas, I. (2009). Seasonal analysis of the thermal behaviour of traditional underground wine cellars in Spain. Renewable Energy, 34(11), 2484–2492.

    Article  Google Scholar 

  • Mazarrón, F. R., Cid-Falceto, J., & Cañas, I. (2012). An assessment of using ground thermal inertia as passive thermal technique in the wine industry around the world. Applied Thermal Engineering, 33–34, 54–61.

    Article  Google Scholar 

  • Mendell, M. J., Mirer, A. G., Cheung, K., Tong, M., & Douwes, J. (2011). Respiratory and allergic health effects of dampness, mold, and dampness-related agents: a review of the epidemiologic evidence. Environmental Health Perspectives, 119(6), 748–756.

    Article  CAS  Google Scholar 

  • Miklós, I., Sipiczki, M., & Benko, Z. (1994). Osmotolerant yeasts isolated from Tokaj wines. Journal of Basic Microbiology, 34(6), 379–385.

    Article  Google Scholar 

  • Moularat, S., Hulin, M., Robine, E., Annesi-Maesano, I., & Caillaud, D. (2011). Airborne fungal volatile organic compounds in rural and urban dwellings: detection of mould contamination in 94 homes determined by visual inspection and airborne fungal volatile organic compounds method. Science of the Total Environment, 409(11), 2005–2009.

    Article  CAS  Google Scholar 

  • Naumov, G. I., Naumova, E. S., Antunovics, Z., & Sipiczki, M. (2002). Saccharomyces bayanus var. uvarum in Tokaj wine-making of Slovakia and Hungary. Applied Microbiology and Biotechnology, 59(6), 727–730.

    Article  CAS  Google Scholar 

  • Nyizsalovszki, R., & Fórián, T. (2007). Human impact on the landscape in the Tokaj foothill region Hungary. Geografia Fisica e Dinamica Quaternaria, 30(2), 219–224.

    Google Scholar 

  • O’Donnell, K. (1993). Fusarium and its near relatives. In D. R. Reynolds & J. W. Taylor (Eds.), The Fungal Holomorph: Mitotic, Meiotic and Pleomorphic Speciation in Fungal Systematic (pp. 225–233). Wallingford: CAB International.

    Google Scholar 

  • Oros, G., & Cserháti, T. (2009). Use of principal component analysis and spectral mapping technique for the evaluation of the antifungal activity of anthracene-based synthetic dyes. SAR & QSAR in Environmental Sciences, 20(3), 379–391.

    Article  CAS  Google Scholar 

  • Oros, G., Cserháti, T., & Forgács, E. (2003). Separation of the strength and selectivity of the microbiological effect of synthetic dyes by spectral mapping technique. Chemosphere, 52(1), 185–193.

    Article  CAS  Google Scholar 

  • Picco, A. M., & Rodolfi, M. (2004). Assesment of indoor fungi in selected wineries of Oltrepo Pavese (Northern Italy) and Sottoceneri (Switzerland). American Journal of Enology and Viticulture, 55(4), 355–362.

    Google Scholar 

  • Prak, S., Gunata, Z., Guiraud, J.-P., & Schorr-Gallindo, S. (2007). Fungal strains isolated from cork stoppers and the formation of 2,4,6-trichloroanisole involved in the cork taint of wine. Food Microbiology, 24, 271–280.

    Article  CAS  Google Scholar 

  • Raper, K. B., & Fennell, D. I. (1977). The Genus Aspergillus. RE Krieger Publishing Company. New York: Huntington.

    Google Scholar 

  • Sammon, J. W. (1969). A nonlinear mapping for data structure analysis. IEEE Transactions on Computers, 100(5), 401–409.

    Article  Google Scholar 

  • Samson, R. A. (2010). Food and Indoor Fungi. CBS Laboratory Manual Series. Utrecht: CBS-KNAW Fungal Biodiversity Centre.

    Google Scholar 

  • Scott, J. A., Untereiner, W. A., Ewaze, J. O., Wong, B., & Doyle, D. (2007). Baudoinia, a new genus to accommodate Torula compniacensis. Mycologia, 99(4), 592–601.

    Article  Google Scholar 

  • Simeray, J., Mandin, D., Mercier, M., & Chaumont, J.-P. (2001). Survey of viable airborne fungal propagules in French wine cellars. Aerobiologia, 17, 19–24.

    Article  Google Scholar 

  • Singh, K. (1991). An illustrated manual on identification of some seed-borne Aspergilli, Fusaria, Penicillia and their mycotoxins. Hellerup: Danish Government Institute of Seed Pathology for Developing Countries.

    Google Scholar 

  • Sipiczki, M. (2016). Overwintering of vineyard yeasts: survival of interacting yeast communities in grapes mummified on vines. Frontiers in Microbiology, 7, 212.

    Article  Google Scholar 

  • Sipiczki, M., Romano, P., Lipani, G., Miklos, I., & Antunovics, Z. (2001). Analysis of yeasts derived from natural fermentation in a Tokaj winery. Antonie van Leeuwenhoek, 79(1), 97–105.

    Article  CAS  Google Scholar 

  • Sváb, J. (1979). Multivariate methods in biometrics. Budapest: Mezőgazdasági Kiadó. (in Hungarian).

    Google Scholar 

  • Tanner, H., & Zanier, C. (1981). Zur analytischen Differenzierung von Muffton und Korkgeschmack in Weinen. Schweizer Zeitschrift für Obst und Weinbau, 117, 752–757.

    CAS  Google Scholar 

  • Tóth, D. (2006). Diversity of microflora in Tokaj cellars, Tokaj winegrowing and winemaking in Slovakia: almanac account from specialized seminar activity from 19. November 2002 in Vinicky, Agrogenofond, Nitra.

  • UNESCO description: Tokaj Wine Region Historic Cultural Landscape. http://whc.unesco.org/ Accessed 03 November 2015.

  • Von Arx, J. A. (1981). The genera of fungi sporulating in pure culture (No. Ed. 3). Vaduz: J. Cramer.

  • White, T. J., Bruns, T., Lee, S., & Taylor, J. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In M. H. Innes, D. H. Gelfand, J. J. Sninsky, & T. J. White (Eds.), PCR protocols (pp. 315–322). San Diego: Academic Press.

    Google Scholar 

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Authors and Affiliations

  1. Department of Air Hygiene and Aerobiology, National Public Health Institute, Albert Flórián Str. 2–6, Budapest, Hungary

    Donát Magyar

  2. Research Institute for Viticulture and Oenology, Tokaj, Hungary

    Zoltán Kállai & Zoltán Bihari

  3. Department of Genetics and Applied Microbiology, University of Debrecen, Debrecen, Hungary

    Zoltán Kállai & Matthias Sipiczki

  4. Institute of Aquaculture and Environmental Safety, Szent István University, Gödöllő, Hungary

    Csaba Dobolyi & Flóra Sebők

  5. Ministry of Human Capacities, Budapest, Hungary

    Tímea Beregszászi

  6. Department of Microbiology, Faculty of Science and Informatics, University of Szeged, Szeged, Hungary

    László Kredics

  7. Plant Protection Institute, Hungarian Academy of Sciences, Budapest, H-1022, Hungary

    Gyula Oros

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  1. Donát Magyar
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  2. Zoltán Kállai
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Correspondence to Donát Magyar.

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Magyar, D., Kállai, Z., Sipiczki, M. et al. Survey of viable airborne fungi in wine cellars of Tokaj, Hungary. Aerobiologia 34, 171–185 (2018). https://doi.org/10.1007/s10453-017-9505-3

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