Fungal diversity in the grapes-to-wines chain with emphasis on Penicillium species
DOI:
https://doi.org/10.5219/882Keywords:
wine grapes, must, wine, mycobiota, mycotoxinAbstract
The aim of this work was the description of surface and endogenous mycobiota colonisation of grapes, fresh grape juice, grape must, and wine primarily focused to the current spectrum of the penicillium species. One sample of white grape variety Palava and one sample of blue grape variety Dornfelder were collected in Small Carpathian wine growing region of Slovakia in the year 2017. Direct plating of grapes on agar plates was used for analysis of surface mycobiota of grapes while surface sterilsed grapes were used for endogenous mycobiota analysis. Mycobiota of juice, must, and wine was analysed by plate dilution method. Overall, we isolated 148 strains belonging to 13 genera of filamentous microscopic fungi and Mycelia sterilia from grape variety Palava, while the most frequent was Alternaria. Alternaria was the most common genus in the surface and endogenous colonisation with an average relative density 50% and 73.6%, respectively. A total of 2 species of Penicillium were detected from the grapes to wine, potentially toxigenic Penicillium expansum and P. chrysogenum. A total of 39 strains belonging to 6 genera and Mycelia sterilia were identified from grape variety Dornfelder. The most abundant genus was also Alternaria (51.3%), followed by Penicillium (12.8%). Alternaria was the most common genus in the surface and endogenous colonisation and fresh grape juice with an average relative density from 20% (grape juice) to 71% (endogenous colonisation of grapes). A total of 3 species of Penicillium were detected from the grapes to wine, where Penicillium expansum were detected most commonly. In the second part of our work some selected isolates were tested to the ability to produce mycotoxins such as patulin, citrinin, and roquefortin C in in vitro condition by thin layer chromatography method. All tested strains of Penicillium species were able to produce at least one mycotoxin.
Downloads
Metrics
References
Abrunhosa, L., Paterson, R. R. M., Kozakiewicz, Z., Lima, N., Venancio, A. 2001. Mycotoxin production from fungi isolated from grapes. Lett Appl Microbiol, vol. 32, no. 4, p. 240-242. https://doi.org/10.1046/j.1472765x.2001.00897.x DOI: https://doi.org/10.1046/j.1472-765X.2001.00897.x
Alshannaq, A., Yu, J. H. 2017. Occurrence, Toxicity, and Analysis of Major Mycotoxins in Food. Int. J. Environ. Res. Public Health, vol. 14, no. 6, p. 632. https://doi.org/10.3390/ijerph14060632 DOI: https://doi.org/10.3390/ijerph14060632
Barboráková, Z., Tančinová, D., Lejková, J., Mašková, Z., Dovičičová, M., Labuda, R., Kačániová, M., Mokrý, M. 2011. Mycobiota of selected Slovak origin wines (production year 2009) during the vinification with focus on the Aspergillus and Penicillium genera and their potential mycotoxin production. Potravinarstvo, vol. 5, Special issue February 2011, p. 109-116. Available at: http://www.potravinarstvo.com/dokumenty/mc_februar_2011/pdf/2/barborakova.pdf (In Slovak)
Bau, M., Bragulat, M. R., Abarca, M. L., Minguez, S., Cabañes, F. J. 2005. Ochratoxigenic species from Spanish wine grapes. International Journal of Food Microbiology, vol. 98, no. 2, p. 125-130. https://doi.org/10.1016/j.ijfoodmicro.2004.05.015 DOI: https://doi.org/10.1016/j.ijfoodmicro.2004.05.015
Bau, M., Bragulat, M. R., Abarca, M. L., Minguez, S., Cabañes, F. J. 2006. Ochratoxin A producing fungi from Spanish vineyards. In Hocking, A. D., Pitt, J. I., Samson, R. A., Thrane, U. Advances in Food Mycology. Advances in Experimental Medicine and Biology. New York, USA : Springer, p. 173-179. ISBN-13: 978-0387-28385-2. https://doi.org/10.1007/0-387-28391-9 DOI: https://doi.org/10.1007/0-387-28391-9_10
Bejaoui, H., Mathieu, F., Taillandier, P., Lebrihi, A. 2006. Black aspergilli and ochratoxin A production in French vineyards. Int. J. Food Microbiol., vol. 111, no. 6, p. 46-52. https://doi.org/10.1016/j.ijfoodmicro.2006.03.004 DOI: https://doi.org/10.1016/j.ijfoodmicro.2006.03.004
Briceño, E. X., Latorre, B. A., Bordeu, E. 2009. Effect of Cladosporium rot on the composition and aromatic compounds of red wine. SJAR, vol. 7, no. 1, p. 119-128. https://doi.org/10.5424/sjar/2009071-404 DOI: https://doi.org/10.5424/sjar/2009071-404
Charoenchai, C., Fleet, G. H., Henschke, P. A. 1998. Effects of temperature, pH, and sugar concentration on the growth rates and cell biomass of wine yeasts. Am. J. Enol. Vitic., vol. 49, p. 283-288.
Drusch, S., Ragab, W. 2003. Mycotoxins in fruits, fruit juices, and dried fruits. J. Food. Prot., vol. 66, no. 8, p. 1514-1527. https://doi.org/10.4315/0362-028x-66.8.1514 DOI: https://doi.org/10.4315/0362-028X-66.8.1514
Felšöciová, S. 2016. Diverzita mikromycét asociovaných s Vitis vinifera L. s dôrazom na zástupcov rodu Penicillium Link (Diversity of micromycotes associated with Vitis vinifera L. with emphasis on representatives of the genus Penicillium Link.) Habilitation work, Nitra, Slovakia : Slovak University of Agriculture in Nitra, 156 p.
Felšöciová, S., Tančinová, D., Rybárik, Ľ., Mašková, Z., Kačániová, M. 2015. Mycobiota of Slovak wine grapes with emphasis on Aspergillus and Penicillium species in the Small Carphathian area. Potravinarstvo, vol. 9, no. 1, p. 501-508. https://doi.org/10.5219/529 DOI: https://doi.org/10.5219/529
Fernández-Cruz, M. L., Mansilla, M. L., Tadeo, J. L. 2010. Mycotoxins in fruits and their processed products: Analysis, occurrence and health implications. Journal of Advanced Research, vol. 1, no. 2, p. 113-122. https://doi.org/10.1016/j.jare.2010.03.002 DOI: https://doi.org/10.1016/j.jare.2010.03.002
Fredj, M. B. S., Chebil, S., Mliki, A. 2009. Isolation and characterization of ochratoxin A and aflatoxin B1 producing fungi infecting grapevines cultivated in Tunisia. Afr. J. Microbiol. Res., vol. 3, no. 9, p. 523-527.
García-Cela, E., Crespo-Sempere, A., Gil-Serna, J., Porqueres, A., Marin, S. 2015. Fungal diversity, incidence and mycotoxin contamination in grapes from two agro-climatic Spanish regions with emphasis on Aspergillus species. J. Sci. Food. Agric., vol. 95, no. 8, p. 1716-29. https://doi.org/10.1002/jsfa.6876 DOI: https://doi.org/10.1002/jsfa.6876
Gautam, A., Sharma, S., Bhadauria, R. 2009. Detection of toxigenic fungi and mycotoxins in medicinally important powdered herbal drugs. The Internet Journal of Microbiology, vol. 7, no. 2, p. 1-8. https://doi.org/10.5580/104b DOI: https://doi.org/10.5580/104b
Girbau, T., Stummer, B. E., Pocock, K. F., Baldock, G. A., Scott, E. S., Waters, E. J. 2004. The effect of Uncinula necator (powdery mildew) and Botrytis cinerea infection of grapes on the levels of haze-forming pathogenesis-related proteins in grape juice and wine. Australian Journal of Grape and Wine Research, vol. 10, no. 2, p. 125-133. https://doi.org/10.1111/j.17550238.2004.tb00015.x DOI: https://doi.org/10.1111/j.1755-0238.2004.tb00015.x
González, H. H. L., Martinez, E. J., Pacin, A., Resnik, S. L. 1999. Relationship between Fusarium graminearum and Alternaria alternata contamination and deoxinivalenol occurrence on Argentinian durum wheat. Mycopathologia, vol. 144, no. 2, p. 97-102. https://doi.org/10.1023/a:1007020822134 DOI: https://doi.org/10.1023/A:1007020822134
Kalíková, Ľ., Jankura, E., Šrobárová, A. 2009. First report of Alternaria bunch rot of grapevines in Slovakia. Australasian Plant Disease Notes, vol. 4, no. 1, p. 68-69.
König, H., Unden, G., Fröhlich, J. 2009. Biology of microorganisms on grapes, in must and in wine. Verlay Berlin Heidelberg : Springer. 516 p. ISBN 978-3-540-85462-3. https://doi.org/10.1007/978-3-540-85463-0 DOI: https://doi.org/10.1007/978-3-540-85463-0
La Guerche, S., Dauphin, B., Pons, M., Blancard, D., Darriet, P. 2006. Characterization of some mushroom and earthy off-odors microbially induced by the development of rot on grapes. Journal of Agricultural and Food Chemistry, vol. 54, no. 24, p. 9193-9200. https://doi.org/10.1021/jf0615294 DOI: https://doi.org/10.1021/jf0615294
La Guerche, S., Gracia, C., Darriet, P., Dubourdieu, D., Labarère, J. 2004. Characterization of Penicillium species isolated from grape berries by their internal transcribed spacer (ITS1) sequences and by gas chromatography-mass spectrometry analysis of geosmin production. Curr. Microbiol., vol. 48, no. 4, p. 405-411. https://doi.org/10.1007/s00284-003-4176-4 DOI: https://doi.org/10.1007/s00284-003-4176-4
La Guerche, S., Chamont, S., Blancard, D., Dubourdieu, D., Darriet, P. 2005. Origin of (-)-geosmin of grapes: on the complementary action of two fungi, Botrytis cinerea and Penicillium expansum. Antonie van Leeuwenhoek, vol. 88, no. 2, p. 131-139. https://doi.org/10.1007/s10482-005-3872-4 DOI: https://doi.org/10.1007/s10482-005-3872-4
Labuda, R., Tančinová, D. 2006. Fungi recovered from Slovakian poultry feed mixtures and their toxinogenity. Annals of Agricultural and Environmental Medicine, vol. 13, no. 2, p. 193-200.
Liu, X., Jia, B., Sun, X., Ai, J., Wang, L., Wang, C., et al. 2015. Effect of initial pH on growth characteristics and fermentation properties of Saccharomyces cerevisiae. J. Food Sci., vol. 80, no. 4, p. M800-M808. https://doi.org/10.1111/1750-3841.12813 DOI: https://doi.org/10.1111/1750-3841.12813
Magnoli, C., Violante, M., Combina, M., Palacio, G., Dalcero, A. 2003. Mycoflora and ochratoxin-producing strains of Aspergillus section Nigri in wine grapes in Argentina. Lett. Appl. Microbiol., vol. 37, no. 2, p. 179-184. https://doi.org/10.1046/j.1472765x.2003.01376.x DOI: https://doi.org/10.1046/j.1472-765X.2003.01376.x
Marin, S., Ramos, A. J., Cano-Sancho, G., Sanchis, V. 2013. Mycotoxins: occurrence, toxicology, and exposure assessment. Food Chem Toxicol., vol. 60, p. 218-237. https://doi.org/10.1016/j.fct.2013.07.047 DOI: https://doi.org/10.1016/j.fct.2013.07.047
Medina, A., Mateo, R., López-Ocaña, L. L., Valle-Algarra, F. M., Jiménez, M. 2005. Study of spanish grape mycobiota and ochratoxin A production by isolates of Aspergillus tubingensis and other members of Aspergillus section Nigri. Appl. Environ. Microbiol., vol. 71, no. 8, p. 4696-4702. DOI: https://doi.org/10.1128/AEM.71.8.4696-4702.2005
Pitt, J. I., Hocking, A. D. 2009. Fungi and Food Spoilage. 3rd ed. London, UK : Springer. 519 p. ISBN 978-0-387-92206-5. https://doi.org/10.1016/j.ijfoodmicro.2010.08.005 DOI: https://doi.org/10.1016/j.ijfoodmicro.2010.08.005
Prendes, L. P., Merín, M. G., Andreoni, M. A., Ramirez, M. L., de Ambrosini, V. I. M. 2015. Mycobiota and toxicogenic Alternaria spp. strains in Malbec wine grapes from DOC San Rafael, Mendoza, Argentina. Food control, vol. 57, p. 122-128. https://doi.org/10.1016/j.foodcont.2015.03.041 DOI: https://doi.org/10.1016/j.foodcont.2015.03.041
Puel, O., Galtier, P., Oswald, I. P. 2010. Biosynthesis and toxicological effects of patulin. Toxins (Basel). vol. 2, no. 12, p. 613-631. https://doi.org/10.3390/toxins2040613 DOI: https://doi.org/10.3390/toxins2040613
Rousseaux, S., Diguta, C. F., Radoï-Matei, F., Alexandre, H., Guilloux-Bénatier, M. 2014. Non-botrytis grape-rotting fungi responsible for earthy and moldy off-flavors and mycotoxins. Food Microbiol., vol. 38, p. 104-121. https://doi.org/10.1016/j.fm.2013.08.013 DOI: https://doi.org/10.1016/j.fm.2013.08.013
Russell, R., Paterson, R. R. M., Armando, V., Lima, N., Guilloux-Bénatier, M., Rousseaux, S. 2017. Predominant mycotoxins, mycotoxigenic fungi and climate change related to wine. Food Research International, vol. 103, p. 478-491. https://doi.org/10.1016/j.foodres.2017.09.080 DOI: https://doi.org/10.1016/j.foodres.2017.09.080
Sage, L., Krivoboc, S., Delbos, E., Seigle-Murandi, F., Creppy, E. E. 2002. Fungal flora and ochratoxin A production in grapes and musts from France. Journal of Agriculture and Food Chemistry, vol. 50, no. 5, p. 1306-1311. https://doi.org/10.1021/jf011015z DOI: https://doi.org/10.1021/jf011015z
Samson, R. A., Frisvad, J. C. 2004. Polyphasic taxonomy of Penicillium subgenus Penicillium: new taxonomic schemes and mycotoxins and other extrolites. Utrecht, Netherlands : Centraalbureau voor Schimmelcultures. 260 p. ISBN 90-70351-53-6.
Samson, R. A., Hoekstra, E. S., Frisvad, J. C., Filtenborg, O. 2002a. Introduction to food- and airborne fungi. 6th revised ed. (with some corrections). Utrecht, Netherlands : Centraalbureau voor Schimmelcultures. 389 p. ISBN 90-70351-42-0.
Samson, R. A., Hoekstra, E. S., Lund, F., Filtenborg, O., Frisvad, J. C. 2002b. Method for the detection, isolation and characterisation of food-borne fungi. In Samson, R. A., Hoekstra, E. S., Frisvad, J. C., Filtenborg, O. Introduction to food- and airborne fungi. Utrecht, Netherlands : Centraalbureau voor Schimmecultures. p. 283-297. ISBN 90-70351-42-0.
Samson, R. A., Houbraken, J., Thrane, U., Frisvad, J. C., Andersen, B. 2010. Food and Indoor Fungi. Utrecht, netherlands : CBS - KNAW Fungal Biodiversity Centre. 390 p. ISBN 978-90-70351-82-3.
Santini, A., Mikušová, P., Sulyok, M., Krska, R., Labuda, R., Šrobárová, A. 2014. Penicillium strains isolated from Slovak grape berries taxonomy assessment by secondary metabolite profile. Mycotoxin Research, vol. 30, no. 4, p. 213-220. https://doi.org/10.1007/s12550-014-0205-3 DOI: https://doi.org/10.1007/s12550-014-0205-3
Serra, R., Braga, A., Venâncio, A. 2005. Mycotoxin-producing and other fungi isolated from grapes for wine production, with particular emphasis on ochratoxin A. Res. Microbiol., vol. 156, no. 4, p. 515-521. https://doi.org/10.1016/j.resmic.2004.12.005 DOI: https://doi.org/10.1016/j.resmic.2004.12.005
Serra, R., Lourenço, A., Alipio, P., Venâncio, A. 2006. Influence of the region of origin on the mycobiota of grapes with emphasis on Aspergillus and Penicillium species. Mycol. Res., vol. 110, no. 8, p. 971-978. https://doi.org/10.1016/j.mycres.2006.05.010 DOI: https://doi.org/10.1016/j.mycres.2006.05.010
Stein, R. A., Bulboacӑ, A. E. 2017. Mycotoxins. In Dodd, Ch., Aldsworth, T., Stein, R. A., Cliver, D., Riemann, H. Foodborne Diseases. 3rd ed. London, United Kingdom : Elsevier, Academic Press, p. 407-446. ISBN 978-0-12-385007-2. https://doi.org/10.1016/B978-0-12-385007-2.00021-8 DOI: https://doi.org/10.1016/B978-0-12-385007-2.00021-8
Susca, A., Proctor, R. H., Mulè, G., Stea, G., Ritieni, A., Logrieco, A., Moretti, A. 2010. Correlation of mycotoxin fumonisin B2 production and presence of the fumonisin biosynthetic gene fum8 in Aspergillus niger from grape. Journal of Agricultural and Food Chemistry, vol. 58, no. 6, p. 9266-9272. https://doi.org/10.1021/jf101591x DOI: https://doi.org/10.1021/jf101591x
Tančinová, D., Felšöciová, S., Rybárik, Ľ., Mašková, Z., Císarová, M. 2015. Colonization of grape berries and cider by potential producers of patulin. Potravinarstvo, vol. 9, no. 1, p. 138-142. https://doi.org/10.5219/460 DOI: https://doi.org/10.5219/460
Yang, J., Li, J., Jiang, Y., Duan, X., Qu, H., Yang, B., Chen, F., Sivakumar, D. 2014. Natural occurrence, analysis, and prevention of mycotoxins in fruits and their processed products. Crit. Rev. Food Sci. Nutr., vol. 54, no. 1, p. 64-83. https://doi.org/10.1080/10408398.2011.569860 DOI: https://doi.org/10.1080/10408398.2011.569860
Downloads
Published
How to Cite
Issue
Section
License
This license permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited, and is not altered, transformed, or built upon in any way.
