Abstract
Species belonging to Aspergillus section Nigri are widespread in the vineyard environment, both in soil and on plant surfaces. We used plate counts and droplet digital PCR (ddPCR) methods to compare populations of the four most prevalent species (A. carbonarius, A. niger, A. welwitschiae, and A. tubingensis) over two consecutive years in conventional and organic vineyards, to determine whether management affects the potential distribution of mycotoxigenic Aspergillus species. In 2016, plate counts showed that soil populations of total filamentous fungi and of Aspergillus section Nigri species were not significantly different between conventional and organic vineyards. In 2017, while total fungal populations in soil were not significantly different, Aspergillus section Nigri populations were significantly higher in organic vineyard soil. In both years, there were no significant differences in total fungal populations and in Aspergillus section Nigri populations on fruit surfaces collected from conventional and organic vineyards. Likewise, ddPCR methods did not show significant differences in percent distribution of Aspergillus species in soil and fruit between conventional and organic vineyards. These results suggest that intervention strategies for preharvest control of potential mycotoxigenic fungi are likely to be equally compatible with either vineyard management strategy.
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References
Leong SL, Hocking AD, Scott ES (2007) Aspergillus species producing ochratoxin A: isolation from vineyard soils and infection of Semillon bunches in Australia. J Appl Microbiol 102:124–133
Leong SL, Hocking AD, Pitt JI, Kazi BA, Emmett RW, Scott ES (2006) Black Aspergillus species in Australian vineyards: from soil to ochratoxin A in wine. In: Hocking AD, Pitt JI, Samson RA, Thrane U (eds) Advances in food mycology, vol 571. Advances in experimental medicine and biology. Springer, Boston, pp 153–171
Logrieco A, Moretti A, Perrone G, Mule G (2007) Biodiversity of complexes of mycotoxigenic fungal species associated with Fusarium ear rot of maize and Aspergillus rot of grape. Int J Food Microbiol 119:11–16
Varga J, Juhasz A, Kevei F, Kozakiewicz Z (2004) Molecular diversity of agriculturally important Aspergillus species. Eur J Plant Pathol 110:627–640
Kazi BA, Emmett RW, Nancarrow N, Partington DL (2008) Berry infection and the development of bunch rot in grapes caused by Aspergillus carbonarius. Plant Pathol 57:301–307. https://doi.org/10.1111/j.1365-3059.2007.01767.x
Battilani P, Giorni P, Bertuzzi T, Formenti S, Pietri A (2006) Black aspergilli and ochratoxin A in grapes in Italy. Int J Food Microbiol 111:S53–S60
Bau M, Bragulat MR, Abarca ML, Minguez S, Cabanes FJ (2005) Ochratoxigenic species from Spanish wine grapes. Int J Food Microbiol 98:125–130
Leong SL, Hocking AD, Pitt JI, Kazi BA, Emmett RW, Scott ES (2006) Australian research on ochratoxigenic fungi and ochratoxin A. Int J Food Microbiol 111(Suppl 1):S10–S17
Magnoli C, Astoreca A, Ponsone L, Combina M, Palacio G, Rosa CA, Dalcero AM (2004) Survey of mycoflora and ochratoxin A in dried vine fruits from Argentina markets. Lett Appl Microbiol 39:326–331
Palumbo JD, O’Keeffe TL, Vasquez SJ, Mahoney NE (2011) Isolation and identification of ochratoxin A-producing Aspergillus section Nigri strains from California raisins. Lett Appl Microbiol 52:330–336
Sage L, Krivobok S, Delbos E, Seigle-Murandi F, Creppy EE (2002) Fungal flora and ochratoxin A production in grapes and musts from France. J Agric Food Chem 50:1306–1311
Serra R, Abrunhosa L, Kozakiewicz Z, Venancio A (2003) Black Aspergillus species as ochratoxin A producers in Portuguese wine grapes. Int J Food Microbiol 88:63–68
Somma S, Perrone G, Logrieco AF (2012) Diversity of black Aspergilli and mycotoxin risks in grape, wine and dried vine fruits. Phytopathol Mediterr 51:131–147
Varga J, Kozakiewicz Z (2006) Ochratoxin A in grapes and grape-derived products. Trends Food Sci Technol 17:72–81
Abrunhosa L, Calado T, Venancio A (2011) Incidence of fumonisin B2 production by Aspergillus niger in Portuguese wine regions. J Agric Food Chem 59:7514–7518
Chiotta ML, Susca A, Stea G, Mule G, Perrone G, Logrieco A, Chulze SN (2011) Phylogenetic characterization and ochratoxin A-fumonisin profile of black Aspergillus isolated from grapes in Argentina. Int J Food Microbiol 149:171–176. https://doi.org/10.1016/j.ijfoodmicro.2011.06.002
Logrieco A, Ferracane R, Haidukowsky M, Cozzi G, Visconti A, Ritieni A (2009) Fumonisin B2 production by Aspergillus niger from grapes and natural occurrence in must. Food Addit Contam 26:1495–1500
Mogensen JM, Frisvad JC, Thrane U, Nielsen KF (2010) Production of fumonisin B2 and B4 by Aspergillus niger on grapes and raisins. J Agric Food Chem 58:954–958
Palumbo JD, O’Keeffe TL, McGarvey JA (2011) Incidence of fumonisin B2 production within Aspergillus section Nigri populations isolated from California raisins. J Food Prot 74:672–675
Barberis MG, Giaj Merlera G, Reynoso MM, Chulze SN, Torres AM (2014) Factors affecting distribution and abundance of Aspergillus section Nigri in vineyard soils from grapevine growing regions of Argentina. J Sci Food Agric 94:3001–3007. https://doi.org/10.1002/jsfa.6647
Cordero-Bueso G, Arroyo T, Serrano A, Tello J, Aporta I, Velez MD, Valero E (2011) Influence of the farming system and vine variety on yeast communities associated with grape berries. Int J Food Microbiol 145:132–139. https://doi.org/10.1016/j.ijfoodmicro.2010.11.040
Cordero-Bueso G, Arroyo T, Serrano A, Valero E (2011) Influence of different floor management strategies of the vineyard on the natural yeast population associated with grape berries. Int J Food Microbiol 148:23–29. https://doi.org/10.1016/j.ijfoodmicro.2011.04.021
Kecskemeti E, Berkelmann-Lohnertz B, Reineke A (2016) Are epiphytic microbial communities in the carposphere of ripening grape clusters (Vitis vinifera L.) different between conventional, organic, and biodynamic grapes? PLoS ONE 11:e0160852. https://doi.org/10.1371/journal.pone.0160852
King AD Jr, Hocking AD, Pitt JI (1979) Dichloran-rose bengal medium for enumeration and isolation of molds from foods. Appl Environ Microbiol 37:959–964
Palumbo JD, O’Keeffe TL, Ho YS, Fidelibus MW (2016) Population dynamics of Aspergillus section Nigri species on vineyard samples of grapes and raisins. J Food Prot 79:448–453. https://doi.org/10.4315/0362-028X.JFP-15-437
Palumbo JD, O’Keeffe TL, Fidelibus MW (2016) Characterization of Aspergillus section Nigri species populations in vineyard soil using droplet digital PCR. Lett Appl Microbiol 63:458–465. https://doi.org/10.1111/lam.12667
Battilani P, Giorni P, Pietri A (2003) Epidemiology of toxin-producing fungi and ochratoxin A occurrence in grape. Eur J Plant Pathol 109:715–722
Bellí N, Mitchell D, Marín S, Alegre I, Ramos AJ, Magan N, Sanchis V (2005) Ochratoxin A-producing fungi in Spanish wine grapes and their relationship with meteorological conditions. Eur J Plant Pathol 113:233–239. https://doi.org/10.1007/s10658-005-5547-4
Serra R, Mendonça C, Venâncio A (2006) Ochratoxin A occurrence and formation in Portuguese wine grapes at various stages of maturation. Int J Food Microbiol 111:S35–S39. https://doi.org/10.1016/j.ijfoodmicro.2006.03.007
Valero A, Marin S, Ramos AJ, Sanchis V (2005) Ochratoxin A-producing species in grapes and sun-dried grapes and their relation to ecophysiological factors. Lett Appl Microbiol 41:196–201
Bellí N, Marín S, Argilés E, Ramos AJ, Sanchis V (2007) Effect of chemical treatments on ochratoxigenic fungi and common mycobiota of grapes (Vitis vinifera). J Food Prot 70:157–163. https://doi.org/10.4315/0362-028X-70.1.157
Bellí N, Marín S, Sanchis V, Ramos AJ (2006) Impact of fungicides on Aspergillus carbonarius growth and ochratoxin A production on synthetic grape-like medium and on grapes. Food Addit Contam 23:1021–1029. https://doi.org/10.1080/02652030600778702
Malandrakis AA, Vattis KN, Doukas EG, Markoglou AN (2013) Effect of phenylpyrrole-resistance on fitness parameters and ochratoxin production in Aspergillus carbonarius. Int J Food Microbiol 165:287–294. https://doi.org/10.1016/j.ijfoodmicro.2013.05.019
Medina Á, Mateo R, Valle-Algarra FM, Mateo EM, Jiménez M (2007) Effect of carbendazim and physicochemical factors on the growth and ochratoxin A production of Aspergillus carbonarius isolated from grapes. Int J Food Microbiol 119:230–235. https://doi.org/10.1016/j.ijfoodmicro.2007.07.053
Özaltaca N, Teksür PK (2016) Effects of spray programs in vineyard and different type of sun-drying system on formation of ochratoxin A on raisins. Acta Horticultur 1144:169–173. https://doi.org/10.17660/ActaHortic.2016.1144.24
Terra MF, Lira NDA, Passamani FRF, Santiago WD, Cardoso MDG, Batista LR (2016) Effect of fungicides on growth and ochratoxin A production by Aspergillus carbonarius from Brazilian wine grapes. J Food Prot 79:1508–1516. https://doi.org/10.4315/0362-028X.JFP-16-037
Valero A, Marín S, Ramos AJ, Sanchis V (2007) Effect of preharvest fungicides and interacting fungi on Aspergillus carbonarius growth and ochratoxin A synthesis in dehydrating grapes. Lett Appl Microbiol 45:194–199. https://doi.org/10.1111/j.1472-765X.2007.02168.x
Garcia-Cela E, Ramos AJ, Sanchis V, Marin S (2012) Ochratoxigenic moulds and effectiveness of grape field antifungals in a climatic change scenario. J Sci Food Agric 92:1455–1461. https://doi.org/10.1002/jsfa.4726
Tjamos SE, Antoniou PP, Kazantzidou A, Antonopoulos DF, Papageorgiou I, Tjamos EC (2004) Aspergillus niger and Aspergillus carbonarius in Corinth raisin and wine-producing vineyards in Greece: population composition, ochratoxin A production and chemical control. J Phytopathol 152:250–255
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This work was supported by U.S. Department of Agriculture Agricultural Research Service CRIS project 2030-42000-039-00D. We thank the laboratory of Matthew Fidelibus for assistance with sample collection.
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Palumbo, J.D., O’Keeffe, T.L., Quejarro, B.J. et al. Comparison of Aspergillus Section Nigri Species Populations in Conventional and Organic Raisin Vineyards. Curr Microbiol 76, 848–854 (2019). https://doi.org/10.1007/s00284-019-01697-6
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DOI: https://doi.org/10.1007/s00284-019-01697-6