Skip to main content
SpringerLink
Log in

Effect of indigenous mycobiota on ochratoxin A production by Aspergillus carbonarius isolated from soil

Ochratoxin in mixed cultures

  • Original Paper
  • Published:
Mycotoxin Research Aims and scope Submit manuscript

Abstract

This study determined the biotic interaction between 30 non-toxigenic indigenous strains of Aspergillus niger aggregate, Aspergillus flavus, Trichoderma spp., Mucor spp., Cladosporium spp., Ulocladium spp., Curvularia spp., Absidia spp., Geotrichum spp. and Acremonium spp., isolated from soil destined for maize crops, with respect to their ability to prevent ochratoxin A (OTA) production by A. carbonarius on “in vitro” assay, on liquid and solid medium. OTA production was completely inhibited when A. carbonarius was inoculated in a interactive mixed culture with all A. niger aggregate strains assayed, a 80 % of Trichoderma spp. strains, a 40 % of Cladosporium spp. strains, Acremonium spp and Geotrichum spp; only one strain of A. flavus tested was able to completely inhibit the mycotoxin accumulation. OTA production increased when A. carbonarius ACS 8 was growing on liquid interactive mixed culture with Mucor spp strains. These results demonstrated that OTA production by Aspergillua carbonarius strain was significantly influenced by the presence of different non-toxigenic fungal strains when growing together on paired cultures.

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

  • Abrunhosa L, Serra R, Venâncio A (2002) Biodegradation of ochratoxin A by fungi isolated from grapes. J Agric Food Chem 50:7493–7496

    Article  CAS  PubMed  Google Scholar 

  • Astoreca A, Magnoli C, Barberis C, Chiacchiera SM, Combina M, Dalcero AM (2007) Ochratoxin A production in relation to ecophysiological factors by Aspergillus section Nigri strains isolated from different substrates in Argentina. Sci Tot Environ 388:16–23

    Article  CAS  Google Scholar 

  • Aziz NH, Shahin AA (1997) Influence of other fungi on aflatoxin production by Aspergillus flavus in maize kernels. J Food Safety 17:113–23

    Article  CAS  Google Scholar 

  • Barberis C,Astoreca A,Fernandez-Juri G,Chulze S,Dalcero A,Magnoli C (2009) Use of propyl paraben to control growth and ochratoxin A production by Aspergillus section Nigri species on peanut meal extract agar. Int J Food Microbiol 136:133–136

  • Bragulat MR, Abarca ML, Cabañes FJ (2001) An easy screening method for fungi producing ochratoxin A in pure culture. Int J Food Microbiol 71:139–144

    Google Scholar 

  • Caldas ED, Silva SC, Oliveira JN (2002) Aflatoxins and ochratoxin A in food and rosks to human health. Rev Saude Publi 36:319–323

    Article  Google Scholar 

  • Calistru C, McLean M, Berjak P (1997) In vitro studies of the potential for biological control of Aspergillus flavus and Fusarium moniliforme by Trichoderma species. 2. A study of the production of extracelular metabolites by Trichoderma species. Mycopathologia 137:115–24

    Article  CAS  PubMed  Google Scholar 

  • Cavaglieri L, Andres L, Ibanez M, Etcheverry M (2005a) Rhizobacteria and their potential to control Fusarium verticillioides: effect of maize bacterisation and inoculums density. Antoinie Van Leeuwenhoek 87(3):179–87

    Article  CAS  Google Scholar 

  • Cavaglieri L, Passone A, Etcheverry M (2005b) Screening procedures to select rhizobacteria with biocontrol activity on Fusarium verticillioides growth and fumonisin B1 production. Res Microbiol 155:747–54

    Article  Google Scholar 

  • Commission of the European Communities (2006) Commission regulation (EC) N° 1881/2006 of 19 Dicember 2006 setting maximum levels for certain contaminants in foodstuffs. Off J Eur Union L364:5–24

    Google Scholar 

  • Cuero R, Smith JE, Lacey I (1988) Mycotoxin formation by Aspergillus flavus and Fusarium graminearum in irradiated maize grains in the presence of other fungi. J Food Protect 6:452–456

    Google Scholar 

  • Cvetnic Z, Pepeljnjak S (2007) Interaction between certain moulds and aflatoxin b1 producer Aspergillus flavus NRRL 3251. Arh Hig Rada Tokiskol 58:429–434

    CAS  Google Scholar 

  • Dalcero A, Magnoli C, Hallak C, Chiacchiera SM, Palacio G, Da Rocha RCA (2002) Detection of ochratoxin A in animal feeds and capacity to produce this mycotoxin by Aspergillus section Nigri in Argentina. Food Addit Contam 19:1065–1072

    Article  CAS  PubMed  Google Scholar 

  • Deberghes P, Betbeder AM, Boisard F, Blanc R, Delaby JF, Krivobok S, Steiman R, Seigle-Murandi F, Creppy EE (1995) Detoxification of ochratoxin A, a food contaminant: prevention of growth of Aspergillus ochraceus and its production of ochratoxin A. Mycotoxin Res 11:37–47

    Article  CAS  PubMed  Google Scholar 

  • Dorner JW, Cole RJ (2002) Effect of application of nontoxigenic strains of Aspergillus flavus and A. parasiticus on subsequent aflatoxin contamination of peanuts in storage. J Stored Prod Res 38:329–39

    Article  CAS  Google Scholar 

  • Dorner JW, Cole RJ, Connick WJ, Daigle DJ, McGuire MR, Shasha BS (2003) Evaluation of biological control formulations to reduce aflatoxin contamination in peanuts. Biocontrol 26:318–24

    Google Scholar 

  • Fraga ME, Curvello FA, Gatti MJ, Cavaglieri LR, Dalcero AM, Rosa CAR (2007) Potential aflatoxin and ochratoxin A production by Aspergillus species in poultry feed processing. Vet Res Commun 31:343–353

    Article  CAS  PubMed  Google Scholar 

  • Garber RK, Cotty PJ (1997) Formation of sclerotia and aflatoxins in developing cotton bolls infected by the S strain of Aspergillus flavus and potential for biocontrol with an atoxigenic strain. Phytopathologia 87:940–5

    Article  CAS  Google Scholar 

  • Gonzalez HHL, Resnik SL, Boca RT, Marasas WFO (1995) Mycoflora of Argentine corn harvested in the main production area in 1990. Mycopathologia 130:29–36

    Article  CAS  PubMed  Google Scholar 

  • Hwang CA, Draughon FA (1994) Degradation of ochratoxin A by Acinetobacter calcoaceticus. J Food Prot 57:410–414

    CAS  Google Scholar 

  • IARC. International Agency for Research on Cancer (1993) Ochratoxin A. In: monographs on the evaluation of carcinogenic risks to human: some naturally occurring substances; food items and constituents, heterocyclic aromatic amines and mycotoxins, vol 56. WHO, Lyon, pp 489–521

  • Klich MA (ed) (2002) Identification of Common Aspergillus Species. Centraal bureau voor Schimmelcultures, Utrecht

    Google Scholar 

  • La Penna M, Etcheverry M (2006) Impact on growth and aflatoxin B1 accumulation by Kluyveromyces isolates at different water activity conditions. Mycopathologia 162:347–53

    Article  PubMed  Google Scholar 

  • La Penna M, Nesci A, Etcheverry M (2004) In vitro studies on the potential for biological control on Aspergillus section Flavi by Kluyveromyces spp. Lett Appl Microbiol 38:257–64

    Article  PubMed  Google Scholar 

  • 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 37:179–184

    Article  CAS  PubMed  Google Scholar 

  • Magnoli C, Astoreca A, Ponsone L, Combina M, Palacio G, da Rocha Rosa CA, Dalcero AM (2004) Survey of mycoflora and ochratoxin A in dried vine fruits from Argentina markets. Lett Appl Microbiol 39:326–331

    Article  CAS  PubMed  Google Scholar 

  • Magnoli C, Hallak C, Astoreca A, Ponsone L, Chiacchiera SM, Palacio G, Dalcero A (2005) Surveillance of toxigenic fungi and ochratoxin A in feedstuffs from Córdoba province, Argentina. Vet Res Commun 29:431–445

    Article  CAS  PubMed  Google Scholar 

  • Magnoli C, Hallak C, Chiacchiera S, Dalcero A (2006a) Occurrence of ochratoxin A- producing fungi in commercial corn kernels in Argentina. Mycopathology 161:53–58

    Article  CAS  Google Scholar 

  • Magnoli C, Astoreca A, Ponsone L, Chiacchiera S, Dalcero A (2006b) Ochratoxin A and the occurrence of ochratoxin A- producing black aspergilli in stored peanut seeds from Córdoba, Argentina. J Sci Food Agric 86:2369–2373

    Article  CAS  Google Scholar 

  • Magnoli C, Astoreca A, Ponsone LM, Fernández-Juri G, Barberis C, Dalcero AM (2007) Ochratoxin A and Aspergillus section Nigri in peanut seeds at different months of storage in Córdoba, Argentina. Int J Food Microbiol 119:213–218

    Article  CAS  PubMed  Google Scholar 

  • McSpadden-Gardener BB, Fravel DR (2002) Biological control of plant pathogens: research, commmercialization and application in the USA. Plant Health Prog. doi:10.1094/PHP-2002-0510-01-RV

    Google Scholar 

  • Milus EA, Rothrock CS (1996) Efficacy of bacterial seed treatments for controlling Pythium root rot of winter wheat. Plant Dis 81:180–4

    Article  Google Scholar 

  • Nesci A, Bluma R, Etcheverry M (2005) In vitro selection of maize rhizobacteria to study potential biological control of Aspergillus section Flavi. Eur J Plant Pathol 113(2):1–13

    Article  Google Scholar 

  • O’Brien E, Dietrich DR (2005) Ochratoxin A: the continuing enigma. Crit Rev Toxicol 35:33–60

    Article  PubMed  Google Scholar 

  • Pereira P, Nesci A, Etcheverry M (2007) Effects of biocontrol agents on Fusarium verticillioides count and fumonisin content in the maize agroecosystem. Impact on rhizospheric bacterial and fungal groups. Biol Control 42:281–7

    Article  Google Scholar 

  • Pereira P, Nesci A, Etcheverry M (2008) Efficacy of bacterial seed treatments for the control of Fusarium verticillioides in maize. Biocontrol. doi:10.1007/s10526-007-9148-3

    Google Scholar 

  • Pfohl-Leszkowicz A, Manderville RA (2007) Ochratoxin A: An overview on toxicity and carcinogenicity in animals and humans. Mol Nut Food Res 51:61–99

    Article  CAS  Google Scholar 

  • Picco M, Nesci A, Barro, G, Cavaglier, L Etcheverry M (1999) Aflatoxin B1 and fumosin B1 in mixed cultures of Aspergillus flavus and Fusarium proliferatum on maize. J Nat Toxins 7:331–336

  • Ponsone ML, Chiotta ML, Combina M, Dalcero AM, Chulze SN (2009) Fate of ochratoxin A content in Argentinian red wine during a pilot scale vinification. Rev Argent Microbial 41(4):245–50

    CAS  Google Scholar 

  • Ponsone ML, Combina M, Dalcero A, Chulze S (2007) Ochratoxin A and ochratoxigenic Aspergillus species in Argentinean wine grapes cultivated under organic and non-organic systems. Int J Food Microbiol 114:131–135

    Article  CAS  PubMed  Google Scholar 

  • Quinn GP, Keough MJ (eds) (2002) Experimental Desing Data Analysis for Biologists. Cambridge University Press, Cambridge

    Google Scholar 

  • Rosa CAR, Ribeiro JMM, Fraga MJ, Gatti M, Cavaglieri L, Magnoli CE, Dalcero AM, Lopez CWG (2006) Mycoflora of poultry feeds and ochratoxin- producing ability of isolated Aspergillus and Penicillium species. Vet Microbiol 113:89–96

    Article  CAS  PubMed  Google Scholar 

  • Samson RA, Hockstra ES, Frisvad JC, Filtenborg O (2000) Introduction to Food and Airborne Fungi. Centaalbureau Voorschimmelculturs, Utrecht

    Google Scholar 

  • Scudamore KA, MacDonald SJ (1998) A collaborative study of an HPLC method for determination of ochratoxin A in wheat using immunoaffinity column clean-up. Food Addit Contam 15:401–410

    Article  CAS  PubMed  Google Scholar 

  • Secretaría de Agricultura, ganadería, Pesca y Alimentación (2013) Fuente de internet: http://www.sagpya.mecon.gov.ar. Accessed 26 August 2013

  • Shantha T (1999) Fungal degradation of aflatoxin B1. Nat Toxins 7:175–78

    Article  CAS  PubMed  Google Scholar 

  • Shantha T, Rati ER, Shankar TNB (1990) Behavior of Aspergillus flavus in presence of Aspergillus niger during biosynthesis of aflatoxin B. Antonie Van Leeuwenhoek 58:121–7

    Article  CAS  PubMed  Google Scholar 

  • Téren J, Varga J, Hamar Z, Rinyu E, Kevei F (1996) Immunochemical detection of ochratoxin A in black Aspergillus strains. Mycopathologia 134:171–176

    Article  PubMed  Google Scholar 

  • Torres AM, Ramírez ML, Reynoso MM, Rodriguez M, Chulze S (1997) Natural co occurrence of Fusarium species (section Liseola) and Aspergillus flavus group species, fumonisin and aflatoxin in argentinian corn. Cereal Res Commun 25:389–392

    Google Scholar 

  • Valero A, Farré J, Sanchis V, Ramos A, Marín S (2006) Effects of fungal interaction on ochratoxin A production by A. carbonarius at different temperatures and aw. Int J Food Microbiol 110:160–164

    Article  CAS  PubMed  Google Scholar 

  • Varga J, Péteri J, Tábori K, Téren J, Vágvölgyi C (2005) Degradation of ochratoxin A and other mycotoxins by Rhizopus isolates. Int J Food Microbiol 99:321–328

    Article  CAS  PubMed  Google Scholar 

  • Varga J, Rigo K, Téren J (2000) Degradation of ochratoxin A by Aspergillus species. Int J Food Microbiol 59:1–7

    Article  CAS  PubMed  Google Scholar 

  • Wicklow D, Roth S, Deyrup S, Gloer J (2005) A protective endophyte of maize: Acremonium zeae antibiotics inhibitory to Aspergillus flavus and Fusarium verticillioides. Mycol Res 109(5):610–618

    Article  CAS  PubMed  Google Scholar 

  • Wicklow DT (1988) Patterns of fungal associations within maize kernels in North Carolina. Plant Dis 72:113–115

    Article  Google Scholar 

  • Widstrom NW, McMillian WW, Wilson DM, Richard JL, Zumo N, Beaver RW (1994) Preharvest aflatoxin contamination of maize inoculated with Aspergillus Flavus and Fusarium moniliforme. Mycopathologia 128:118–123

    Article  Google Scholar 

  • Xiao H, Marquardt RR, Frohlich AA, Philips GD, Vitti TG (1991) Effect of hay and a grain diet on the rate of hydrolysis of ochratoxin A in the rumen sheep. J Anim Sci 69:3706–3714

    CAS  PubMed  Google Scholar 

  • Yoshizawa T, Yamashita A, Chokethaworn N (1996) Occurrence of fumonisind and aflatoxins in corn from Thailand. Food Add Contam 13:163–168

    Article  CAS  Google Scholar 

  • Zuber MS, Lillehoj EB (1993) Aflatoxin contamination in maize and its biocontrol. In: Mukerji KG, Garg KL (eds) Biocontrol of Plant Diseases. CBS, New Delhi, pp 86–102

    Google Scholar 

Download references

Acknowledgements

This work was carried out thanks to grants from the Consejo Nacional de Ciencia y Tecnología (CONICET-PIP), Secretaría de Ciencia y Técnica de la Universidad Nacional de Río Cuarto (SECYT-UNRC) and Fondo para la Investigación Científica y Tecnológica (FONCYT-PICTO).

Conflict of interest

None

Author information

Authors and Affiliations

  1. Departamento de Microbiología e Inmunología, Facultad de Ciencias Exactas, Físico, Químicas y Naturales, Universidad Nacional de Río Cuarto, Ruta Nacional Nº 36 Km 601, 5800, Río Cuarto, Córdoba, Argentina

    Carla L. Barberis, Gabriela Pena, Cecilia Carranza & Carina E. Magnoli

  2. Member of the Research Career of CONICET, Buenos Aires, Argentina

    Carla L. Barberis & Carina E. Magnoli

  3. Fellowship of CONICET, Buenos Aires, Argentina

    Gabriela Pena & Cecilia Carranza

Authors
  1. Carla L. Barberis
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gabriela Pena
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Cecilia Carranza
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Carina E. Magnoli
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Carla L. Barberis.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Barberis, C.L., Pena, G., Carranza, C. et al. Effect of indigenous mycobiota on ochratoxin A production by Aspergillus carbonarius isolated from soil. Mycotoxin Res 30, 1–8 (2014). https://doi.org/10.1007/s12550-013-0181-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12550-013-0181-z

Keywords

Search

Navigation