Next Article in Journal
Snake Venom Disintegrins and Cell Migration
Next Article in Special Issue
Wavelength-Dependent Degradation of Ochratoxin and Citrinin by Light in Vitro and in Vivo and Its Implications on Penicillium
Previous Article in Journal
Warfarin Toxicity and Individual Variability—Clinical Case
Previous Article in Special Issue
Response to Comments of Peter G. Mantle
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Toxins
Volume 2
Issue 11
10.3390/toxins2112593
toxins-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Ecophysiology of Aspergillus Section Nigri Species Potential Ochratoxin A Producers

by
Andrea L. Astoreca
*,
Carina E. Magnoli
and
Ana M. Dalcero
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
*
Author to whom correspondence should be addressed.
Toxins 2010, 2(11), 2593-2605; https://doi.org/10.3390/toxins2112593
Submission received: 9 September 2010 / Revised: 28 September 2010 / Accepted: 26 October 2010 / Published: 29 October 2010
(This article belongs to the Special Issue Ochratoxins)
Versions Notes

Abstract

:
After aflatoxins, ochratoxin A (OTA) is the most studied mycotoxin due to the toxicological significance in human and animal diets. OTA presence has been extensively reported worldwide in the last decade in several agricultural products. The main OTA producer in tropical and temperate climates is Aspergillus carbonarius followed by species belonging to A. niger aggregate. Currently, many scientists worldwide have studied the influence of water activity and temperature for growth and biosynthesis of OTA by these species on synthetic media. This article reviews ecophysiological studies of Aspergillus section Nigri strains on synthetic media and natural substrates. The results of these investigations suggest that significant amounts of OTA can be produced in only five days and that the use of different storage practices, such as aW and temperature levels below 0.930 and 15 °C, respectively, allow controlling fungal contamination and minimizing the OTA production in several products as peanuts, corn, dried grapes and derived products for human consumption.

1. Introduction

The Aspergillus genus is distributed worldwide but is most commonly isolated from latitudes 26°–35° north or south of the Ecuador. Therefore, these fungi are common in warm and temperate climates. Their ability to develop under conditions of high temperature and relatively low aw allows them to adapt and colonize a diverse array of cereals and dried fruits [1].
Some of the species belonging to this genus, A. niger, A. sojae and A. oryzae, are known as producers of industrial enzymes and metabolites able to give flavor to food. However, there are other species capable to infect plant tissue and produce mycotoxins [2]. Ochratoxins—the second mycotoxin group in importance after aflatoxins—includes at least nine metabolites that are similar in structural terms, of which ochratoxin A (OTA) is the most studied metabolite due to its occurrence in food and feed and toxicological significance in human and animal diets. This toxin is known to have nephrotoxic, immunotoxic, teratogenic and carcinogenic effects on animals. The International Agency for Research of Cancer (IARC) has classified OTA as a group 2B carcinogen based on toxicity on rats [3,4]. For these reasons, the European Commission has fixed maximum limits for OTA in several agricultural products destined for human and animal consumption [5].
OTA presence has been extensively reported worldwide in the last decade in several products, such as coffee [6,7], wines [8,9,10,11,12,13,14], beers [15,16,17], grapes [18,19,20], dried grapes [7,21,22,23,24], cereals and derivatives destined for humans and animals [25,26,27,28,29,30,31,32,33,34], oilseeds and derivates products [35] and occasionally, in body fluids, plasm, meat and kidneys of several animal species [36,37].
In the 90s, this toxin was considered to be only produced by Penicillium verrucosum in temperate and cold climates, and A. ochraceus and related species in warm and tropical climates. Due to their physiological differences, each of these species occupies a particular ecological niche. In the last years, several studies reported the presence of potential OTA producers Aspergillus section Nigri species in food and feed; considering Aspergillus carbonarius as the main OTA producer followed by species belonging to the A. niger aggregate [38].
In Argentina, as in other temperate and tropical countries, P. verrucosum and A. ochraceus have not been reported as frequent colonizers in agricultural products, while A. carbonarius, A. niger aggregate species and monoseriates Aspergillus species such as A. aculeatus and A. japonicus have been frequently isolated from several agricultural products, e.g., coffee beans, red wine, dried grapes, corn and peanut kernels and feeds. OTA was detected in some of these substrates except in coffee beans and corn kernels [10,13,21,25,35,39,40,41,42,43]. In others South American countries, several authors have also informed the presence of this species in cocoa and coffee beans, grapes and poultry feed [44,45,46,47,48].
Crops contaminated with mycotoxins reflect a loss of income for agricultural producers. The strategies that prevent the entry of these metabolites in the food chain protect public health and reduce economic losses caused by contaminated agricultural products.
The knowledge of the ecophysiology of OTA producing fungi and ecological factors that influence OTA production is essential to optimize the implementation of preventive strategies aimed at controlling the sanitary quality of raw materials and/or products susceptible to fungal colonization.
There are multiple factors significantly involved in the development of section Nigri species and secondary metabolites biosynthesis, e.g., humidity, temperature, presence of oxygen and carbon dioxide, incubation time, substrate composition, loss of grain integrity caused by insects or mechanical/thermal damage, fungal inoculum, and the interaction/competition between other contaminated fungal species. Of these factors, water activity (aW) and temperature have shown the greatest effects on growth and OTA production. In general, the toxigenic species are not aggressive pathogens, but are often well adapted to substrates with low humidity, and they can easily colonize cereal grains and oilseeds that are stored under inappropriate environmental conditions.
In recent years, scientific studies have focused mainly on the influence of environmental factors on OTA production by P. verrucosum and A. ochraceus since they are recognized as the main producer species. Several ecophysiological studies on A. ochraceus were reported in the two last decades [49,50,51,52,53,54,55] as well as studies on P. viridicatum, nowadays classified as P. verrucosum [56,57,58,59].
Currently, many scientists worldwide have studied the influence of water activity and temperature for biosynthesis of OTA by other ochratoxigenic species belonging to section Nigri such as A. niger aggregate and A. carbonarius [60,61,62,63,64,65,66,67,68,69,70,71,72,73,74,75,76,77,78,79], although only a few studies have reported the effect of incubation time on the amount of OTA produced by some strains belonging to the genera Aspergillus section Nigri [80,81,82].
Besides environmental factors, biological factors have a noticeable influence on growth and OTA production. Some of these biological factors are intrinsic; hence, depend only on the genetic basis of the fungal strain. The strains vary in their ability to produce OTA as well as the quantity produced. Recently, several studies have allowed the detection of some genes that may be involved in the biosynthesis of this toxin. Initially, genes encoding a polyketide synthase of A. ochraceus [83,84], P. verrucosum [85] and P. nordicum [86] were characterized; but these genes had low homology between the last two species. The simultaneous presence of different bacteria or other fungi in the substrates also influences the growth of these ochratoxigenic species and OTA production.

2. Ecophysiological Studies of Aspergillus Section Nigri Strains on Synthetic Media

Several authors have shown minima and optima conditions for mycelial growth of ochratoxigenic species belonging to Aspergillus section Nigri on different culture media [60,64,65,66,67,68,69,70,71,72,76,77,79,80,82] (Table 1). In these studies, growth rates of Aspergillus section Nigri species showed a marked decrease with the reduction of temperature and water activity level, and were not higher than 3 mm day−1 at 15 °C at the lowest aW. The highest growth rates of these species found at optimal conditions differ depending on the agar media used. The highest growth rates achieved by A. carbonarius species was found on CYA by Romero et al. [79] at 0.95 aW and 30 °C (17.46 mm day−1) with a strain isolated from Argentinean dried vine fruits and Leong et al. [77] reported a maximum growth rate (11.35 mm day−1) for an A. niger aggregate strain at 0.98 aW and 35 °C on a simulated grape juice medium. However, the literature shows that in most combinations of temperature and aw tested, A. niger grew more rapidly than A. carbonarius. The reproducibility of these optima for growth indicates that A. niger aggregate has a higher optimum temperature for growth than A. carbonarius and possibly also takes greater advantage of high water activities for rapid growth. In general, the optimum conditions for growth of assayed strains belonging to the A. niger aggregate and A. carbonarius strains were similar than that reported by the former authors. These optimal conditions for growth by Aspergillus section Nigri strains are in agreement with previous European works [60,63,70,81], which reported optimal growth rates for A. carbonarius strains at temperatures between 30–35 °C and 0.950-0.980 aW. The environmental conditions of growth inhibition observed by Astoreca et al. [64] agree with those obtained previously on synthetic media with strains of section Nigri isolated from maize grains [87] and from grapes [60,70,81]. In another study from Argentina, Romero et al. [79] evaluated the growth rate of A. carbonarius strains isolated from dried grapes at different aW and temperature conditions and the results showed that the inhibition of growth occurred at 15 °C among 0.825 to 0.900 aW, and 25 °C at 0.825 aW.
Ochratoxin A production in relation to ecophysiological factors by Aspergillus section Nigri strains was evaluated by several authors on synthetic media [62,63,65,66,67,68,69,70,71,73,81,82] (Table 2).
Astoreca et al. [65] evaluated the influence of ecophysiological factors on OTA production by six A. niger aggregate strains isolated from peanut seeds, corn kernels and coffee beans; and two A. carbonarius strains isolated from dried grapes in Argentina. These authors observed that the optimum temperature for OTA production was 25 °C for all strains belonging to the A. niger aggregate; while the A. carbonarius strains produced the highest OTA levels at 25 and 30 °C, without significant differences in production profiles between these strains. These OTA production patterns agree with those previously reported by Bellí et al. [72]. In this study, the results of OTA production by Aspergillus section Nigri species on a medium similar to grape composition were modeled by a multiple linear regression and predictive models were obtained. The results showed that high levels of aW (0.960 and 0.995) favored OTA production by A. carbonarius and A. niger aggregate strains as Bellí et al. [81], Esteban et al. [61,62], Joosten et al. [6] and Romero et al. [78] reported. On the other hand, Oueslati et al. [80] evaluated the effect of three alternating temperatures cycles (20/30, 20/37 and 25/42 °C) and photoperiod on growth and OTA production of six strains of A. carbonarius from Tunisian grapes on synthetic nutrient medium. The different temperature regimes assayed affected significantly both the mycelial growth and the OTA production. The best growth and OTA production were recorded with the 20/30 °C cycle.
Several studies have detected similar minimum aW level, 0.90–0.94 for OTA production by Aspergillus niger aggregate and A. carbonarius strains on different synthetic media (Table 2), whereas, Romero et al. [78] reported A. carbonarius strains able to produce traces amounts of OTA at lowest aW level (0.87) on CYA medium. The results present in the literature shows that different substrates significantly affect the optimum and the minimum aW conditions for OTA synthesis.

3. Ecophysiological Studies of Aspergillus Section Nigri Strains on Natural Substrates

Results obtained on synthetic substrates may not accurately represent the real fungal ability to produce OTA on a natural substrate. Therefore, studies on OTA production have been frequently carried out on natural and common substrates for ochratoxigenic A. ochraceus and P. verrucosum, such as cereal grains, green coffee beans and grapes, but there is little information about the influence of aW and temperature on growth parameters and OTA production of Aspergillus section Nigri strains on natural substrates.
Table
Table 1. Optima and minima conditions (temperature and water activity) for Aspergillus section Nigri species growth on different culture media.
Table 1. Optima and minima conditions (temperature and water activity) for Aspergillus section Nigri species growth on different culture media.
Fungal speciesMediumTested temperature range (°C)Optimum temperature (°C)Optimum aWMinimum aWReferences
A. section NigriGrains and fruits based15–30300.970.85Astoreca et al. [64]
Synthetic nutrient10–3730–370.98-Bellí et al. [72]
CYA-YES5–4530–35--Esteban et al. [82]
A. niger aggregateCorn grains15–30300.950.91Astoreca et al. [66]
Peanut seeds15–30300.990.91Astoreca et al. [67]
Coffee beans15–30250.990.93Astoreca et al. [68]
Synthetic nutrient10–37250.95-Selouane et al. [76]
Simulated grape juice15–35350.980.92 (15 °C)Leong et al. [77]
A. carbonariusSynthetic grape juice10–40350.980.88Mitchell et al. [60]
Dried grapes15–3025–300.990.91Astoreca et al. [64]
Synthetic grape15–37300.95–0.990.90 (15 °C)Bellí et al. [70]
Synthetic nutrient20–2828--Bellí et al. [71]
Synthetic nutrient10–37250.95-Selouane et al. [76]
Simulated grape juice15–35300.9650.92 (15 °C)Leong et al. [77]
CYA15–35300.950.85Romero et al. [79]
Synthetic nutrient20/3020/30--Oueslati et al. [80]
20/37
25/42
CYA: Czapek Yeast Autolysate agar; YES: Yeast Extract Sucrose agar; -: Data not reported.
Table
Table 2. Optima and minima conditions for ochratoxin A (OTA) production by Aspergillus section Nigri species on different culture media.
Table 2. Optima and minima conditions for ochratoxin A (OTA) production by Aspergillus section Nigri species on different culture media.
Fungal speciesMediumTested temperature range (°C)Optimum temperature (°C)Optimum aWMinimum aWReferences
A. section NigriGrains and fruits based15–3025–300.97–0.990.89–0.90Astoreca et al. [65]
CYA-YES5–4525--Esteban et al. [82]
A. niger aggregateCYA-YES--0.990.94Esteban et al. [61]
15–30150.980.90Esteban et al. [62]
Corn grains15–30250.970.91–0.93Astoreca et al. [66]
Peanut seeds15–30250.97 (25°C)0.91Astoreca et al. [67]
Coffee beans15–30300.990.95Astoreca et al. [68]
Synthetic nutrient10–3730–370.90–0.95-Selouane et al. [76]
Simulated grape juice15–35150.95-Leong et al. [77]
Synthetic nutrient10–37300.995-Bellí et al. [81]
A. carbonariusCoffee cherries15–35250.990.94Joosten et al. [6]
Synthetic grape juice10–4015–200.95–0.98-Mitchell et al. [60]
Dried grapes15–30300.990.91Astoreca et al. [69]
Synthetic grape15–37200.95–0.990.90Bellí et al. [70]
Synthetic Nutrient20–2828--Bellí et al. [71]
Table grapes20–30300.99-Bellí et al. [73]
Synthetic nutrient10–3725–300.95–0.99-Selouane et al. [76]
Simulated grape juice15–35150.95–0.98-Leong et al. [77]
CYA15–35150.950.87Romero et al. [78]
Synthetic nutrient20/3020/30--Oueslati et al. [80]
20/37
25/42
Synthetic nutrient10–37250.96-Bellí et al. [81]
CYA: Czapek Yeast Autolysate agar; YES: Yeast Extract Sucrose agar; -: Data not reported.
Most of the studies were done on solid synthetic and different substrate based media. The first study carried out with OTA producing strains belonging to Aspergillus section Nigri on natural substrate was reported by Joosten et al. [6], who studied the effect of environmental factors on growth parameters and OTA production by A. carbonarius strains on coffee cherries in Thailand. These authors showed that the optimal conditions of OTA production by A. carbonarius were 25 °C and 0.990 aW. In other study, four ochratoxigenic A. carbonarius strains isolated from wine grapes were used to inoculate artificially damaged and undamaged table grapes [73]. Grapes were stored at three levels of relative humidity (80, 90 and 100%) and at two temperatures (20 and 30 °C). The results showed that temperature and relative humidity significantly influenced both infection and toxin content. At 30 °C, the detected OTA amount was higher than at 20 °C in most of the treatments. The highest relative humidity (100%) led to maximum OTA amounts while no significant differences were found between 90% and 80% in the OTA content.
Recently, Astoreca et al. [66,67,68,69] reported on the influence of environmental factors (aW: 0.995, 0.973, 0.951, 0.928 and 0.910 and temperature: 15, 25 and 30 °C) on lag phase, growth rate, and OTA production by strains belonging to A. niger aggregate on irradiated corn, peanuts, dried grapes and coffee beans at 7, 14 and 21 days of incubation. The observed general pattern of in vitro growth [64,65] was different from those obtained on the natural substrates. The assayed strains on irradiated peanut seeds showed the shortest lag phases at the optimum conditions (7 h at 30 °C and 0.995) while the other strains reached the exponential phases only after around 35.3, 13.2 and 94.8 h at the same condition on irradiated corn, dried grapes and coffee beans, respectively. Under optimal conditions (0.973 aW, 25 °C and seven days of incubation), the OTA production in irradiated corn, peanut and dried grapes were significantly greater than the concentrations obtained by these strains on the medium based on each substrate.
Marín et al. [88] developed a suitable validated model to predict the growth and OTA production boundaries by an A. carbonarius strain in the function of moisture content and storage temperature of pistachios. These authors showed that OTA accumulation was mainly a function of the temperature of storage, with a sharp increase at <15-20 °C; this value was very different from 30 to 35 °C, which was optimum for growth. This suggests that the substrate combined with certain environmental conditions on which strains are developed affects OTA production. According to these results, significant amounts of OTA on natural substrates could be produced in only five days at aW ≥ 0.970 in a wide temperature range. These studies of predictive models represent an essential improvement to the quality and safety of food, allowing the prediction of toxin contamination.

4. Conclusions

In general, temperature and aW range for OTA production is more restricted than fungal growth, both on natural substrate but also on the culture media based substrate. The knowledge of the ecophysiology of strains belonging to the genera Aspergillus section Nigri is critical in the development and prediction of risk models for contamination of both raw materials and finished foods with these species under the interaction of several environmental parameters. The use of different storage practices, such as aW and temperature levels below 0.930 and 15 °C, respectively, allow controlling fungal contamination and minimizing OTA production in several products as peanuts, corn, dried grapes and derived products for human consumption.

References

  1. Pitt, J.I.; Hocking, A.D. Fungi and Food Spoilage; Blackie Academic and Professional: London, UK, 1997; p. 592. [Google Scholar]
  2. Perrone, G.; Susca, A.; Cozzi, G.; Ehrlich, K.; Varga, J.; Frisvad, J.C.; Meijer, M.; Noonim, P.; Mahakarnchanakul, W.; Samson, R.A. Biodiversity of Aspergillus species in some important agricultural products. Stud. Mycol. 2007, 59, 53–66. [Google Scholar]
  3. International Agency for Research on Cancer. Ochratoxin A. In IARC Monographs on the Evaluation of Carcinogenic Risks to Human: Some Naturally Occurring Substances; Food Items and Constituents, Heterocyclic Aromatic Amines and Mycotoxins; IARC: Lyon, France, 1993; Volume 56, pp. 26–32. [Google Scholar]
  4. JECFA. Safety Evaluation of Certain Mycotoxins in Food, Fifty-sixth Meeting of the Joint FAO/WHO Expert Committee on Food Additives (JECFA), WHO Food Additives Series No. 47; WHO: Geneva, Switzerland, 2001.
  5. European Commission. Commission Regulation (EU) No 105/2010 of 5 February 2010 amending Regulation (EC) No 1881/2006 setting maximum levels for certain contaminants in foodstuffs as regards ochratoxin A. Off. J. Eur. Union 2010, L35, 7–8.
  6. Joosten, H.M.; Goetz, J.; Pittet, A.; Schellenberg, M.; Bucheli, P. Production of ochratoxin A by Aspergillus carbonarius on coffee cherries. Int. J. Food Microbiol. 2001, 65, 39–44. [Google Scholar]
  7. Aoyama, K.; Nakajima, M.; Tabata, S.; Ishikuro, E.; Tanaka, T.; Norizuki, H.; Itoh, Y.; Fujita, K.; Kai, S.; Tsutsumi, T.; et al. Four-year surveillance for ochratoxin A and fumonisins in retail foods in Japan. J. Food Prot. 2010, 73, 344–352. [Google Scholar]
  8. Ratola, N.; Barros, P.; Simoes, T.; Cerdeira, A.; Venancio, A.; Alves, A. Worldwide interlaboratory study on the determination of ochratoxin A in different wine type samples. Talanta 2006, 70, 720–731. [Google Scholar] [Green Version]
  9. Serra, R.; Mendonça, C.; Venancio, A. Ochratoxin A occurrence and formation in Portuguese wine grapes at various stages of maturation. Int. J. Food Microbiol. 2006, 111, S35–S39. [Google Scholar]
  10. Ponsone, M.L.; Combina, M.; Dalcero, A.; Chulze, S. Ochratoxin A and ochratoxigenic Aspergillus species in Argentinean wine grapes cultivated under organic and non-organic systems. Int. J. Food Microbiol. 2007, 114, 131–135. [Google Scholar]
  11. Var, I.; Kabak, B. Occurrence of ochratoxin A in Turkish wines. Microchem. J. 2007, 86, 241–247. [Google Scholar]
  12. Valero, A.; Marín, S.; Ramos, A.J.; Sanchis, V. Survey: Ochratoxin A in European special wines. Food Chem. 2008, 108, 593–599. [Google Scholar] [CrossRef]
  13. Ponsone, M.L.; Chiotta, M.L.; Combina, M.; Dalcero, A.M.; Chulze, S.N. Fate of ochratoxin A content in Argentinian red wine during a pilot scale vinification. Rev. Argent. Microbiol. 2009, 41, 245–250. [Google Scholar]
  14. Tessini, C.; Mardones, C.; Von Baer, D.; Vega, M.; Herlitz, E.; Saelzer, R.; Silva, J.; Torres, O. Alternatives for sample pre-treatment and HPLC determination of ochratoxin A in red wine using fluorescence detection. Anal. Chim. Acta 2010, 660, 119–126. [Google Scholar]
  15. Medina, A.; Jiménez, M.; Gimeno-Adelantado, J.; Valle-Algarra, F.; Mateo, R. Determination of ochratoxin A in beer marketed in Spain by liquid chromatography with fluorescence detection using lead hydroxyacetate as a clean-up agent. J. Chromatogr. A 2005, 1083, 7–13. [Google Scholar]
  16. Mateo, R.; Medina, A.; Mateo, E.M.; Mateo, F.; Jiménez, M. An overview of ochratoxin A in beer and wine. Int. J. Food Microbiol. 2007, 119, 79–83. [Google Scholar]
  17. Reinsch, M.; Topfer, A.; Lehmann, A.; Nehls, I.; Panne, U. Determination of ochratoxin A in beer by LC-MS/MS ion trap detection. Food Chem. 2007, 100, 312–317. [Google Scholar]
  18. Battilani, P.; Magan, N.; Logrieco, A. European research on ochratoxin A in grapes and wine. Int. J. Food Microbiol. 2006, 111, S2–S4. [Google Scholar]
  19. Lasram, S.; Bellí, N.; Chebil, S.; Nahla, Z.; Ahmed, M.; Sanchís, V.; Ghorbel, A. Short communication: Occurrence of ochratoxigenic fungi and ochratoxin A in grapes from a Tunisian vineyard. Int. J. Food Microbiol. 2007, 114, 376–379. [Google Scholar]
  20. Varga, J.; Kozakiewicz, Z. Ochratoxin A in grapes and grape derived products. Trends Food Sci. Technol. 2006, 17, 72–81. [Google Scholar]
  21. Magnoli, C.; Astoreca, A.; Ponsone, L.; Combina, M.; Palacio, G.; Rosa, C.A.R.; Dalcero, A. Survey of mycoflora and ochratoxin A in dried vine fruits from Argentina markets. Lett. Appl. Microbiol. 2004, 39, 326–331. [Google Scholar]
  22. Chulze, S.N.; Magnoli, C.E.; Dalcero, A.M. Review: Occurrence of ochratoxin A in wine and ochratoxigenic mycoflora in grapes and dried vine fruits in South America. Int. J. Food Microbiol. 2006, 111, S5–S9. [Google Scholar]
  23. Karbancıoglu-Guler, F.; Heperkan, D. Natural occurrence of ochratoxin A in dried figs. Anal. Chim. Acta 2008, 617, 32–36. [Google Scholar]
  24. Bircan, C. Incidence of ochratoxin A in dried fruits and co-occurrence with aflatoxins in dried figs. Food Chem. Toxicol. 2009, 47, 1996–2001. [Google Scholar]
  25. Dalcero, A.; Magnoli, C.; Hallak, C.; Chiacchiera, S.M.; Palacio, G.; Rosa, C.A.R. Detection of ochratoxin A in animal feeds and capacity to produce this mycotoxin by Aspergillus section Nigri in Argentina. Food Addit. Contam. 2002, 19, 1065–1072. [Google Scholar]
  26. Araguás, C.; González-Peñas, E.; López de Cerain, A. Study on ochratoxin A in cereal-derived products from Spain. Food Chem. 2005, 92, 459–464. [Google Scholar]
  27. Magnoli, C.; Astoreca, A.; Chiacchiera, S.M.; Dalcero, A. Occurrence of ochratoxin A and ochratoxigenic mycoflora in corn and corn based foods and feeds in some South American countries. Mycopathologia 2007, 163, 249–260. [Google Scholar]
  28. Juan, C.; Moltó, J.C.; Lino, C.M.; Mañes, J. Analytical methods: Determination of ochratoxin A in organic and non-organic cereals and cereal products from Spain and Portugal. Food Chem. 2008, 107, 525–530. [Google Scholar] [CrossRef]
  29. Juan, C.; Pena, A.; Lino, C.; Moltó, J.C.; Mañes, J. Levels of ochratoxin A in wheat and maize bread from the central zone of Portugal. Int. J. Food Microbiol. 2008, 127, 284–289. [Google Scholar] [CrossRef] [PubMed]
  30. Juan, C.; Zinedine, A.; Idrissi, L.; Mañes, J. Ochratoxin A in rice on the Moroccan retail market. Int. J. Food Microbiol. 2008, 126, 83–85. [Google Scholar] [CrossRef] [PubMed]
  31. Villa, P.; Markaki, P. Aflatoxin B1 and ochratoxin A in breakfast cereals from at hens market: Occurrence and risk assessment. Food Control 2009, 20, 455–461. [Google Scholar]
  32. Zaied, C.; Abid, S.; Zorgui, L.; Bouaziz, C.; Chouchane, S.; Jomaa, M.; Bacha, H. Natural occurrence of ochratoxin A in Tunisian cereals. Food Control 2009, 20, 218–222. [Google Scholar]
  33. Duarte, S.C.; Pena, A.; Lino, C.M. A review on ochratoxin A occurrence and effects of processing of cereal and cereal derived food products. Food Microbiol. 2010, 27, 187–198. [Google Scholar]
  34. Monbaliu, S.; Van Poucke, C.; Detavernier, C.; Dumoulin, F.; Van de Velde, M.; Schoeters, E.; Van Dyck, F.; Averkieva, O.; Van Peteghem, C.; De Saeger, S. Occurrence of mycotoxins in feed as analyzed by a multi-mycotoxin LC-MS/MS method. J. Agric. Food Chem. 2010, 58, 66–71. [Google Scholar]
  35. Magnoli, C.; Astoreca, A.; Ponsone, M.L.; Fernández-Juri, M.G.; Barberis, C.; Dalcero, A. Ochratoxin A and Aspergillus section Nigri in peanut seeds at different months of storage in Córdoba, Argentina. Int. J. Food Microbiol. 2007, 119, 213–218. [Google Scholar] [CrossRef] [PubMed]
  36. Matrella, R.; Monaci, L.; Milillo, M.A.; Palmesano, F.; Tantillo, M.G. Ochratoxin A determination in paired kidneys and muscle samples from swines slaughtered in southern Italy. Food Control 2006, 17, 114–117. [Google Scholar]
  37. Aoudia, N.; Tangni, E.K.; Larondelle, Y. Distribution of ochratoxin A in plasma and tissues of rats fed a naturally contaminated diet amended with micronized wheat fibers: Effectiveness of mycotoxin sequestering activity. Food Chem. Toxicol. 2008, 46, 871–878. [Google Scholar]
  38. Abarca, M.L.; Accensi, F.; Cano, J.; Cabañes, F.J. Taxonomy and significance of black Aspergilli. Antonie Van Leeuwenhoek 2004, 86, 33–49. [Google Scholar]
  39. Magnoli, C.; Hallak, C.; Astoreca, A.; Ponsone, L.; Chiacchiera, S.M.; Palacio, G.; Dalcero, A. Surveillance of toxigenic fungi and ochratoxin A in feedstuffs from Córdoba province, Argentina. Vet. Res. Commun. 2005, 29, 431–445. [Google Scholar]
  40. Magnoli, C.; Hallak, C.; Chiacchiera, S.M.; Dalcero, A. Occurrence of ochratoxin A-producing fungi in commercial corn kernels in Argentina. Mycophatologia 2006, 161, 53–58. [Google Scholar] [CrossRef]
  41. Magnoli, C.; Astoreca, A.; Ponsone, L; Chiacchiera, S.M.; Dalcero, A. Ochratoxin A producing fungi in stored peanut seeds from Córdoba province, Argentina. J. Sci. Food Agric. 2006, 86, 2369–2373. [Google Scholar] [CrossRef]
  42. Romero, S.M.; Comerio, R.M.; Larumbe, G.; Ritieni, A.; Vaamonde, G.; Fernández Pinto, V. Toxigenic fungi isolated from dried vine fruits in Argentina. Int. J. Food Microbiol. 2005, 104, 43–49. [Google Scholar]
  43. Chiotta, M.L.; Ponsone, M.L.; Combina, M.; Torres, A.M.; Chulze, S.N. Aspergillus section Nigri species isolated from different wine-grape growing regions in Argentina. Int. J. Food Microbiol. 2009, 136, 137–141. [Google Scholar]
  44. Batista, L.R.; Chalfoun, S.M.; Prado, G.; Schwan, R.F.; Wheals, A.E. Toxigenic fungi associated with processed (green) coffee beans (Coffea arabica L.). Int. J. Food Microbiol. 2003, 85, 293–300. [Google Scholar] [CrossRef] [PubMed]
  45. Rosa, C.A.R.; Ribeiro, J.M.M.; Fraga, M.J.; Gatti, M.; Cavaglieri, L.R.; Magnoli, C.E.; Dalcero, A.M.; Lopes, C.W.G. Mycoflora of poultry feeds and ochratoxin-producing ability of isolated Aspergillus and Penicillium species. Vet. Microbiol. 2006, 113, 89–96. [Google Scholar]
  46. Sartori, D.; Furlaneto, M.C.; Martins, M.K.; Ferreira de Paula, M.R.; Pizzirani-Kleiner, A.A.; Taniwaki, M.H.; Pelegrinelli Fungaro, M.H. PCR method for the detection of potential ochratoxin-producing Aspergillus species in coffee beans. Res. Microbiol. 2006, 157, 350–354. [Google Scholar]
  47. Díaz, G.A.; Torres, R.; Vega, M.; Latorre, B.A. Ochratoxigenic Aspergillus species on grapes from Chilean vineyards and Aspergillus threshold levels on grapes. Int. J. Food Microbiol. 2009, 133, 195–199. [Google Scholar]
  48. Copetti, M.V.; Pereira, J.L.; Iamanaka, B.T.; Pitt, J.I.; Taniwaki, M.H. Ochratoxigenic fungi and ochratoxin A in cocoa during farm processing. Int. J. Food Microbiol. 2010, 143, 67–70. [Google Scholar]
  49. Ramakrishna, N.; Lacey, J.; Smith, J.E. Colonization of barley grain by Penicillium verrucosum and ochratoxin A formation in the presence of competing fungi. J. Food Prot. 1996, 59, 1311–1317. [Google Scholar]
  50. Lee, H.B.; Magan, N. Environmental factors influence in vitro interespecific interactions between A. ochraceus and other maize spoilage fungi, growth and ochratoxin production. Mycophatologia 1999, 146, 43–47. [Google Scholar] [CrossRef]
  51. Ramos, A.J.; Labernia, N.; Marin, S.; Sanchís, V.; Magan, N. Effect of water activity and temperature on growth and ochratoxin production by three strains of Aspergillus ochraceus on a barley extract medium and on barley grains. Int. J. Food Microbiol. 1998, 44, 133–140. [Google Scholar]
  52. Kapetanakou, A.E.; Panagou, E.Z.; Gialitaki, M.; Drosinos, E.H.; Skandamis, P.N. Evaluating the combined effect of water activity, pH and temperature on ochratoxin A production by Aspergillus ochraceus and Aspergillus carbonarius on culture medium and Corinth raisins. Food Control 2009, 20, 725–732. [Google Scholar]
  53. Pardo, E.; Marín, S.; Sanchís, V.; Ramos, A.J. Prediction of fungal growth and ochratoxin A production by Aspergillus ochraceus on irradiated barley grain as influenced by temperature and water activity. Int. J. Food Microbiol. 2004, 95, 79–88. [Google Scholar]
  54. Pardo, E.; Marín, S.; Sanchís, V.; Ramos, A.J. Impact of relative humidity and temperature on visible fungal growth and OTA production of ochratoxigenic Aspergillus ochraceus isolates on grapes. Food Microbiol. 2005, 22, 383–389. [Google Scholar] [CrossRef]
  55. Pardo, E.; Ramos, A.J.; Sanchís, V.; Marín, S. Modeling of the effects of water activity and growth of ochratoxigenic isolates of Aspergillus ochraceus on a green coffee-based medium. Int. J. Food Microbiol. 2005, 98, 1–9. [Google Scholar] [CrossRef] [PubMed]
  56. Pardo, E.; Marín, S.; Ramos, A.J.; Sanchís, V. Ecophysiology of ochratoxigenic Aspergillus ochraceus and Penicillium verrucosum isolates. Predictive models for fungal spoilage prevention—a review. Food Addit. Contam. 2006, 23, 398–410. [Google Scholar] [CrossRef] [PubMed]
  57. Arroyo, M.; Aldred, D.; Magan, N. Environmental factors and weak organic acid interactions have differential effects on control of growth and ochratoxin A production by Penicillium verrucosum isolates in bread. Int. J. Food Microbiol. 2005, 98, 223–231. [Google Scholar]
  58. Czaban, J.; Wróblewska, B.; Stochmal, A.; Janda, B. Growth of Penicillium verrucosum and production of ochratoxin A on nonsterilized wheat grain incubated at different temperatures and water content. Pol. J. Microbiol. 2006, 55, 321–331. [Google Scholar]
  59. Aldred, D.; Cairns-Fuller, V.; Magan, N. Environmental factors affect efficacy of some essential oils and resveratrol to control growth and ochratoxin A production by Penicillium verrucosum and Aspergillus westerdijkiae on wheat grain. J. Stored. Prod. Res. 2008, 44, 341–346. [Google Scholar]
  60. Mitchell, D.; Parra, R.; Aldred, D.; Magan, N. Water and temperature relations of growth and ochratoxin A production by Aspergillus carbonarius strains from grapes in Europe and Israel. J. Appl. Microbiol. 2004, 97, 439–445. [Google Scholar]
  61. Esteban, A.; Abarca, M.L.; Bragulat, M.R.; Cabañes, F.J. Study of the effect of water activity and temperature on ochratoxin A production by Aspergillus carbonarius. Food Microbiol. 2006, 23, 634–640. [Google Scholar] [CrossRef] [PubMed]
  62. Esteban, A.; Abarca, M.L.; Bragulat, M.R.; Cabañes, F.J. Effect of water activity on ochratoxin A production by Aspergillus niger aggregate species. Int. J. Food Microbiol. 2006, 108, 188–195. [Google Scholar] [CrossRef] [PubMed]
  63. Marín, S.; Bellí, N.; Lasram, S.; Chebil, S.; Ramos, A.J.; Ghorbel, A. Kinetics of ochratoxin A production and accumulation by Aspergillus carbonarius on synthetic grape medium at different temperature levels. J. Food Sci. 2006, 71, 196–199. [Google Scholar]
  64. Astoreca, A.; Magnoli, C.; Ramirez, M.L.; Combina, M.; Dalcero, A. Water activity and temperature effects on growth of Aspergillus niger, A. awamori and A. carbonarius isolated from different substrates in Argentina. Int. J. Food Microbiol. 2007, 119, 314–318. [Google Scholar] [CrossRef] [PubMed]
  65. Astoreca, A.; Magnoli, C.; Barberis, C.; Chiacchiera, S.M.; Combina, M.; Dalcero, A. Ochratoxin A production in relation to ecophysiological factors by Aspergillus section Nigri strains isolated from different substrates in Argentina. Sci. Total Environ. 2007, 388, 16–23. [Google Scholar] [CrossRef] [PubMed]
  66. Astoreca, A.; Barberis, C.; Magnoli, C.; Combina, M.; Dalcero, A. Ecophysiological factors effect on growth rate, lag phase and ochratoxin A production by Aspergillus niger aggregate strains in irradiated peanut seeds. Int. J. Food Microbiol. 2009, 129, 131–135. [Google Scholar] [CrossRef] [PubMed]
  67. Astoreca, A.; Magnoli, C.; Barberis, C.; Combina, M.; Chiacchiera, S.M.; Dalcero, A. Influence of ecophysiological factors on growth, lag phase and ochratoxin A production by Aspergillus niger aggregate strains in corn grains. Int. J. Food Microbiol. 2009, 129, 174–179. [Google Scholar] [CrossRef] [PubMed]
  68. Astoreca, A.; Magnoli, C.; Barberis, C.; Combina, M.; Dalcero, A. Growth and ochratoxin A production by Aspergillus niger group strains in coffee beans in relation to environmental factors. World Mycotoxin J. 2010, 3, 59–65. [Google Scholar] [CrossRef]
  69. Astoreca, A.; Magnoli, C.; Barberis, C.; Combina, M.; Dalcero, A. Aspergillus carbonarius growth and ochratoxin A production in irradiated dried grapes under different water activity and temperature conditions. World Mycotoxin J. 2010, 3, 175–182. [Google Scholar] [CrossRef]
  70. Bellí, N.; Ramos, A.J.; Coronas, I.; Sanchís, V.; Marín, S. Aspergillus carbonarius growth and ochratoxin A production on a synthetic grape medium in relation to environmental factors. J. Appl. Microbiol. 2005, 98, 839–844. [Google Scholar]
  71. Bellí, N.; Ramos, A.J.; Sanchís, V.; Marín, S. Effect of photoperiod and day-night temperatures simulating field conditions on growth and ochratoxin A production of Aspergillus carbonarius strains isolated from grapes. Food Microbiol. 2006, 23, 622–627. [Google Scholar]
  72. Bellí, N.; Marín, S.; Sanchís, V.; Ramos, A.J. Influence of water activity and temperature on growth of isolates of Aspergillus section Nigri obtained from grapes. Int. J. Food Microbiol. 2004, 96, 19–27. [Google Scholar] [CrossRef] [PubMed]
  73. Bellí, N.; Marín, S.; Coronas, I.; Sanchís, V.; Ramos, A.J. Skin damage, high temperature and relative humidity as detrimental factors for Aspergillus carbonarius infection and ochratoxin A production in grapes. Food Control 2007, 18, 1343–1349. [Google Scholar]
  74. Valero, A.; Farré, J.R.; Sanchís, V.; Ramos, A.J.; Marín, S. Effects of fungal interaction on ochratoxin A production by A. carbonarius at different temperatures and water activity. Int. J. Food Microbiol. 2006, 110, 160–164. [Google Scholar] [CrossRef] [PubMed]
  75. Valero, A.; Begum, M.; Hocking, A.D.; Marín, S.; Ramos, A.J.; Sanchís, V. Mycelial growth and ochratoxin A production by Aspergillus section Nigri on simulated grape medium in modified atmospheres. J. Appl. Microbiol. 2008, 105, 372–379. [Google Scholar]
  76. Selouane, A.; Bouya, D.; Lebrihi, A.; Decock, C.; Bouseta, A. Impact of some environmental factors on growth and production of ochratoxin A of/by Aspergillus tubingensis, A. niger, and A. carbonarius isolated from Moroccan grapes. J. Microbiol 2009, 47, 411–419. [Google Scholar] [CrossRef] [PubMed]
  77. Leong, S.L.; Hocking, A.D.; Scout, E.S. Effect of temperature and water activity on growth and ochratoxin A production by Australian Aspergillus carbonarius and A. niger isolates on a simulated grape juice medium. Int. J. Food Microbiol. 2006, 110, 209–216. [Google Scholar]
  78. Romero, S.M.; Fernández Pinto, V.; Patriarca, A.; Vaamonde, G. Ochratoxin A production by a mixed inoculum of Aspergillus carbonarius at different conditions of water activity and temperature. Int. J. Food Microbiol. 2010, 140, 277–281. [Google Scholar]
  79. Romero, S.M.; Patriarca, A.; Fernández Pinto, V.; Vaamonde, G. Effect of water activity and temperature on growth of ochratoxigenic strains of Aspergillus carbonarius isolated from Argentinean dried vine fruits. Int. J. Food Microbiol. 2007, 115, 140–143. [Google Scholar]
  80. Oueslati, S.; Lasram, S.; Ramos, A.J.; Marin, S.; Mliki, A.; Sanchís, V.; Ghorbel, A. Alternating temperatures and photoperiod effects on fungal growth and ochratoxin A production by Aspergillus carbonarius isolated from Tunisian grapes. Int. J. Food Microbiol. 2010, 139, 210–213. [Google Scholar]
  81. Bellí, N.; Ramos, A.J.; Sanchís, V.; Marín, S. Incubation time and water activity effects on ochratoxin A production by Aspergillus section Nigri strains isolated from grapes. Lett. Appl. Microbiol. 2004, 38, 72–77. [Google Scholar]
  82. Esteban, A.; Abarca, M.L.; Bragulat, M.R.; Cabañes, F.J. Effects of temperature and incubation time on production of ochratoxin A by black aspergilli. Res. Microbiol. 2004, 155, 861–866. [Google Scholar]
  83. O’Callaghan, J.; Caddick, M.X.; Dobson, A.D.W. A polyketide synthase gene required for ochratoxin A biosynthesis in Aspergillus ochraceus. Microbiology 2003, 149, 3485–3491. [Google Scholar]
  84. Abbas, A.; Valez, H.; Dobson, A.D. Analysis of the effect of nutritional factors on OTA and OTB biosynthesis and polyketide synthase gene expression in Aspergillus ochraceus. Int. J. Food Microbiol. 2009, 135, 22–27. [Google Scholar]
  85. Schmidt-Heydt, M.; Baxter, E.; Geisen, R.; Magan, N. Physiological relationship between food preservatives, environmental factors, ochratoxin and otapksPV gene expression by Penicillium verrucosum. Int. J. Food Microbiol. 2007, 119, 277–283. [Google Scholar]
  86. Geisen, R. Molecular monitoring of environmental conditions influencing the induction of ochratoxin A biosynthesis genes in Penicillium nordicum. Mol. Nutr. Food Res. 2004, 48, 532–540. [Google Scholar]
  87. Marín, S.; Sanchís, V.; Ramos, A.J.; Vinas, I.; Magan, N. Environmental factors, in vitro interactions, and niche overlap between Fusarium moniliforme, F. proliferatum and F. graminearum, Aspergillus and Penicillium species from maize grain. Mycol. Res. 1998, 102, 831–837. [Google Scholar] [CrossRef]
  88. Marín, S.; Hodžić, I.; Ramos, A.J.; Sanchís, V. Predicting the growth/no-growth boundary and ochratoxin A production by Aspergillus carbonarius in pistachio nuts. Food Microbiol. 2008, 25, 683–689. [Google Scholar]

Share and Cite

MDPI and ACS Style

Astoreca, A.L.; Magnoli, C.E.; Dalcero, A.M. Ecophysiology of Aspergillus Section Nigri Species Potential Ochratoxin A Producers. Toxins 2010, 2, 2593-2605. https://doi.org/10.3390/toxins2112593

AMA Style

Astoreca AL, Magnoli CE, Dalcero AM. Ecophysiology of Aspergillus Section Nigri Species Potential Ochratoxin A Producers. Toxins. 2010; 2(11):2593-2605. https://doi.org/10.3390/toxins2112593

Chicago/Turabian Style

Astoreca, Andrea L., Carina E. Magnoli, and Ana M. Dalcero. 2010. "Ecophysiology of Aspergillus Section Nigri Species Potential Ochratoxin A Producers" Toxins 2, no. 11: 2593-2605. https://doi.org/10.3390/toxins2112593

APA Style

Astoreca, A. L., Magnoli, C. E., & Dalcero, A. M. (2010). Ecophysiology of Aspergillus Section Nigri Species Potential Ochratoxin A Producers. Toxins, 2(11), 2593-2605. https://doi.org/10.3390/toxins2112593

Article Metrics

Back to TopTop