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<I>Aspergillus</I> Section 702 Journal of Food Protection, Vol. 76, No. 4, 2013, Pages 702–706 doi:10.4315/0362-028X.JFP-12-431 Research Note Distribution and Mycotoxigenic Potential of Aspergillus Section Nigri Species in Naturally Contaminated Almonds JEFFREY D. PALUMBO* AND TERESA L. O’KEEFFE U.S. Department of Agriculture, Agricultural Research Service, Plant Mycotoxin Research Unit, Albany, California 94710, USA MS 12-431: Received 28 September 2012/Accepted 9 December 2012 ABSTRACT In a previous study, inedible almond pick-out samples were assayed for aflatoxin and aflatoxigenic Aspergillus species. These samples contained high populations of black-spored Aspergillus section Nigri species. To investigate whether these species may contribute to the total potential mycotoxin content of almonds, Aspergillus section Nigri strains were isolated from these samples and assayed for ochratoxin A (OTA) and fumonisin B2 (FB2). The majority of isolates (117 strains, 68%) were identified as Aspergillus tubingensis, which do not produce either mycotoxin. Of the 47 Aspergillus niger and Aspergillus awamori isolates, 34 strains (72%) produced FB2 on CY20S agar, and representative strains produced lower but measurable amounts of FB2 on almond meal agar. No OTA-producing strains of Aspergillus section Nigri were detected. Almond pick-out samples contained no measurable FB2, suggesting that properly dried and stored almonds are not conducive for FB2 production by resident A. niger and A. awamori populations. However, 3 of 21 samples contained low levels (,1.5 ng/g) of OTA, indicating that sporadic OTA contamination may occur but may be caused by OTA-producing strains of other Aspergillus species. The California almond industry produces 80% of the fumonisin B2 (FB2), one of several carcinogenic and world’s supply of almonds. After harvesting, almonds are cytotoxic fumonisin mycotoxins (14, 16). Fumonisins stored in stockpiles until they are transported to processors, currently are not regulated in commodities other than maize where they are hulled, shelled, sorted, graded, and either (11, 33), but the recent demonstration that FB2 produced by stored in bulk or packaged for sale. Sorting is performed at Aspergillus species can be found in grapes, wine, and raisins least once after shelling, particularly to remove nuts that (20–23, 35) suggests that these fungi might contribute to show visible mechanical or insect damage. Damaged nuts health risks in other commodities. are associated with increased risk for aflatoxin contamina- Although Aspergillus section Nigri species have been tion (31), and almonds that are sorted out (‘‘pick-outs’’) are found on almonds (5), very little is known about the risks of deemed inedible by processors. In the harvest years between mycotoxin contamination in this situation. Therefore, the 2001–2002 and 2010–2011, inedible nuts represented 1 to goals of this study were to characterize Aspergillus section 2% of each year’s crop (3). Nigri populations found in almond pick-out samples and to In a recent study of volatile compounds released from determine the mycotoxigenic potential of these populations. almond pick-out samples, Beck et al. (7) found high To accomplish these goals, both almond samples and aflatoxin levels and recovered Aspergillus flavus and isolated fungal strains were assayed for OTA and FB2 by Aspergillus parasiticus from these nuts. During that study, high-performance liquid chromatography (HPLC) methods. the authors also found a high incidence of black-spored MATERIALS AND METHODS aspergilli, members of Aspergillus section Nigri (6). This section contains several species, including A. carbonarius, Isolation of Aspergillus section Nigri strains. Twenty-one A. niger, A. awamori, A. tubingensis, and A. brasiliensis almond pick-out samples were provided previously by the Almond (1, 30, 34). A. carbonarius and certain strains of A. niger Board of California from almond processors in the California and A. awamori produce ochratoxin A (OTA), a mycotoxin Central Valley. As previously described (7), 7 of the 21 samples had been blanched during commercial processing (Table 1). characterized as nephrotoxic, carcinogenic, teratogenic, Almond samples were finely ground with an Electrolux Assistent immunosuppressive, and cytotoxic (12, 17, 18, 28). OTA food processor with a nut grater attachment (Magic Mill USA, concentrations in many commodities are regulated in the Upper Saddle River, NJ) and stored at 220uC until used. To European Union and other countries (10), which makes this enumerate total fungi and Aspergillus species from each sample, 3 g toxin an important consideration for exported tree nuts. In of ground almonds was added to 27 ml of sterile 0.05% Tween 80 addition, many strains of A. niger and A. awamori produce diluent and mixed by vortexing for 1 min. Almond suspensions were serially diluted in 0.05% Tween 80 diluent, and dilutions * Author for correspondence. Tel: 510-559-5876; Fax: 510-559-5737; were spread plated on dichloran–rose bengal–chloramphenicol E-mail: [email protected]. agar (DRBC). For recovery of A. carbonarius, dilutions were J. Food Prot., Vol. 76, No. 4 ASPERGILLUS SECTION NIGRI SPECIES IN ALMONDS 703 TABLE 1. Fungal populations recovered from almond samples Aspergillus section Nigri Mean ¡ SD total fungus Sample no. population (CFU/g) Mean ¡ SD population (CFU/g) % of total fungal population 1 7.15 ¡ 0.07 | 104 2.40 ¡ 0.28 | 103 3.4 2 2.55 ¡ 0.64 | 104 1.05 ¡ 0.07 | 104 41.2 3a 6.65 ¡ 0.21 | 104 1.25 ¡ 0.50 | 104 18.8 4 1.80 ¡ 0.00 | 103 1.00 ¡ 0.00 | 103 55.6 5 7.00 ¡ 0.28 | 104 4.30 ¡ 0.42 | 104 61.4 6a 3.05 ¡ 0.21 | 104 3.00 ¡ 0.00 | 102 1.0 7a ,10 ,10 NDb 8 5.25 ¡ 1.91 | 103 3.70 ¡ 1.56 | 103 70.5 9 5.05 ¡ 1.77 | 104 4.60 ¡ 2.97 | 103 9.1 10a 9.00 ¡ 1.41 | 102 5.00 ¡ 0.00 | 102 55.6 11a 5.00 ¡ 7.07 | 101 5.00 ¡ 7.07 | 101 100 12 1.60 ¡ 0.00 | 104 3.40 ¡ 1.60 | 103 21.3 13 6.40 ¡ 0.71 | 103 3.30 ¡ 0.42 | 103 51.6 14a ,10 ,10 ND 15 2.00 ¡ 0.28 | 104 8.50 ¡ 0.42 | 103 42.5 16a 4.00 ¡ 2.83 | 102 ,10 ND 17 1.90 ¡ 0.28 | 105 6.15 ¡ 1.34 | 104 32.4 18 4.70 ¡ 0.14 | 104 2.55 ¡ 0.07 | 104 54.3 19 1.45 ¡ 0.37 | 104 6.50 ¡ 0.71 | 102 4.5 20 3.50 ¡ 1.13 | 104 1.00 ¡ 0.14 | 104 28.6 21 1.32 ¡ 0.11 | 105 1.20 ¡ 0.14 | 105 90.9 a Blanched almond samples. b ND, not determined. plated on malt extract agar containing 10 mg/ml boscalid (MEA-B) Tool (BLAST) analyses (National Center for Biotechnology (29). Plates were incubated at 28uC for 3 days. Isolates of Information, Bethesda, MD). Aspergillus section Nigri, recognizable by dark brown to black sporulation, were transferred to potato dextrose agar for mainte- Mycotoxin analyses of almonds. For analysis of OTA and nance, and conidial suspensions of these isolates were stored in FB2 in each almond pick-out sample, 25 g of ground almonds and 0.05% Tween 80 plus 30% glycerol at 280uC. 2.5 g of NaCl were blended with 100 ml of 70% methanol for 1 min in a blender (Waring, Torrington, CT) and filtered through P8 Identification of Aspergillus species. DNA from Aspergillus coarse fluted filter paper (Fisher Scientific, Santa Clara, CA). strains was isolated as previously described (25). Conidia of each Lipids were partially removed by mixing 20 ml of filtrate with an fungal strain were inoculated into 1 ml of potato dextrose broth in equal volume of cyclohexane in a separatory funnel. After phase 1.5-ml microcentrifuge tubes and grown for 24 h at 28uC with separation, the aqueous fraction was collected and adjusted to 20 ml shaking at 150 rpm. Fungal biomass was collected by centrifugation with 70% methanol. For OTA purification, 10 ml of extract was at 15,000 | g for 10 min and homogenized with a Teflon diluted 1:5 with phosphate-buffered saline (PBS) plus 0.01% microcentrifuge tube pestle (Bel-Art Products, Pequannock, NJ) Tween 20 and filtered with 0.22-mm-pore-size Millex-GP poly- attached to a rotary tool (model 750, Dremel, Racine, WI). Genomic ethersulfone syringe filters (Millipore, Bedford, MA). Twenty DNA was isolated from homogenates with a MasterPure Yeast DNA milliliters of each diluted extract was applied to an OchraTest purification kit (Epicentre Biotechnologies, Madison, WI) and immunoaffinity column (VICAM, Milford, MA), columns were diluted 1:10 with sterile water for use as PCR templates. Fragments washed as recommended by the manufacturer, and OTA was of b-tubulin and calmodulin genes were amplified with primer eluted in 1.5 ml of methanol. To quantify OTA, 50 ml of each sets Bt2a (59-GGTAACCAAATCGGTGCTGCTTTC-39) and Bt2b sample was separated using an HPLC system (model 1100, Agilent (59-ACCCTCAGTGTAGTGACCCTTGGC-39) (15) and CF1L Technologies, Santa Clara, CA). Separations were performed on an (59-GCCGACTCTTTGACYGARGAR-39) and CF4 (59-TTTYTG- Inertsil ODS 3 column (5 mm, 4.6 by 250 mm; GL Sciences, Inc., CATCATRAGYTGGAC-39) (27), respectively. PCR conditions as Torrance, CA), with acetonitrile–0.1% phosphoric acid (65:35) as follows: 95uC for 5 min; 35 cycles of 95uC for 30 s, 61uC (for Bt2a/ the mobile phase at a flow rate of 1 ml/min. OTA was detected by Bt2b) or 52uC (for CF1L/CF4) for 30 s, and 72uC for 1 min; and fluorescence, with excitation and emission wavelengths of 333 and 72uC for 5 min. Amplified fragments were purified with the Clean & 460 nm, respectively. OTA was quantified from peak areas relative Concentrator-5 Kit (Zymo Research Corp., Irvine, CA), sequenced to a standard curve consisting of authentic OTA recovered from with the same primers with BigDye v.
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