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Article

Occurrence of Aspergillus chevalieri and A. niger on Herbal Tea and Their Potential to Produce Ochratoxin A (OTA)

by
Maryam T. Noorabadi
1,2,†,
Antonio Roberto Gomes de Farias
2,
Ausana Mapook
2,
Kevin D. Hyde
1,2,3,* and
Saranyaphat Boonmee
1,2,*,†
1
School of Science, Mae Fah Luang University, Chiang Rai 57100, Thailand
2
Center of Excellence in Fungal Research, Mae Fah Luang University, Chiang Rai 57100, Thailand
3
Innovative Institute for Plant Health, Zhongkai University of Agriculture and Engineering, Guangzhou 510225, China
*
Authors to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Diversity 2023, 15(12), 1183; https://doi.org/10.3390/d15121183
Submission received: 14 November 2023 / Revised: 27 November 2023 / Accepted: 27 November 2023 / Published: 29 November 2023
(This article belongs to the Special Issue The Hidden Fungal Diversity in Asia 2.0)
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Abstract

:
Herbal teas, including Camellia sinensis (black and green teas), are popular beverages with health benefits for consumers worldwide. These products are prepared from natural materials of different plant parts containing antioxidant properties and vitamins. The aim of this study was to investigate fungal contaminants and their ability to produce ochratoxin A (OTA) in herbal tea samples. Seven herbal teas were obtained from local markets in Chiang Rai, northern Thailand. Samples were incubated on potato dextrose agar (PDA), and the growing mycelia were isolated into a pure culture. The cultures were identified via both morphology and molecular analysis to confirm species identification. The identified species were subjected to OTA analysis using high-performance liquid chromatography (HPLC) with a fluorescence detector. Ochratoxin A was produced by Aspergillus chevalieri and A. niger, isolated from seven herbal tea samples (black tea, green tea, bael fruit, goji berry, jasmine, lavender, and rose). This finding raises concerns about the safety of herbal tea and should be investigated further for potential health implications.

1. Introduction

Phytotherapeutic sources have become important for healthy drink and food consumption and healthcare. Herbal teas have become popular beverages [1,2], with Camellia sinensis L. tea being the most consumed drink in the world [3]. In this paper, herbal tea refers to the aromatic brewing of diverse parts of plants known as herbs (such as leaves, flowers, seeds, bark, stems, and roots) [4,5,6].
The naturally occurring bioactive substances or phytochemicals in herbal teas are released through infusion [7,8,9]. These bioactive compounds include antioxidants and other therapeutic properties, while tea contains rather high amounts of caffeine [1,4,10]. Some of the most popular herbal teas include bael fruit, chamomile, chrysanthemum, jasmine, lavender, marigold, pomegranate, safflower, and rose [11,12,13]. In Thailand, there are several popular flower teas, such as butterfly-pea, chrysanthemum, jasmine flower, rose, roselle, or safflower. They contain color, flavor, taste, fragrance, aesthetic qualities, and antioxidant activities [14,15]. However, most of the herbal teas are produced by local farmers and do not undergo quality inspections, unlike tea products processed by the industry. Some of these herbal plants have been shown to be contaminated by toxigenic fungi in Asian countries such as China, India, Sri Lanka, and Thailand [16].
Herbal tea products include several parts of dried plants, which are suitable substrates for the growth of microorganisms, especially toxicogenic fungi [16,17,18,19]. In the natural environment, fungi habitually grow on organic and inorganic substrates [20,21,22]. Their presence can negatively impact human health, cause infectious diseases, and contaminate food or food ingredients [23,24]. They can also deteriorate agricultural food crops and products under poor post-harvest facilities [25]. A large number of foodborne fungi, also known as storage fungi, are able to produce one or more toxic secondary metabolites (mycotoxins) that cause a wide array of negative effects and other complications in animals and humans [26,27,28].
In Thailand, climatic conditions characterized by high temperatures and high humidity promote the growth of fungi that can produce mycotoxins [29,30,31,32]. Therefore, several agricultural commodities are subjected to mycotoxin contamination such as animal feed, beans, cereal grains, spices, leguminous plants, dried fruits, mushrooms, herbs, and teas [32,33,34,35,36,37]. Several fungal genera can produce mycotoxins, with the most prevalent species being, e.g., aflatoxins (Aspergillus flavus, A. parasiticus), fumonisins (Fusarium verticillioides), ochratoxins (A. ochraceus, Penicillium verrucosum), sterigmatocystin (A. versicolor), trichothecenes (F. graminearum), and zearalenone (F. graminearum) [38,39,40,41,42,43,44,45,46,47].
Ochratoxin A, produced by species within Aspergillus and Penicillium, is one of the most significant toxins that affects agricultural products and human health worldwide [48,49]. Magan and Aldred [50] reported that A. niger within section Nigri, especially A. carbonarius, can produce OTA contamination in grapes, wine, and vine fruits. Han et al. [51] reported OTA contamination in the Chinese food industry from some strains of A. niger. On the other hand, A. chevalieri produces aflatoxins, citrinin, flavoglaucin, gliotoxin, and sterigmatocystin, but OTA production has not been reported in this species [52,53,54,55].
In this study, we investigated the potential of Aspergillus species isolated from herbal tea samples from local markets in Chiang Rai Province and their ability to produce OTA. A. chevalieri and A. niger isolated from seven herbal tea samples were found to produce OTA. The species were identified and are illustrated using both morphological and molecular data. The implications of detecting these species in such products are discussed.

2. Materials and Methods

2.1. Samples Collection and Fungal Isolation

Herbal teas were randomly purchased from five local markets in Chiang Rai Province (Doi Mae Salong, Fah Thai, Mae Sai, and Lan Muang). They included bael fruit, Camellia sinensis (black and green teas), jasmine, goji berry, lavender, and rose (Table 1). Isolation of fungi from the samples was performed under sterile conditions following the method described by Senanayake et al. [56]. One random piece of each tea sample was placed directly on potato dextrose agar (PDA) and incubated at 25 °C for 5 days. Mycelia growing from the herbal tea samples were individually transferred to fresh PDA plates to obtain pure cultures and for identification.

2.2. Macro- and Microscopic Identification of Fungi

Macroscopic and microscopic characteristics were examined by following the identification methods used in previous studies [57,58,59] and structures were measured following Senanayake et al. [56]. Macro- and micro-characteristics, such as conidiophores, conidiogenous cells, and conidia, were observed and photographed using the Nikon Eclipse Ni-U compound microscope connected to the Nikon DS-Ri2 digital camera. The photoplates were prepared with Adobe Photoshop CS3 Extended version 10.0 software (Adobe Systems, San Jose, CA, USA). Specimens were deposited at the Fungarium of Mae Fah Luang University (MFLU), and living cultures were deposited at Mae Fah Luang University Culture Collection (MFLUCC), Chiang Rai, Thailand.

2.3. DNA Extraction, PCR Amplification, Sequencing, and Phylogenetic Analyses

Genomic DNA was extracted from fresh mycelium colonies grown on PDA using the manufacturer’s protocol for Genomic DNA Extraction Kits (OMEGA Bio-Tek Inc., Norcross, GA, USA). Four gene regions were amplified using the corresponding pairs of primers: the internal transcribed spacer (ITS), ITS5/ITS4 [60,61]; β-tubulin (BenA), Bt2a/Bt2b [62,63]; calmodulin (CaM), CMD5/CMD6, CL1/CL2A [63,64]; and RNA polymerase II second largest subunit (RPB2), RPB2f-5f/RPB2f-7cr [65].
Polymerase chain reaction (PCR) was performed in a volume of 25 µL reaction process containing 12.5 µL of 2× Power Taq PCR Master Mix, 1 µL of each primer (20 µM), and 1 µL of 50 ng of DNA template in 9.5 µL of deionized water. PCR amplification conditions for each gene were performed following previous studies (Table 2). The PCR products were purified according to the company protocols and DNA sequencing was performed using Sanger sequencing at Solgent Co., Ltd., Daejeon, South Korea.
Phylogenetic analyses to identify fungal species were performed as described in Dissanayake et al. [69]. The fungal sequence data obtained from this study were deposited in GenBank (Table 3 and Table 4).

2.4. OTA Extraction and Quantification

Isolates of A. chevalieri and A. niger were grown on yeast extract sucrose agar (YES) [68,70,71] and incubated at 25 °C in darkness for 14 days for OTA production [70]. Small pieces of culture agar plugs (6 mm diameter) of each isolate were transferred to 50 mL centrifuge tubes, and 16 mL methanol (HPLC grade) was added, followed by orbital shake at 230 rpm for 60 min, vortexing at every 20 min, and centrifugation at 2683× g (5000 rpm) for 15 min [48,72]. Five microliters of the solution were collected and evaporated to dryness under a nitrogen stream at 50 °C [48,73,74]. The dried extracts were dissolved in 1 mL of methanol, filtered through a 0.22 µm Polyvinylidene difluoride (PVDF) membrane filter into 2 mL amber vials, and sent to the Scientific and Technological Instruments Center (STIC), Mae Fah Luang University, for HPLC analysis. The analyses were performed on a Waters HPLC System with a 2998 PDA detector, following the manufacturer’s instructions.

3. Results

3.1. Phylogenetic Analyses

Phylogenetic analyses were performed using two separate datasets, one for Aspergillus section Aspergillus and the other for Aspergillus section Nigri. Maximum likelihood and Bayesian phylogenetic trees from combined DNA sequences of BenA, CaM, ITS, and RPB2 gene regions had the same topology. The sequence dataset of Aspergillus section Aspergillus consists of 62 taxa (Table 3). Our six isolates (MFLUCC 23-0094, MFLUCC 23-0095, MFLUCC 23-0096, MFLUCC 23-0097, MFLUCC 23-0184, and MFLUCC 23-0185) are clustered with A. chevalieri with 100% MLBS/1.00 BYPP support (Figure 1). We, therefore, identify these strains as A. chevalieri (Table 5).
The sequence dataset of Aspergillus section Nigri consists of 51 taxa (Table 4). Our five isolates (MFLUCC 23-0192, MFLUCC 23-0193, MFLUCC 23-0194, MFLUCC 23-0195, and MFLUCC 23-0200) clustered with A. niger with 100% MLBS/1.00 BYPP support (Figure 2). We, therefore, identify these strains as A. niger (Table 5).

3.2. Taxonomy

3.2.1. Aspergillus chevalieri (L. Mangin) Thom & Church, The Genus Aspergillus: 111 (1926)

Index Fungorum: IF292839; Facesoffungi number: FoF 14734; Figure 3.
Colonies on PDA 16.5–26 mm diameter in 7 days at 25 °C, initially white, gradually becoming light yellow from the center outwards, granulose due to the presence of ascomata, sporulation abundant, with conidial masse olive green, margin entire.
Conidiophores up to 247 × 4–6 µm, uniseriate with radiating conidial heads, stipes hyaline to subhyaline, smooth-walled. Vesicles 24–46 µm diameter, subglobose to pyriform, hyaline, smooth-walled. Phialides variable in shape and size, ampulliform to cylindrical. Conidia 3–6 × 2–5 µm, globose to subglobose, sometimes pyriform, hyaline, rough-walled. Ascomata 118–128 µm diameter, cleistothecium, globose to subglobose, light yellow to yellow, surrounded by hyaline to light brown hyphae. Peridium consisting of one layer of textura angularis to textura globulosa, light yellow, smooth-walled. Asci 8–10 µm diameter, globose to subglobose, thin-walled. Ascospores 3–4 × 4–5 µm, globose to subglobose, lenticular, aseptate, hyaline, with a slight furrow in the equatorial region, convex surface smooth-walled to finely roughened.
Material examined: Thailand, Chiang Rai Province, Mae Fah Luang District, Doi Mae Salong market, jasmine flower tea, 13 January 2022, Saranyaphat Boonmee, JM1–1A(CR), MFLU MFLU23-0273, living culture MFLUCC 23-0095, JM1–2A(CR), MFLU 23-0272, living culture MFLUCC 23-0094, JM3–2A(CR), MFLU 23-0274, living culture MFLUCC 23-0096; rose flower tea, 13 January 2022, Saranyaphat Boonmee RF3-1A(CR), MFLU 23-0275, living culture MFLUCC 23-0097; beal fruit, 10 June 2022, Maryam Tavakol Noorabadi, INB-043, MFLU 23-0365, living culture MFLUCC 23-0184; black tea, 10 June 2022, Maryam Tavakol Noorabadi, Btea-47, MFLU 23-0366, living culture MFLUCC 23-0185.
Notes: Six isolates obtained from this study clustered with the clade A. chevalieri (DTO 092-D3, CBS 522.65, and CBS141769) based on the phylogenetic analysis of BenA, Cam, ITS, and RPB2 sequence data (Figure 1). The isolates were morphologically identical to A. chevalieri strains (Figure 3). A. chevalieri is a member of section Aspergillus (formerly the genus Eurotium), which was described by Thom and Church [75]. They are generally characterized by yellow cleistothecia, lenticular, hyaline ascospores, and globose, subglobose, or ellipsoidal conidia [76,77]. This species produces some mycotoxins, such as aflatoxins, citrinin, gliotoxin, and sterigmatocystin, but it has not previously been shown to produce OTA [53,54,55,76,78,79,80]. In this study, we found that A. chevalieri isolated from herbal teas (bael fruit, black tea, jasmine flower, and rose flower) produced OTA.
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Figure 3. Aspergillus chevalieri (MFLUCC 23-0094). (a,b) Fungal isolation from jasmine flower samples on PDA. (c) Pure culture colony on PDA at 25 °C for 7 days from surface. (d,e) Ascomata. (f,g) Cleistothecial ascomata and peridium. (h,i) Asci and ascospores. (j,k) Phialides bearing apical uniseriate conidia. (l) Conidia. Scale bars: (d) = 500 µm, (e) = 100 µm, (f,g) = 50 µm, (h,i,l) = 10 µm, (j,k) = 20 µm.
Figure 3. Aspergillus chevalieri (MFLUCC 23-0094). (a,b) Fungal isolation from jasmine flower samples on PDA. (c) Pure culture colony on PDA at 25 °C for 7 days from surface. (d,e) Ascomata. (f,g) Cleistothecial ascomata and peridium. (h,i) Asci and ascospores. (j,k) Phialides bearing apical uniseriate conidia. (l) Conidia. Scale bars: (d) = 500 µm, (e) = 100 µm, (f,g) = 50 µm, (h,i,l) = 10 µm, (j,k) = 20 µm.
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3.2.2. Aspergillus niger Tiegh., Annls Sci. Nat., Bot., sér. 5 8: 240 (1867)

Index Fungorum: IF284309; Facesoffungi number: FoF 10087; Figure 4.
Colonies on PDA 57–63 mm diameter in 7 days at 25 °C, irregular, protuberant, margins narrow, entire. Mycelia white and then cream to light yellow, texture velutinous, soluble pigments yellow, exudates tiny, hyaline, and clear, reverse buff, yellow to orange, and with black sectors, from the center outwards, sporulation abundant, with conidial masse dark brown to black.
Conidiophores up to 730 × 12.5–16.5 µm, with biseriate, rarely uniseriate, radiating conidial heads, regularly splitting into columns, stipes smooth-walled to finely roughened, hyaline to light brown. Vesicles 55–78 µm, globose to subglobose, light brow to brown. Metulae 5.5–8.5 × 3–5 µm. Phialides 7.5–10.5 × 3.5–4.8 µm, ampulliform to cylindrical, smooth-walled. Conidia 3.5–5.5 µm, globose, brown to dark brown, coarsely rough to echinulate-walled.
Material examined: Thailand, Chiang Rai Province, Mae Fah Luang District, Doi Mae Salong, goji berry, 15 June 2022, Maryam Tavakol Noorabadi, Goji-41, MFLU 23-0373, living culture MFLUCC 23-0192; beal fruit, 5 June 2022, Maryam Tavakol Noorabadi, INB-50, MFLU 23-0374, living culture MFLUCC 23-0193; Chiang Rai Province, Mae Sai market, lavender flower tea, 5 June 2022, Maryam Tavakol Noorabadi, LAV-85, MFLU 23-0375, living culture MFLUCC 23-0194; Chiang Rai Province, Fah Thai market, green tea, 5 June 2022, Maryam Tavakol Noorabadi, GTEA-39, MFLU 23-0376, living culture MFLUCC 23-0195, and GTEA-78, MFLU 23-0377, living culture MFLUCC 23-0200.
Notes: Five isolates obtained from this study are phylogenetically (Figure 2) and morphologically similar to A. niger strains (Figure 4). This species belongs to the Aspergillus section Nigri. Bian et al. [81] revised the section Nigri based on BenA, CaM, and RPB2 sequence data and new whole-genome sequences for six species that comprise A. brasiliensis, A. eucalypticola, A. luchuensis, A. niger, A. tubingensis, and A. vadensis. Furthermore, A. niger in the section of Nigri can be mainly distinguished by significant differences in colony colors, vesicle, conidiophores, conidia, and sclerotia, i.e., micro- and macro-morphology [82,83,84,85]. A. vinaceus and A. welwitschiae are considered synonyms of A. niger [81]. Morphological comparisons with the ex-type of A. niger (CBS 139.54) indicated no differences between the type strain and our five isolates.
Diversity 15 01183 g004
Figure 4. Aspergillus niger (MFLUCC 23-0192). (a,b) Fungal isolation from goji berry samples. (c,d) Pure colonies on PDA, at 25 °C, after 7 days from surface and reverse, respectively. (e,f) Conidiophores and apical dark conidia. (g–i) Phialide with apical radiating biseriate conidia. (j) Vegetative mycelium. (k) Conidia. Scale bars: (e,g) = 100 µm, (f,h,i) = 50 µm, (j,k) = 10 µm.
Figure 4. Aspergillus niger (MFLUCC 23-0192). (a,b) Fungal isolation from goji berry samples. (c,d) Pure colonies on PDA, at 25 °C, after 7 days from surface and reverse, respectively. (e,f) Conidiophores and apical dark conidia. (g–i) Phialide with apical radiating biseriate conidia. (j) Vegetative mycelium. (k) Conidia. Scale bars: (e,g) = 100 µm, (f,h,i) = 50 µm, (j,k) = 10 µm.
Diversity 15 01183 g004

3.3. Mycotoxin Detection

The set of isolates (Figure 5), representing the different locations from where the various teas were bought, were tested for potential toxigenicity (Table 5). A. niger strains were shown to produce OTA with values ranging between 0.328 and 1.660 ng/L, while A. chevalieri strains produced OTA in the range between 0.663 and 39.182 ng/L (Figure 5).

4. Discussion

In this study, 137 isolates were obtained from herbal teas and teas from local markets in northern Thailand. Eleven isolates, of which six isolates belonged to A. chevalieri and five isolates belonged to A. niger, produced OTA. Phylogenetic trees obtained from the analysis of combined BanA, Cam, ITS, and RPB2 sequence data provided good resolution for identifying the Aspergillus isolates into two sections: (i) section Aspergillus = A. chevalieri (MFLUCC 23-0184, MFLUCC 23-0185, MFLUCC 23-0094, MFLUCC 23-0095, MFLUCC 23-0096, and MFLUCC 23-0097) and (ii) section Nigri = A. niger (MFLUCC 23-0192, MFLUCC 23-0194, MFLUCC 23-0195, MFLUCC 23-0200, and MFLUCC 23-0195). Aspergillus species are commonly isolated from tea samples. A. tubingensis, A. fumigatus, and A. marvanovae were isolated from China’s Pu-erh tea [86], while A. niger was obtained from black and green teas [87]. A. acidus, A. awamori, and A. tubingensis were isolated from herbal teas [88]. In this study, the contamination of herbal teas by Aspergillus species includes five new substrate records: A. chevalieri on bael fruit, black tea, jasmine, and rose flowers; and A. niger on bael fruit, goji berries, green tea, and lavender flowers (Table 5).
Environmental factors such as temperature, air wetness, and water activity play a significant role in influencing mycotoxin production and contamination levels in pre- and post-harvest products. Various studies have highlighted the impact of these factors [89,90,91,92,93,94]. Mycotoxin production is influenced not only by the genetic makeup but also by environmental conditions, such as those from northern Thailand, and potential host effects. In our study, all isolates of A. niger produced low amounts of OTA, which was probably due to environmental factors. The European Union specifies the maximum limits for ochratoxin A (OTA) in dried herbs of 10 μg/kg [95]. OTA production from A. chevalieri has not previously been reported [53,89,96]. OTA production was detected in six isolates of A. chevalieri in this study (Figure 5). This finding raises concerns about OTA contamination in herbal teas and highlights the need for further research and monitoring to ensure consumer safety.
In conclusion, the increasing concern over Aspergillus contaminants and mycotoxin production in teas necessitates further research and analysis of OTA to ensure consumer health and safety. Analyzing and monitoring fungal contamination in teas is essential to meet consumer expectations and demands. The discovery of OTA production by A. chevalieri underscores the importance of continued vigilance in this area.

Author Contributions

Conceptualization, M.T.N. and S.B.; data curation, M.T.N. and S.B.; methodology, M.T.N. and S.B.; resources, M.T.N. and S.B.; formal analysis, M.T.N., S.B., and A.R.G.d.F.; investigation, M.T.N., A.R.G.d.F. and S.B.; writing—original draft, M.T.N., A.R.G.d.F., A.M. and S.B.; writing—review and editing, M.T.N., A.R.G.d.F., A.M., K.D.H. and S.B.; supervision, M.T.N., A.R.G.d.F., A.M., K.D.H. and S.B.; project administration, S.B.; funding acquisition, M.T.N., A.R.G.d.F., A.M., K.D.H. and S.B. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Basic Research Fund supported by the National Science, Research, and Innovation Fund (Grant No. 652A01002).

Institutional Review Board Statement

Not applicable.

Data Availability Statement

The data presented in this study are available within the manuscript.

Acknowledgments

M.T.N. would like to thank the Post–Doctoral Fellowship Fund 2022 from Mae Fah Luang University. M.T.N. thanks Naruemon Huanraluek and Ishani D. Goonasekara for their help during molecular and HPLC analyses.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Phylogram generated from RAxML analysis based on combined BenA, CaM, ITS, and RPB2 sequence data of Aspergillus section Aspergillus taxa. A. osmophilus (CBS 134258) and A. xerophilus (CBS 938.73, NRRL 6132) are selected as the outgroup taxa. Bootstrap support values for ML values equal to or >60% and BYPP values equal to or >0.90 are shown as MLBS/BYPP above the nodes. Newly generated sequences in this study are in blue. Type strains are indicated in bold.
Figure 1. Phylogram generated from RAxML analysis based on combined BenA, CaM, ITS, and RPB2 sequence data of Aspergillus section Aspergillus taxa. A. osmophilus (CBS 134258) and A. xerophilus (CBS 938.73, NRRL 6132) are selected as the outgroup taxa. Bootstrap support values for ML values equal to or >60% and BYPP values equal to or >0.90 are shown as MLBS/BYPP above the nodes. Newly generated sequences in this study are in blue. Type strains are indicated in bold.
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Diversity 15 01183 g002
Figure 2. Phylogram generated from RAxML analysis based on combined BenA, CaM, ITS, and RPB2 sequence data of Aspergillus section Nigri taxa. A. flavus isolates (CBS 100927 and NRRL 447) are selected as the outgroup taxa. Bootstrap support values for ML values equal to or >60% and BYPP values equal to or >0.90 are shown as MLBS/BYPP above the nodes. Newly generated sequences in this study are in blue. Type strains are indicated in bold.
Figure 2. Phylogram generated from RAxML analysis based on combined BenA, CaM, ITS, and RPB2 sequence data of Aspergillus section Nigri taxa. A. flavus isolates (CBS 100927 and NRRL 447) are selected as the outgroup taxa. Bootstrap support values for ML values equal to or >60% and BYPP values equal to or >0.90 are shown as MLBS/BYPP above the nodes. Newly generated sequences in this study are in blue. Type strains are indicated in bold.
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Diversity 15 01183 g005
Figure 5. Analysis of OTA production by isolates of A. chevalieri and A. niger on YES at 25 °C for 14 days. (A,D) A. chevalieri (MFLUCC 23-0184) isolated from bael fruit and A. niger isolates from green tea (MFLUCC 23-0195), respectively. (B,E) UV absorbance traces of extracts from MFLUCC 23-0184 and MFLUCC 23-0195. (C,F) Amount of OTA production by different isolates of A. chevalieri and A. niger.
Figure 5. Analysis of OTA production by isolates of A. chevalieri and A. niger on YES at 25 °C for 14 days. (A,D) A. chevalieri (MFLUCC 23-0184) isolated from bael fruit and A. niger isolates from green tea (MFLUCC 23-0195), respectively. (B,E) UV absorbance traces of extracts from MFLUCC 23-0184 and MFLUCC 23-0195. (C,F) Amount of OTA production by different isolates of A. chevalieri and A. niger.
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Table 1. Tea and herbal teas used in this study obtained from local markets in northern Thailand.
Table 1. Tea and herbal teas used in this study obtained from local markets in northern Thailand.
No.Herbal TeaScientific Name and FamilyHerbal Tea
Substrate		Number of Samples
(Package)		Local Markets
1Black TeaCamellia sinensis, Theaceaeleaves6Doi Mae Salong
Fah Thai
Mae Sai
2Bael FruitAegle marmelos, Rutaceaefruits4Doi Mae Salong
Fah Thai
Mae Sai
3Goji BerryLycium sp., Solanaceae fruits2Doi Mae Salong
Fah Thai
4Green TeaCamellia sinensis, Theaceaeleaves6Doi Mae Salong
Mae Sai
Lan Muang
5JasmineJasminum sp., Oleaceaeflowers2Doi Mae Salong
6LavenderLavandula sp., Lamiaceaeflowers4Lan Muang
Mae Sai
7RoseRosa sp., Rosaceaeflowers2Doi Mae Salong
Table 2. PCR amplification conditions used in the thermal cycler of each gene.
Table 2. PCR amplification conditions used in the thermal cycler of each gene.
GenePrimers
(Forward/Reverse)		PCR ConditionReferences
β-tubulin
(BenA)		Bt2a/Bt2b1 cycle at 94 °C for 3 min; 35 cycles of 94 °C for 30 s; 55 °C for 50 s; 72 °C for 1 min; and a final extension at 72 °C for 10 minFrisvad et al. [58],
Hubka et al. [66,67], Samson et al. [68]
Calmodulin
(CaM)		CMD5/CMD6
CL1/CL2A		1 cycle at 95 °C for 5 min; 35 cycles of 94 °C for 45 s; 55 °C for 45 s; 72 °C for 1 min; and a final extension at 72 °C for 10 min Frisvad et al. [58],
Hubka et al. [66,67], Samson et al. [68]
Internal transcribed spacer
(ITS)		ITS5/ITS41 cycle at 94 °C for 3 min; 35 cycles of 94 °C for 30 s; 55 °C for 50 s; 72 °C for 1 min; and a final extension at 72 °C for 10 minFrisvad et al. [58],
Hubka et al. [66,67], Samson et al. [68]
RNA polymerase II
second largest subunit(RPB2)		RPB2f-5f/RPB2f-7cr1 cycle at 95 °C for 5 min; 40 cycles of 95 °C for 1 min; 57 °C for 1 min; 72 °C for 1 min; and a final extension at 72 °C for 10 minFrisvad et al. [58],
Samson et al. [68]
Table 3. GenBank and culture collection numbers of Aspergillus section Aspergillus used in the phylogenetic analysis. The newly generated sequences are indicated in blue.
Table 3. GenBank and culture collection numbers of Aspergillus section Aspergillus used in the phylogenetic analysis. The newly generated sequences are indicated in blue.
TaxaCulture Collection
No.		GenBank Accession No.
ITSBenACAMRPB2
A. aeriusCBS 141771LT670916LT670990LT670991LT670992
A. appendiculatusCBS 101746HE615133HE801334HE801319HE801308
A. appendiculatusCBS 374.75 THE615132HE801333HE801318HE801307
A. aurantiacoflavusCBS 141930 TLT670917LT670993LT670994LT670995
A. aurantiacoflavusCCF 5391LT670918LT670996LT670997LT670998
A. brunneusCBS 113.27EF652056EF651904EF651997EF651938
A. brunneusCBS 112.26 TEF652060EF651907EF651998EF651939
A. caperatusCBS 141774 TLT670922LT671008LT671009LT671010
A. chevalieriDTO 092-D3LT670929LT671029LT671030LT671031
A. chevalieriCBS 141769LT670927LT671023LT671024LT671025
A. chevalieriCBS 522.65 TEF652068EF651911EF652002EF651954
A. chevalieriMFLUCC 23-0094OR478693OR508967N/AN/A
A. chevalieriMFLUCC 23-0095OR478694OR508966OR508963N/A
A. chevalieriMFLUCC 23-0096OR478695OR508968OR508964N/A
A. chevalieriMFLUCC 23-0097OR478696OR508969OR508965N/A
A. chevalieriMFLUCC 23-0184OR502380OR573934OR604627OR604629
A. chevalieriMFLUCC 23-0185OR501403OR573933N/AOR604628
A. cibariusKACC 46346 TJQ918177JQ918180JQ918183JQ918186
A. cibariusKAC 46764JQ918178JQ918184JQ918181JQ918187
A. costiformisCBS 101749 THE615136HE801338HE801320HE801309
A. cristatusCBS 123.53 TEF652078EF651914EF652001EF651957
A. cumulatusKACC 47316KF928303KF928297KF928300KF928294.
A. endophyticusCBS 141766 TLT670941LT671067LT671068LT671069
A. equitisNRRL 25823EF652073EF651895EF652015EF651961
A. glaucusCBS 516.65 TEF652052EF651989EF651887EF651934
A. glaucusNRRL 117EF652053EF651990EF651888EF651935
A. heterocaryoticusNRRLA-13891 TEU021619EU021670EU021687EU021659
A. intermediusCBS 377.75HE974459HE974432HE974437HE974425
A. intermediusCBS 523.65 TEF652074EF651892EF652012EF651958
A. leucocarpusCBS 353.68 TEF652087EF651925EF652023EF651972
A. levisporusCBS 141767 TLT670950LT671094LT671095LT671096
A. mallochiiCBS 141928 TKX450907KX450889KX450902KX450894
A. mallochiiCBS 141776KX450908KX450890KX450903KX450895
A. megasporusCBS 141772KX450911KX450893KX450906KX450898
A. megasporusCBS 141929 TKX450910KX450892KX450905KX450897
A. microperforatusCBS 142376 TLT627271LT627296LT627321LT627346
A. microperforatusUTHSCSADI16-400LT627270LT627295LT627320LT627345
A. montevidensisCBS 518.65EF652076EF651897EF652017EF651963
A. montevidensisCBS 491.65 TEF652077EF651898EF652020EF651964
A. neocarnoyiEXF-10029LT670955LT671109LT671110LT671111
A. neocarnoyiCBS 471.65 TEF652057EF651903EF651985EF651942
A. niveoglaucusCBS 101750HE615135HE801331HE801323HE801312
A. niveoglaucusCBS 114.27 TEF652058EF651905EF651993EF651943
A. osmophilusCBS 134258 TKC473921KC473924KC473918KX512310
A. porosusCBS 375.75LT670963LT671136LT671137LT671138
A. porosusCBS 141770 TLT670961LT671130LT671131LT671132
A. proliferansCBS 121.45 TEF652064EF651891EF651988EF651941
A. proliferansNRRL 114EF652051EF651886EF651987EF651933
A. pseudoglaucusCBS 379.75HE615131HE801336HE801322HE801311
A. pseudoglaucusCBS 123.28 TEF652050EF651917EF652007EF651952
A. ruberCBS 530.65 TEF652066EF651920EF652009EF651947
A. ruberCBS 101748HE615134HE801337HE801325HE801315
A. sloaniiCBS 138178KJ775542KJ775076KJ775313KX450900
A. sloaniiCBS 138177 TKJ775540KJ775074KJ775309KX463365
A. tamarindosoliCBS 141775 TLT670981LT671191LT671192LT671193
A. teporisCBS 141768 TLT670982LT671194LT671195LT671196
A. tonophilusCBS 405.65 TEF652081EF651919EF652000EF651969
A. umbrosusNRRL120EF652054EF651889EF651991EF651936
A. xerophilusCBS 938.73 TEF652085EF651923EF651983EF651970
A. xerophilusNRRL 6132EF652086EF651924EF651984EF651971
A. zutongqiiCGMCC 3.06103LT670989LT671215LT671216LT671217
A. zutongqiiCBS 141773 TLT670986LT671206LT671207LT671208
Note: The ex-type cultures are marked as “T”, and “N/A” indicates sequence is unavailable.
Table 4. GenBank and culture collection numbers of Aspergillus section Nigri used in the phylogenetic analysis. The newly generated sequences are indicated in blue.
Table 4. GenBank and culture collection numbers of Aspergillus section Nigri used in the phylogenetic analysis. The newly generated sequences are indicated in blue.
TaxaCulture Collection
No.		Gene Bank Accession No.
ITSBenACAMRPB2
A. aculeatinusCBS 121060 TEU159211EU159220EU159241HF559233
A. aculeatusCBS 172.66 TEF661221HE577806EF661148EF661046
A. awamoriITEM 4509 TAM087614AY820001AJ964874HE984360
A. brasiliensisCBS 101740 TFJ629321FJ629272FN594543KY006765
A. brunneoviolaceusCBS 621.78 TAJ280003EF661105EF661147EF661045
A. carbonariusCBS 111.26 TEF661204EF661099EF661167EF661068
A. chiangmaiensisSDBR-CMUI4MW588209MW602898MK457199MW602899
A. costaricaensisCBS 115574 TDQ900602FJ629277FN594545HE984361
A. ellipticusCBS 482.65 TEF661194EF661122EF661170EF661051
A. eucalypticolaCBS 122712 TEU482439EU482435EU482433MN969070
A. flavusCBS 100927 TAF027863EF661485EF661508EF661440
A. flavusNRRL 447 TEF661560EF661483EF661506EF661438
A. fijiensisCBS 313.89 TFJ491680FJ491688FJ491695N/A
A. floridensisNRRL 62478 TN/AHE984412HE984429HE984376
A. foetidusCBS 121 28 TFJ491683FJ491690FJ491694N/A
A. homomorphusCBS 101899 TEF166063AY820015FN594549N/A
A. heteromorphusCBS 11755 TEU821305EF661103EF661169EF661050
A. hydeiKUMCC 18-0196MT152332MT161679MT178247MT384370
A. ibericusITEM 4776 TNR 119514AM419748AJ971805N/A
A. ibericusNRRL 35645 TEF661201EF661101EF661164N/A
A. indologenusCBS 114.80 TAJ280005AY585539AM419750HE984366
A. japonicusCBS 114.51 TAJ279985HE577804FN594551N/A
A. labruscusCCT 7800 TKU708544KT986014KT986008N/A
A. lacticoffeatusCBS 101883 TFJ629336AY819998EU163270HE984367
A. luchuensisCBS 205.80 TJX500081JX500062JX500071LC179910
A. nigerCBS 554 65 TEF661186EF661089EF661154EF661058
A. nigerIHEM 2312MH613218MH614521MH645010OP082127
A. nigerIHEM 5296MH613217MH614519MH645009OP082167
A. nigerMFLUCC 23-0192OR502379OR594234OR502379OR604630
A. nigerMFLUCC 23-0193OR501408OR594235OR501408OR604631
A. nigerMFLUCC 23-0194OR501405OR594237OR501405OR604634
A. nigerMFLUCC 23-0195OR500483OR594236OR500483OR604632
A. nigerMFLUCC 23-0200OR501402OR573928OR501402OR604633
A. neonigerCBS 115656 TFJ491682FJ491691FJ491700KC796429
A. piperisCBS 112811 TEU821316FJ629303EU163267KC796427
A. piperisCMV011A9N/AMK451187MK451493MK450798
A. pseudopiperisSDBR-CMUI7 TMK457204MK457206MK457205MK457208
A. pseudopiperisSDBR-CMUI1 TMW588212MW602913MW602912MW602914
A. pseudotubingensisSDBR CMUO2 TMK457204MK457206MK457205MK457208
A. pseudotubingensisSDBR CMU20 TMW588212MW602913MW602912MW602914
A. sclerotiicarbonariusCBS 121057 TEU159216EU159229EU159235N/A
A. saccharolyticusCBS 127449 THM853552HM853553HM853554HF559235
A. sclerotionigerCBS 115572 TDQ900606AY819996FN594557HE984369
A. trinidadensisNRRL 62479 TN/AHE984420HE984434HE984379
A. tubingensisPW3161AB987902LC000547LC000560LC000573
A. tubingensisNRRL 4875 TEF661193EF661086EF661151EF661055
A. uvarumCBS 121591 TAM745757AM745751AM745755HE984370
A. uvarumITEM 14819N/AHE984421HE984435HE984380
A. vadensisCBS 113365 TAY585549AY585531FN594560HE984371
A. violaceofuscusCBS 102.03 TFJ491677FJ491686FJ491697HF559234
A. welwitschiaeCBS 139.54 TMH857271FJ629291KC480196MN969100
Note: The ex-type cultures are marked as “T”, and “N/A” indicates sequence is unavailable.
Table 5. Fungal identification of 11 isolates from seven herbal tea samples.
Table 5. Fungal identification of 11 isolates from seven herbal tea samples.
No.Isolate No.TaxaHerbal Tea/Market
1MFLUCC 23-0094A. chevalieriJasmine/Doi Mae Salong
2MFLUCC 23-0095A. chevalieriJasmine/Doi Mae Salong
3MFLUCC 23-0096A. chevalieriJasmine/Doi Mae Salong
4MFLUCC 23-0097A. chevalieriRose/Doi Mae Salong
5MFLUCC 23-0184A. chevalieriBael fruit/Doi Mae Salong
6MFLUCC 23-0185A. chevalieriBlack tea/Doi Mae Salong
7MFLUCC 23-0192A. nigerGoji berry/Doi Mae Salong
8MFLUCC 23-0193A. nigerBael fruit/Mae Sai
9MFLUCC 23-0194A. nigerLavender/Mae Sai
10MFLUCC 23-0195A. nigerGreen tea/Fah Thai
11MFLUCC 23-0200A. nigerGreen tea/Fah Thai
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Noorabadi, M.T.; Gomes de Farias, A.R.; Mapook, A.; Hyde, K.D.; Boonmee, S. Occurrence of Aspergillus chevalieri and A. niger on Herbal Tea and Their Potential to Produce Ochratoxin A (OTA). Diversity 2023, 15, 1183. https://doi.org/10.3390/d15121183

AMA Style

Noorabadi MT, Gomes de Farias AR, Mapook A, Hyde KD, Boonmee S. Occurrence of Aspergillus chevalieri and A. niger on Herbal Tea and Their Potential to Produce Ochratoxin A (OTA). Diversity. 2023; 15(12):1183. https://doi.org/10.3390/d15121183

Chicago/Turabian Style

Noorabadi, Maryam T., Antonio Roberto Gomes de Farias, Ausana Mapook, Kevin D. Hyde, and Saranyaphat Boonmee. 2023. "Occurrence of Aspergillus chevalieri and A. niger on Herbal Tea and Their Potential to Produce Ochratoxin A (OTA)" Diversity 15, no. 12: 1183. https://doi.org/10.3390/d15121183

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