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29 November 2023

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

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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.
Diversity2023, 15(12), 1183;https://doi.org/10.3390/d15121183
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.
Table 1. Tea and herbal teas used in this study obtained from local markets in northern Thailand.

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.
Table 2. PCR amplification conditions used in the thermal cycler of each gene.
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).
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 4. GenBank and culture collection numbers of Aspergillus section Nigri used in the phylogenetic analysis. The newly generated sequences are indicated in blue.

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).
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.
Table 5. Fungal identification of 11 isolates from seven herbal tea samples.
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).
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.

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.

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.
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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.

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).
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.

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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