Characterization of the Fungal Community in Fritillariae Cirrhosae Bulbus through DNA Metabarcoding
Abstract
:1. Introduction
2. Materials and Methods
2.1. Sample Collection
2.2. DNA Extraction and PCR Amplification
2.3. Bioinformatic Analysis
3. Results
3.1. Analysis of the Fungal Diversity in FCB Samples
3.2. Analysis of the Fungal Community in the FCB Samples
3.3. Comparison of the Differences in Fungal Community in Five FCB Groups Based on Collection Areas
3.4. Interaction Analysis between Fungal Genera in FCB Samples
4. Discussion
4.1. Fungal Community in the FCB Samples
4.2. Relationship between Fungi and Herb in the Whole Production Chain
4.3. DNA Metabarcoding Provides an Early Warning for Fungal and Mycotoxin Contamination
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Data Availability Statement
Conflicts of Interest
References
- Chinese Pharmacopeia Commission. Pharmacopoeia of People’s Republic of China (Part 1); Press of Chemical Industry: Beijing, China, 2020; p. 38.
- Wang, D.; Wang, S.; Chen, X.; Xu, X.; Zhu, J.; Nie, L.; Long, X. Antitussive, expectorant and anti-inflammatory activities of four alkaloids isolated from Bulbus of Fritillaria wabuensis. J. Ethnopharmacol. 2012, 139, 189–193. [Google Scholar] [CrossRef]
- Chen, T.; Zhong, F.; Yao, C.; Chen, J.; Xiang, Y.; Dong, J.; Yan, Z.; Ma, Y. A Systematic Review on Traditional Uses, Sources, Phytochemistry, Pharmacology, Pharmacokinetics, and Toxicity of Fritillariae Cirrhosae Bulbus. Evid.-Based Complement. Altern. Med. 2020, 2020, 1536534. [Google Scholar] [CrossRef] [PubMed]
- Quan, Y.; Li, L.; Yin, Z.; Chen, S.; Yi, J.; Lang, J.; Zhang, L.; Yue, Q.; Zhao, J. Bulbus Fritillariae Cirrhosae as a Respiratory Medicine: Is There a Potential Drug in the Treatment of COVID-19? Front. Pharmacol. 2022, 12, 784335. [Google Scholar] [CrossRef] [PubMed]
- Zheng, R.; Wang, W.-L.; Tan, J.; Xu, H.; Zhan, R.-T.; Chen, W.-W. An investigation of fungal contamination on the surface of medicinal herbs in China. Chin. Med. 2017, 12, 2. [Google Scholar] [CrossRef] [PubMed]
- Han, Z.; Ren, Y.; Zhu, J.; Cai, Z.; Chen, Y.; Luan, L.; Wu, Y. Multianalysis of 35 Mycotoxins in Traditional Chinese Medicines by Ultra-High-Performance Liquid Chromatography–Tandem Mass Spectrometry Coupled with Accelerated Solvent Extraction. J. Agric. Food Chem. 2012, 60, 8233–8247. [Google Scholar] [CrossRef]
- Yu, J.; Yang, M.; Han, J.; Pang, X. Fungal and mycotoxin occurrence, affecting factors, and prevention in herbal medicines: A review. Toxin Rev. 2021, 41, 1925696. [Google Scholar] [CrossRef]
- Chen, A.J.; Tang, D.; Zhou, Y.Q.; Da Sun, B.; Li, X.J.; Wang, L.Z.; Gao, W.W. Identification of Ochratoxin A Producing Fungi Associated with Fresh and Dry Liquorice. PLoS ONE 2013, 8, e78285. [Google Scholar] [CrossRef]
- Jiao, X.; Lu, X.; Chen, A.J.; Luo, Y.; Hao, J.J.; Gao, W. Effects of Fusarium solani and F. oxysporum Infection on the Metabolism of Ginsenosides in American Ginseng Roots. Molecules 2015, 20, 10535–10552. [Google Scholar] [CrossRef]
- Kong, W.; Wei, R.; Logrieco, A.F.; Wei, J.; Wen, J.; Xiao, X.; Yang, M. Occurrence of toxigenic fungi and determination of mycotoxins by HPLC-FLD in functional foods and spices in China markets. Food Chem. 2014, 146, 320–326. [Google Scholar] [CrossRef]
- Porter, T.M.; Hajibabaei, M. Scaling up: A guide to high-throughput genomic approaches for biodiversity analysis. Mol. Ecol. 2018, 27, 313–338. [Google Scholar] [CrossRef]
- Ritter, C.D.; Forster, D.; Azevedo, J.A.R.; Antonelli, A.; Nilsson, R.H.; Trujillo, M.E.; Dunthorn, M. Assessing Biotic and Abiotic Interactions of Microorganisms in Amazonia through Co-Occurrence Networks and DNA Metabarcoding. Microb. Ecol. 2021, 82, 746–760. [Google Scholar] [CrossRef] [PubMed]
- Nilsson, R.H.; Anslan, S.; Bahram, M.; Wurzbacher, C.; Baldrian, P.; Tedersoo, L. Mycobiome diversity: High-throughput sequencing and identification of fungi. Nat. Rev. Microbiol. 2019, 17, 95–109. [Google Scholar] [CrossRef] [PubMed]
- Fang, Y.; Zhang, J.; Zhu, S.; He, M.; Ma, S.; Jia, Q.; Sun, Q.; Song, L.; Wang, Y.; Duan, L. Berberine ameliorates ovariectomy-induced anxiety-like behaviors by enrichment in equol generating gut microbiota. Pharmacol. Res. 2021, 165, 105439. [Google Scholar] [CrossRef] [PubMed]
- Matsuoka, S.; Sugiyama, Y.; Shimono, Y.; Ushio, M.; Doi, H. Evaluation of seasonal dynamics of fungal DNA assemblages in a flow-regulated stream in a restored forest using eDNA metabarcoding. Environ. Microbiol. 2021, 23, 4797–4806. [Google Scholar] [CrossRef]
- Yu, J.; Guo, M.; Jiang, W.; Yang, M.; Pang, X. Assessment of the Microbiome and Potential Aflatoxin Associated with the Medicinal Herb Platycladus orientalis. Front. Microbiol. 2020, 11, 582679. [Google Scholar] [CrossRef]
- Guo, M.; Jiang, W.; Yang, M.; Dou, X.; Pang, X. Characterizing fungal communities in medicinal and edible Cassiae Semen using high-throughput sequencing. Int. J. Food Microbiol. 2020, 319, 108496. [Google Scholar] [CrossRef]
- Jiang, W.; Guo, M.; Yang, M.; Mantri, N.; Chen, X.; Pang, X. High-throughput analysis of fungal communities in Myristicae Semen. LWT 2020, 128, 109499. [Google Scholar] [CrossRef]
- Yang, F.; Yang, D.; Liu, S.; Xu, S.; Wang, F.; Chen, H.; Liu, Y. Use of High-Throughput Sequencing to Identify Fungal Communities on the Surface of Citri Reticulatae Pericarpium during the 3-Year Aging Process. Curr. Microbiol. 2021, 78, 3142–3151. [Google Scholar] [CrossRef]
- White, T.J.; Bruns, T.; Lee, S.; Taylor, J. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In PCR Protocols: A Guide to Methods and Applications; Academic Press: San Diego, CA, USA, 1990; pp. 315–322. [Google Scholar]
- Silva, J.J.; Puel, O.; Lorber, S.; Ferranti, L.S.; Ortiz, L.F.; Taniwaki, M.H.; Iamanaka, B.T.; Fungaro, M.H.P. Occurrence and diversity of Aspergillus in commercial yerba mate elaborated for the Brazilian beverage ‘chimarrão’. Food Res. Int. 2019, 121, 940–946. [Google Scholar] [CrossRef]
- Zhu, T.; Li, L.; Petridis, A.; Xydis, G.; Ren, M. First Report of Fusarium asiaticum Causing Stem Rot of Ligusticum chuanxiong in China. Plant Dis. 2022, 106, 325. [Google Scholar] [CrossRef]
- Chen, L.; Guo, W.; Zheng, Y.; Zhou, J.; Liu, T.; Chen, W.; Liang, D.; Zhao, M.; Zhu, Y.; Wu, Q.; et al. Occurrence and Characterization of Fungi and Mycotoxins in Contaminated Medicinal Herbs. Toxins 2020, 12, 30. [Google Scholar] [CrossRef] [PubMed]
- Ndagijimana, M.; Chaves-López, C.; Corsetti, A.; Tofalo, R.; Sergi, M.; Paparella, A.; Guerzoni, M.; Suzzi, G. Growth and metabolites production by Penicillium brevicompactum in yoghurt. Int. J. Food Microbiol. 2008, 127, 276–283. [Google Scholar] [CrossRef] [PubMed]
- Overy, D.P.; Frisvad, J.C. Mycotoxin Production and Postharvest Storage Rot of Ginger (Zingiber officinale) by Penicillium brevicompactum. J. Food Prot. 2005, 68, 607–609. [Google Scholar] [CrossRef]
- Huang, Y.; Pan, W.; Cai, W.; Ju, J.; Sun, S. Exposure to citrinin induces DNA damage, autophagy, and mitochondria dysfunction during first cleavage of mouse embryos. Environ. Toxicol. 2021, 36, 2217–2224. [Google Scholar] [CrossRef] [PubMed]
- Balasubramanian, G.; Hanumegowda, U.; Reddy, C.S. Secalonic Acid D Alters the Nature of and Inhibits the Binding of the Transcription Factors to the Phorbol 12-O-Tetradecanoate-13 Acetate-Response Element in the Developing Murine Secondary Palate. Toxicol. Appl. Pharmacol. 2000, 169, 142–150. [Google Scholar] [CrossRef]
- Li, W.; Bi, Y.; Ge, Y.; Li, Y.; Wang, J.; Wang, Y. Effects of postharvest sodium silicate treatment on pink rot disease and oxidative stress-antioxidative system in muskmelon fruit. Eur. Food Res. Technol. 2012, 234, 137–145. [Google Scholar] [CrossRef]
- Oh, S.-Y.; Nam, K.-W.; Yoon, D.-H. Identification of Acremonium acutatum and Trichothecium roseum isolated from Grape with White Stain Symptom in Korea. Mycobiology 2014, 42, 269–273. [Google Scholar] [CrossRef]
- Tang, Y.; Xue, H.; Bi, Y.; Li, Y.; Wang, Y.; Zhao, Y.; Shen, K. A method of analysis for T-2 toxin and neosolaniol by UPLC-MS/MS in apple fruit inoculated with Trichothecium roseum. Food Addit. Contam. Part A 2015, 32, 480–487. [Google Scholar] [CrossRef]
- Li, Y.; Wang, Z.; Beier, R.C.; Shen, J.; De Smet, D.; De Saeger, S.; Zhang, S. T-2 Toxin, a Trichothecene Mycotoxin: Review of Toxicity, Metabolism, and Analytical Methods. J. Agric. Food Chem. 2011, 59, 3441–3453. [Google Scholar] [CrossRef]
- García-Ortega, L.; Lacadena, J.; Mancheño, J.M.; Oñaderra, M.; Kao, R.; Davies, J.; Olmo, N.; Martinez-Del-Pozo, A.; Pozo, D.; Gavilanes, J.G. Involvement of the amino-terminal β-hairpin of the Aspergillus ribotoxins on the interaction with membrances and nonspecific ribonuclease activity. Protein Sci. 2001, 10, 1658–1668. [Google Scholar] [CrossRef]
- Wei, X.; Cao, P.; Wang, G.; Han, J. Microbial inoculant and garbage enzyme reduced cadmium (Cd) uptake in Salvia miltiorrhiza (Bge.) under Cd stress. Ecotoxicol. Environ. Saf. 2020, 192, 110311. [Google Scholar] [CrossRef] [PubMed]
- Engel, R.; Szabó, K.; Abrankó, L.; Rendes, K.; Füzy, A.; Takács, T.M. Effect of Arbuscular Mycorrhizal Fungi on the Growth and Polyphenol Profile of Marjoram, Lemon Balm, and Marigold. J. Agric. Food Chem. 2016, 64, 3733–3742. [Google Scholar] [CrossRef] [PubMed]
- Shao, S.-C.; Wang, Q.-X.; Beng, K.C.; Zhao, D.-K.; Jacquemyn, H. Fungi isolated from host protocorms accelerate symbiotic seed germination in an endangered orchid species (Dendrobium chrysotoxum) from southern China. Mycorrhiza 2020, 30, 529–539. [Google Scholar] [CrossRef] [PubMed]
- Wang, Z.; Okutsu, K.; Futagami, T.; Yoshizaki, Y.; Tamaki, H.; Maruyama, T.; Toume, K.; Komatsu, K.; Hashimoto, F.; Takamine, K. Microbial Community Structure and Chemical Constituents in Shinkiku, a Fermented Crude Drug Used in Kampo Medicine. Front. Nutr. 2020, 7, 115. [Google Scholar] [CrossRef]
- He, L.; Bai, L.; Shan, L.; Yu, P.; Zhang, L.; Dou, X.; Yang, M. Variations in fungal microbiota and aflatoxin contamination during the processing of Yuanzhi, a traditional Chinese medicine. Ind. Crop. Prod. 2020, 152, 112509. [Google Scholar] [CrossRef]
- Ghareeb, H.; Zhao, Y.; Schirawski, J. Sporisorium reilianum possesses a pool of effector proteins that modulate virulence on maize. Mol. Plant Pathol. 2018, 20, 124–136. [Google Scholar] [CrossRef]
- Chen, N.; Xiao, S.; Sun, J.; He, L.; Liu, M.; Gao, W.; Xu, J.; Wang, H.; Huang, S.; Xue, C. Virulence and Molecular Diversity in the Kabatiella zeae Population Causing Maize Eyespot in China. Plant Dis. 2020, 104, 3197–3206. [Google Scholar] [CrossRef]
- Cabañas, C.; Hernández, A.; Martínez, A.; Tejero, P.; Vázquez-Hernández, M.; Martín, A.; Ruiz-Moyano, S. Control of Penicillium glabrum by Indigenous Antagonistic Yeast from Vineyards. Foods 2020, 9, 1864. [Google Scholar] [CrossRef]
- Qin, X.; Xiao, H.; Cheng, X.; Zhou, H.; Si, L. Hanseniaspora uvarum prolongs shelf life of strawberry via volatile production. Food Microbiol. 2017, 63, 205–212. [Google Scholar] [CrossRef]
- Amobonye, A.; Bhagwat, P.; Pandey, A.; Singh, S.; Pillai, S. Biotechnological potential of Beauveria bassiana as a source of novel biocatalysts and metabolites. Crit. Rev. Biotechnol. 2020, 40, 1019–1034. [Google Scholar] [CrossRef]
- Jiang, W.; Chen, X.; Guo, M.; Yu, J.; Yang, M.; Pang, X. Analysis of Fungal Microbiomes in Edible Medicinal Morindae Officinalis Radix and Alpiniae Oxyphyllae Fructus Using DNA Metabarcoding. Foods 2022, 11, 1748. [Google Scholar] [CrossRef] [PubMed]
- Lu, Q.; Guo, M.-Y.; Tian, J.; Luo, J.-Y.; Yang, M.-H. A comprehensive study on multi-mycotoxin screening, changes of mycotoxin residues and fungal community analysis from barley germination to malt. Int. J. Food Microbiol. 2022, 372, 109678. [Google Scholar] [CrossRef] [PubMed]
- Yu, J.; Guo, M.; Jiang, W.; Dao, Y.; Pang, X. Illumina-Based Analysis Yields New Insights into the Fungal Contamination Associated with the Processed Products of Crataegi Fructus. Front. Nutr. 2022, 9, 883698. [Google Scholar] [CrossRef] [PubMed]
- Valencia-Quintana, R.; Milić, M.; Jakšić, D.; Klarić, M.Š.; Tenorio-Arvide, M.; Pérez-Flores, G.; Bonassi, S.; Sánchez-Alarcón, J. Environment Changes, Aflatoxins, and Health Issues, a Review. Int. J. Environ. Res. Public Health 2020, 17, 7850. [Google Scholar] [CrossRef] [PubMed]
- Bullerman, L.B.; Schroeder, L.L.; Park, K.-Y. Formation and Control of Mycotoxins in Food. J. Food Prot. 1984, 47, 637–646. [Google Scholar] [CrossRef]
Sample No. | Sampling Location | Group | Collection Time | Collection Temperature | Genbank Accession No. |
---|---|---|---|---|---|
FCBXZ1 | Tibet, China | FCBXZ | 2021.08 | 23 °C | SAMN24255245 |
FCBXZ2 | Tibet, China | FCBXZ | 2021.08 | 23 °C | SAMN24255246 |
FCBXZ3 | Tibet, China | FCBXZ | 2021.08 | 23 °C | SAMN24255247 |
FCBQH1 | Qinghai, China | FCBQH | 2021.07 | 25 °C | SAMN24255248 |
FCBQH2 | Qinghai, China | FCBQH | 2021.07 | 25 °C | SAMN24255249 |
FCBQH3 | Qinghai, China | FCBQH | 2021.07 | 25 °C | SAMN24255250 |
FCBAH1 | Anhui, China | FCBAH | 2021.08 | 29 °C | SAMN24255251 |
FCBAH2 | Anhui, China | FCBAH | 2021.08 | 29 °C | SAMN24255252 |
FCBAH3 | Anhui, China | FCBAH | 2021.08 | 29 °C | SAMN24255253 |
FCBSC1 | Sichuan, China | FCBSC | 2021.08 | 30 °C | SAMN24255254 |
FCBSC2 | Sichuan, China | FCBSC | 2021.08 | 30 °C | SAMN24255255 |
FCBSC3 | Sichuan, China | FCBSC | 2021.08 | 30 °C | SAMN24255256 |
FCBHB1 | Hebei, China | FCBHB | 2021.08 | 30 °C | SAMN24255257 |
FCBHB2 | Hebei, China | FCBHB | 2021.08 | 30 °C | SAMN24255258 |
FCBHB3 | Hebei, China | FCBHB | 2021.08 | 30 °C | SAMN24255259 |
Samples | Shannon | Chao | Coverage |
---|---|---|---|
FCBSC1 | 3.08 | 159.0 | 0.99998 |
FCBSC2 | 2.60 | 75.0 | 0.99997 |
FCBSC3 | 2.88 | 100.0 | 1.00000 |
FCBQH1 | 3.11 | 70.0 | 0.99996 |
FCBQH2 | 2.78 | 71.0 | 1.00000 |
FCBQH3 | 1.99 | 49.0 | 1.00000 |
FCBXZ1 | 1.79 | 22.0 | 1.00000 |
FCBXZ2 | 2.47 | 63.0 | 0.99998 |
FCBXZ3 | 2.76 | 63.0 | 0.99998 |
FCBHB1 | 3.16 | 186.5 | 0.99953 |
FCBHB2 | 3.25 | 96.0 | 0.99998 |
FCBHB3 | 3.30 | 199.5 | 0.99960 |
FCBAH1 | 3.52 | 109.0 | 0.99993 |
FCBAH2 | 2.21 | 12.0 | 1.00000 |
FCBAH3 | 1.66 | 143.7 | 0.99965 |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Yu, J.; Zhang, W.; Dao, Y.; Yang, M.; Pang, X. Characterization of the Fungal Community in Fritillariae Cirrhosae Bulbus through DNA Metabarcoding. J. Fungi 2022, 8, 876. https://doi.org/10.3390/jof8080876
Yu J, Zhang W, Dao Y, Yang M, Pang X. Characterization of the Fungal Community in Fritillariae Cirrhosae Bulbus through DNA Metabarcoding. Journal of Fungi. 2022; 8(8):876. https://doi.org/10.3390/jof8080876
Chicago/Turabian StyleYu, Jingsheng, Wenjuan Zhang, Yujie Dao, Meihua Yang, and Xiaohui Pang. 2022. "Characterization of the Fungal Community in Fritillariae Cirrhosae Bulbus through DNA Metabarcoding" Journal of Fungi 8, no. 8: 876. https://doi.org/10.3390/jof8080876
APA StyleYu, J., Zhang, W., Dao, Y., Yang, M., & Pang, X. (2022). Characterization of the Fungal Community in Fritillariae Cirrhosae Bulbus through DNA Metabarcoding. Journal of Fungi, 8(8), 876. https://doi.org/10.3390/jof8080876