Integrated Meta-omics Approaches To Understand the Microbiome of Spontaneous Fermentation of Traditional Chinese Pu-erh Tea
ABSTRACT The microbiome in fermentation has direct impacts on the quality of fermented foods and is of great scientific and commercial interest. Despite considerable effort to explain the microbial metabolism associated with food fermentation, the role of the microbiome in pu-erh tea fermentation re...
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American Society for Microbiology
2019
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oai:doaj.org-article:87bd945e41a747cfa685b388b07dc4932021-12-02T19:47:35ZIntegrated Meta-omics Approaches To Understand the Microbiome of Spontaneous Fermentation of Traditional Chinese Pu-erh Tea10.1128/mSystems.00680-192379-5077https://doaj.org/article/87bd945e41a747cfa685b388b07dc4932019-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00680-19https://doaj.org/toc/2379-5077ABSTRACT The microbiome in fermentation has direct impacts on the quality of fermented foods and is of great scientific and commercial interest. Despite considerable effort to explain the microbial metabolism associated with food fermentation, the role of the microbiome in pu-erh tea fermentation remains unknown. Here, we applied integrated meta-omics approaches to characterize the microbiome in two repeated fermentations of pu-erh tea. Metabarcoding analysis of bacterial 16S rRNA genes showed a decrease in the proportion of Proteobacteria and an increase in the abundance of Firmicutes during fermentation. Metabarcoding analysis of fungal internal transcribed spacer (ITS) sequence demonstrated that Rasamsonia, Thermomyces, and Aspergillus were dominant at the intermediate stage, whereas Aspergillus was dominant at other stages in fermentation. Metaproteomics analysis assigned primary microbial metabolic activity to metabolism and identified microbial carbohydrate-active enzymes involved in the degradation of polysaccharides including cellulose, xylan, xyloglucan, pectin, starch, lignin, galactomannan, and chitin. Metabolomics and high-performance liquid chromatography analysis revealed that levels of phenolic compounds, including gallates, decreased whereas contents of gallic acid and ellagic acid significantly increased after fermentation (P < 0.05). The changes in levels of gallates and gallic acid were associated with the hydrolysis of tannase. Glycoside hydrolases, phenol 2-monooxygenase, salicylaldehyde dehydrogenase, salicylate 1-monooxygenase, catechol O-methyltransferase, catechol dioxygenase, and quercetin 2,3-dioxygenases were hypothesized to be related to oxidation, conversion, or degradation of phenolic compounds. We demonstrated microbiota in fermentation and their function in the production of enzymes related to the degradation of polysaccharides, and metabolism of phenolic compounds, resulting in changes in metabolite contents and the quality of pu-erh tea. IMPORTANCE Fermented foods play important roles in diets worldwide and account for approximately one-third of all foods and beverages consumed. To date, traditional fermentation has used spontaneous fermentation. The microbiome in fermentation has direct impacts on the quality and safety of fermented foods and contributes to the preservation of traditional methods. Here, we used an integrated meta-omics approach to study the microbiome in the fermentation of pu-erh tea, which is a well-known Chinese fermented food with a special flavor and healthful benefits. This study advanced the knowledge of microbiota, metabolites, and enzymes in the fermentation of pu-erh tea. These novel insights shed light onto the complex microbiome in pu-erh fermentation and highlight the power of integrated meta-omics approaches in understanding the microbiome in food fermentation ecosystems.Ming ZhaoXiao Q. SuBo NianLi J. ChenDong L. ZhangShuang M. DuanLi Y. WangXing Y. ShiBin JiangWei W. JiangCai Y. LvDao P. WangYang ShiYing XiaoJian-Lin WuYing H. PanYan MaAmerican Society for Microbiologyarticlecarbohydrate-active enzymesfood fermentationmeta-omicsmicrobiomepu-erh teasystemic viewMicrobiologyQR1-502ENmSystems, Vol 4, Iss 6 (2019) |
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DOAJ |
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DOAJ |
| language |
EN |
| topic |
carbohydrate-active enzymes food fermentation meta-omics microbiome pu-erh tea systemic view Microbiology QR1-502 |
| spellingShingle |
carbohydrate-active enzymes food fermentation meta-omics microbiome pu-erh tea systemic view Microbiology QR1-502 Ming Zhao Xiao Q. Su Bo Nian Li J. Chen Dong L. Zhang Shuang M. Duan Li Y. Wang Xing Y. Shi Bin Jiang Wei W. Jiang Cai Y. Lv Dao P. Wang Yang Shi Ying Xiao Jian-Lin Wu Ying H. Pan Yan Ma Integrated Meta-omics Approaches To Understand the Microbiome of Spontaneous Fermentation of Traditional Chinese Pu-erh Tea |
| description |
ABSTRACT The microbiome in fermentation has direct impacts on the quality of fermented foods and is of great scientific and commercial interest. Despite considerable effort to explain the microbial metabolism associated with food fermentation, the role of the microbiome in pu-erh tea fermentation remains unknown. Here, we applied integrated meta-omics approaches to characterize the microbiome in two repeated fermentations of pu-erh tea. Metabarcoding analysis of bacterial 16S rRNA genes showed a decrease in the proportion of Proteobacteria and an increase in the abundance of Firmicutes during fermentation. Metabarcoding analysis of fungal internal transcribed spacer (ITS) sequence demonstrated that Rasamsonia, Thermomyces, and Aspergillus were dominant at the intermediate stage, whereas Aspergillus was dominant at other stages in fermentation. Metaproteomics analysis assigned primary microbial metabolic activity to metabolism and identified microbial carbohydrate-active enzymes involved in the degradation of polysaccharides including cellulose, xylan, xyloglucan, pectin, starch, lignin, galactomannan, and chitin. Metabolomics and high-performance liquid chromatography analysis revealed that levels of phenolic compounds, including gallates, decreased whereas contents of gallic acid and ellagic acid significantly increased after fermentation (P < 0.05). The changes in levels of gallates and gallic acid were associated with the hydrolysis of tannase. Glycoside hydrolases, phenol 2-monooxygenase, salicylaldehyde dehydrogenase, salicylate 1-monooxygenase, catechol O-methyltransferase, catechol dioxygenase, and quercetin 2,3-dioxygenases were hypothesized to be related to oxidation, conversion, or degradation of phenolic compounds. We demonstrated microbiota in fermentation and their function in the production of enzymes related to the degradation of polysaccharides, and metabolism of phenolic compounds, resulting in changes in metabolite contents and the quality of pu-erh tea. IMPORTANCE Fermented foods play important roles in diets worldwide and account for approximately one-third of all foods and beverages consumed. To date, traditional fermentation has used spontaneous fermentation. The microbiome in fermentation has direct impacts on the quality and safety of fermented foods and contributes to the preservation of traditional methods. Here, we used an integrated meta-omics approach to study the microbiome in the fermentation of pu-erh tea, which is a well-known Chinese fermented food with a special flavor and healthful benefits. This study advanced the knowledge of microbiota, metabolites, and enzymes in the fermentation of pu-erh tea. These novel insights shed light onto the complex microbiome in pu-erh fermentation and highlight the power of integrated meta-omics approaches in understanding the microbiome in food fermentation ecosystems. |
| format |
article |
| author |
Ming Zhao Xiao Q. Su Bo Nian Li J. Chen Dong L. Zhang Shuang M. Duan Li Y. Wang Xing Y. Shi Bin Jiang Wei W. Jiang Cai Y. Lv Dao P. Wang Yang Shi Ying Xiao Jian-Lin Wu Ying H. Pan Yan Ma |
| author_facet |
Ming Zhao Xiao Q. Su Bo Nian Li J. Chen Dong L. Zhang Shuang M. Duan Li Y. Wang Xing Y. Shi Bin Jiang Wei W. Jiang Cai Y. Lv Dao P. Wang Yang Shi Ying Xiao Jian-Lin Wu Ying H. Pan Yan Ma |
| author_sort |
Ming Zhao |
| title |
Integrated Meta-omics Approaches To Understand the Microbiome of Spontaneous Fermentation of Traditional Chinese Pu-erh Tea |
| title_short |
Integrated Meta-omics Approaches To Understand the Microbiome of Spontaneous Fermentation of Traditional Chinese Pu-erh Tea |
| title_full |
Integrated Meta-omics Approaches To Understand the Microbiome of Spontaneous Fermentation of Traditional Chinese Pu-erh Tea |
| title_fullStr |
Integrated Meta-omics Approaches To Understand the Microbiome of Spontaneous Fermentation of Traditional Chinese Pu-erh Tea |
| title_full_unstemmed |
Integrated Meta-omics Approaches To Understand the Microbiome of Spontaneous Fermentation of Traditional Chinese Pu-erh Tea |
| title_sort |
integrated meta-omics approaches to understand the microbiome of spontaneous fermentation of traditional chinese pu-erh tea |
| publisher |
American Society for Microbiology |
| publishDate |
2019 |
| url |
https://doaj.org/article/87bd945e41a747cfa685b388b07dc493 |
| work_keys_str_mv |
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| _version_ |
1718375972846174208 |