Integrated Meta-omics Approaches To Understand the Microbiome of Spontaneous Fermentation of Traditional Chinese Pu-erh Tea

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...

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Main Authors: 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
Format: Article
Language:English
Published: American Society for Microbiology 2019-11-01
Series:mSystems
Subjects:
Online Access:https://doi.org/10.1128/mSystems.00680-19
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spelling doaj-6646b9a4b1bb4c208cfb0dbb2ccad8782020-11-25T01:55:06ZengAmerican Society for MicrobiologymSystems2379-50772019-11-0146e00680-1910.1128/mSystems.00680-19Integrated Meta-omics Approaches To Understand the Microbiome of Spontaneous Fermentation of Traditional Chinese Pu-erh TeaMing 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 MaFermented 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.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.https://doi.org/10.1128/mSystems.00680-19carbohydrate-active enzymesfood fermentationmeta-omicsmicrobiomepu-erh teasystemic view
collection DOAJ
language English
format Article
sources DOAJ
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
spellingShingle 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
mSystems
carbohydrate-active enzymes
food fermentation
meta-omics
microbiome
pu-erh tea
systemic view
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
series mSystems
issn 2379-5077
publishDate 2019-11-01
description 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.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.
topic carbohydrate-active enzymes
food fermentation
meta-omics
microbiome
pu-erh tea
systemic view
url https://doi.org/10.1128/mSystems.00680-19
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