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Microbiomics and metabolomics insights into the microbial regulation on the formation of flavor components in the traditional fermentation process of Chinese Hongqu aged vinegar

Shangong Tonga,b,1, Wenlong Lia,b,1, Yuandong Raoa, Yanqin Xiaoa, Yingyin Yana,b, Weiling Guoc, Xucong Lüa,b (), Jinyuan Sund, Lianzhong Aie, Li Nia,b()
Institute of Food Science and Technology, College of Biological Science and Engineering, Fuzhou University, Fuzhou 350108, China
Food Nutrition and Health Research Center, School of Advanced Manufacturing, Fuzhou University, Jinjiang 362200, China
School of Food Science and Technology, Jiangnan University, Wuxi 214122, China
Beijing Laboratory for Food Quality and Safety, Beijing Technology and Business University, Beijing 100048, China
School of Health Science and Engineering, University of Shanghai for Science and Technology, Shanghai 200093, China

1 Co-first authors: Shangong Tong and Wenlong Li contributed equally to this study.

Peer review under responsibility of Tsinghua University Press.

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Highlights

• Microbial community in Hongqu aged vinegar was investigated by high-throughput sequencing.

• Flavor components in Hongqu aged vinegar were revealed by GC-MS and LC-QTOF-MS.

• Amino acids and dipeptides were identified throughout the brewing of Hongqu aged vinegar.

• The potential relationships between the key microbes and flavor components were revealed.

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Abstract

This study aimed to investigate microbial succession and metabolic dynamics during the traditional fermentation of Hongqu aged vinegar, and explore the core functional microbes closely related to the formation of flavor components. Microbiome analysis demonstrated that Lactobacillus, Acetobacter, Bacillus, Enterobacter, Lactococcus, Leuconostoc and Weissella were the predominant bacterial genera, while Aspergillus piperis, Aspergillus oryzae, Monascus purpureus, Candida athensensis, C. xylopsoci, Penicillium ochrosalmoneum and Simplicillium aogashimaense were the predominant fungal species. Correlation analysis revealed that Acetobacter was positively correlated with the production of tetramethylpyrazine, acetoin and acetic acid, Lactococcus showed positive correlation with the production of 2-nonanone, 2-heptanone, ethyl caprylate, ethyl caprate, 1-hexanol, 1-octanol and 1-octen-3-ol, C. xylopsoci and C. rugosa were positively associated with the production of diethyl malonate, 2,3-butanediyl diacetate, acetoin, benzaldehyde and tetramethylpyrazine. Correspondingly, non-volatile metabolites were also detected through ultra-performance liquid chromatography-quadrupole time-of-flight mass spectrometry. A variety of amino acids and functional dipeptides were identified during the traditional brewing of Hongqu aged vinegar. Correlation analysis revealed that Lactobacillus was significantly associated with DL-lactate, indolelactic acid, D-(+)-3-phenyllactic acid, pimelic acid, pregabalin and 3-aminobutanoic acid. This study is useful for understanding flavor formation mechanism and developing effective strategies for the suitable strains selection to improve the flavor quality of Hongqu aged vinegar.

Keywords

Hongqu aged vinegarTraditional fermentationMicrobial dynamicsFlavor componentsBidirectional orthogonal partial least squares

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References

[1]

D. Liu, Y. Zhu, R. Beeftink, et al., Chinese vinegar and its solid-state fermentation process, Food Rev. Int. 20 (2004) 407-424. https://doi.org/10.1081/fri-200033460.

Crossref Google Scholar
[2]

J. Song, J. Zhang, Y. Su, et al., Monascus vinegar-mediated alternation of gut microbiota and its correlation with lipid metabolism and inflammation in hyperlipidemic rats, J. Funct. Foods 74 (2020) 104152. https://doi.org/https://doi.org/10.1016/j.jff.2020.104152.

Crossref Google Scholar
[3]

Z.M. Lu, Z.M. Wang, X.J. Zhang, et al., Microbial ecology of cereal vinegar fermentation: insights for driving the ecosystem function, Curr. Opin. Biotechnol. 49 (2018) 88-93. https://doi.org/10.1016/j.copbio.2017.07.006.

Crossref Google Scholar
[4]

Y. Jiang, X. Lü, C. Zhang, et al., Microbial dynamics and flavor formation during the traditional brewing of Monascus vinegar, Food Res. Int. 125 (2019) 108531. https://doi.org/10.1016/j.foodres.2019.108531.

Crossref Google Scholar
[5]

L. Cocolin, S. Campolongo, V. Alessandria, et al., Culture independent analyses and wine fermentation: an overview of achievements 10 years after first application, Ann. Microbiol. 61 (2011) 17-23. https://doi.org/10.1007/s13213-010-0076-6.

Crossref Google Scholar
[6]

M.d.C. Portillo, A. Mas, Analysis of microbial diversity and dynamics during wine fermentation of Grenache grape variety by high-throughput barcoding sequencing, LWT-Food Sci. Technol. 72 (2016) 317-321. https://doi.org/10.1016/j.lwt.2016.05.009.

Crossref Google Scholar
[7]

A. Dalmasso, M.d.l.D. Soto del Rio, T. Civera, et al., Characterization of microbiota in Plaisentif cheese by high-throughput sequencing, LWT-Food Sci. Technol. 69 (2016) 490-496. https://doi.org/10.1016/j.lwt.2016.02.004.

Crossref Google Scholar
[8]

B. Mayo, C.T. Rachid, A. Alegría, et al., Impact of next generation sequencing techniques in food microbiology, Curr. Genomics 15 (2014) 293-309. https://doi.org/10.2174/1389202915666140616233211.

Crossref Google Scholar
[9]

Q. Peng, Y. Yang, Y. Guo, et al., Analysis of bacterial diversity during acetic acid fermentation of Tianjin duliu aged vinegar by 454 pyrosequencing, Curr. Microbiol. 71 (2015) 195-203. https://doi.org/10.1007/s00284-015-0823-9.

Crossref Google Scholar
[10]

Z. Nie, Y. Zheng, H. Du, et al., Dynamics and diversity of microbial community succession in traditional fermentation of Shanxi aged vinegar, Food Microbiol. 47 (2015) 62-68. https://doi.org/10.1016/j.fm.2014.11.006.

Crossref Google Scholar
[11]

Z.M. Wang, Z.M. Lu, Y.J. Yu, et al., Batch-to-batch uniformity of bacterial community succession and flavor formation in the fermentation of Zhenjiang aromatic vinegar, Food Microbiol. 50 (2015) 64-69. https://doi.org/10.1016/j.fm.2015.03.012.

Crossref Google Scholar
[12]

X. Li, Y. Wang, J. Sun, et al., Chemotaxonomic studies of 12 Dioscorea species from China by UHPLC-QTOF-MS/MS analysis, Phytochem. Anal. 31 (2020) 164-182. https://doi.org/10.1002/pca.2876.

Crossref Google Scholar
[13]

Z. Liu, Z. Wang, X. Lv, et al., Comparison study of the volatile profiles and microbial communities of Wuyi Qu and Gutian Qu, two major types of traditional fermentation starters of Hong Qu glutinous rice wine, Food Microbiol. 69 (2018) 105-115. https://doi.org/10.1016/j.fm.2017.07.019.

Crossref Google Scholar
[14]

W.L. Li, S.G. Tong, Z.Y. Yang, et al., The dynamics of microbial community and flavor metabolites during the acetic acid fermentation of Hongqu aromatic vinegar, Curr. Res. Food Sci. 5 (2022) 1720-1731. https://doi.org/10.1016/j.crfs.2022.10.002.

Crossref Google Scholar
[15]

T. Luo, W. Fan, Y. Xu, Characterization of volatile and semi-volatile compounds in Chinese rice wines by headspace solid phase microextraction followed by gas chromatography-mass spectrometry, J. Inst. Brew. 114 (2008) 172-179. https://doi.org/10.1002/j.2050-0416.2008.tb00323.x.

Crossref Google Scholar
[16]

G.M. Chen, W.L. Li, S.G. Tong, et al., Effects of the microbial community on the formation of volatile compounds and biogenic amines during the traditional brewing of Hongqu rice wine, Curr. Res. Food Sci. 5 (2022) 1433-1444. https://doi.org/10.1016/j.crfs.2022.08.020.

Crossref Google Scholar
[17]

H.Vandendool, P.D. Kratz, A generalization of the retention index system including linear temperature programmed gas-liquid partition chromatography. J. Chromatogr. A 11(1963) 463-471. https://doi.org/https://doi.org/10.1016/S0021-9673(01)80947-X.

Crossref Google Scholar
[18]

Y. Wu, M. Xia, N. Zhao, et al., Metabolic profile of main organic acids and its regulatory mechanism in solid-state fermentation of Chinese cereal vinegar, Food Res. Int. 145 (2021) 110400. https://doi.org/https://doi.org/10.1016/j.foodres.2021.110400.

Crossref Google Scholar
[19]

G.Y. Fang, L.J. Chai, X.Z. Zhong, et al., Deciphering the succession patterns of bacterial community and their correlations with environmental factors and flavor compounds during the fermentation of Zhejiang rosy vinegar, Int. J. Food Microbiol. 341 (2021) 109070. https://doi.org/10.1016/j.ijfoodmicro.2021.109070.

Crossref Google Scholar
[20]

C. García, M. Rendueles, M. Díaz, Liquid-phase food fermentations with microbial consortia involving lactic acid bacteria: a review, Food Res. Int. 119 (2019) 207-220. https://doi.org/https://doi.org/10.1016/j.foodres.2019.01.043.

Crossref Google Scholar
[21]

M. Matsutani, M. Nishikura, N. Saichana, et al., Adaptive mutation of Acetobacter pasteurianus SKU1108 enhances acetic acid fermentation ability at high temperature, J. Biotechnol. 165 (2013) 109-119. https://doi.org/10.1016/j.jbiotec.2013.03.006.

Crossref Google Scholar
[22]

J. Trcek, N.P. Mira, L.R. Jarboe, Adaptation and tolerance of bacteria against acetic acid, Appl. Microbiol. Biotechnol. 99 (2015) 6215-6229. https://doi.org/10.1007/s00253-015-6762-3.

Crossref Google Scholar
[23]

L.J. Chai, T. Qiu, Z.M. Lu, et al., Modulating microbiota metabolism via bioaugmentation with Lactobacillus casei and Acetobacter pasteurianus to enhance acetoin accumulation during cereal vinegar fermentation, Food Res. Int. 138 (2020) 109737. https://doi.org/10.1016/j.foodres.2020.109737.

Crossref Google Scholar
[24]

Y. Zhu, F. Zhang, C. Zhang, et al., Dynamic microbial succession of Shanxi aged vinegar and its correlation with flavor metabolites during different stages of acetic acid fermentation, Sci. Rep. 8 (2018) 8612. https://doi.org/10.1038/s41598-018-26787-6.

Crossref Google Scholar
[25]

S. Lee, J. Lee, Y.I. Jin, et al., Probiotic characteristics of Bacillus strains isolated from Korean traditional soy sauce, LWT-Food Sci. Technol. 79 (2017) 518-524. https://doi.org/10.1016/j.lwt.2016.08.040.

Crossref Google Scholar
[26]

C.L. Wang, D.J. Shi, G.L. Gong, Microorganisms in Daqu: a starter culture of Chinese Maotai-flavor liquor, World J. Microbiol. Biotechnol. 24 (2008) 2183-2190. https://doi.org/10.1007/s11274-008-9728-0.

Crossref Google Scholar
[27]

S.H. Song, C. Lee, S. Lee, et al., Analysis of microflora profile in Korean traditional nuruk, J. Microbiol. Biotechnol. 23 (2013) 40-46. https://doi.org/10.4014/jmb.1210.10001.

Crossref Google Scholar
[28]

C. Zhao, X. Zhao, J. Zhang, et al., Screening of Bacillus strains from sun vinegar for efficient production of flavonoid and phenol, Indian J. Microbiol. 56 (2016) 498-503. https://doi.org/10.1007/s12088-016-0602-8.

Crossref Google Scholar
[29]

C. Zhao, X. Yan, S. Yang, et al., Screening of Bacillus strains from Luzhou-flavor liquor making for high-yield ethyl hexanoate and low-yield propanol, LWT-Food Sci. Technol. 77 (2017) 60-66. https://doi.org/10.1016/j.lwt.2016.11.035.

Crossref Google Scholar
[30]

J. Liu, J. Chen, Y. Fan, et al., Biochemical characterisation and dominance of different hydrolases in different types of Daqu-a Chinese industrial fermentation starter, J. Sci. Food Agric. 98 (2017) 113-121. https://doi.org/10.1002/jsfa.8445.

Crossref Google Scholar
[31]

J. Thongekkaew, T. Fujii, K. Masaki, et al., Evaluation of Candida easanensis JK8 β-glucosidase with potentially hydrolyse non-volatile glycosides of wine aroma precursors, Nat. Prod. Res. 33 (2019) 3563-3567. https://doi.org/10.1080/14786419.2018.1481845.

Crossref Google Scholar
[32]

W.L. Li, J.L. Hong, J.Q. Lu, et al., Comparative transcriptomic and metabolomic analyses reveal the regulatory effect and mechanism of tea extracts on the biosynthesis of monascus pigments, Foods 11 (2022) 3159. https://doi.org/10.3390/foods11203159.

Crossref Google Scholar
[33]

F. Karim, X. Liang, S.H. Qi, Bioassay-guided isolation of antifungal cyclopeptides from the deep-sea-derived fungus Simplicillium obclavatum EIODSF 020, Phytochem. Lett. 48 (2022) 68-71. https://doi.org/10.1016/j.phytol.2022.01.017.

Crossref Google Scholar
[34]

G.D. Dumitriu, N.L. Lerma, C.I. Zamfir, et al., Volatile and phenolic composition of red wines subjected to aging in oak cask of different toast degree during two periods of time, LWT-Food Sci. Technol. 86 (2017) 643-651. https://doi.org/10.1016/j.lwt.2017.08.057.

Crossref Google Scholar
[35]

Y. Feng, A. Zhang, A Floral Fragrance, Methyl benzoate, is an efficient green pesticide, Sci. Rep. 7 (2017) 42168. https://doi.org/10.1038/srep42168.

Crossref Google Scholar
[36]

W.R. Morrison, N.L. Larson, D. Brabec, et al., Methyl benzoate as a putative alternative, environmentally friendly fumigant for the control of stored product insects, J. Econ. Entomol. 112 (2019) 2458-2468. https://doi.org/10.1093/jee/toz179.

Crossref Google Scholar
[37]

B.T. Carvalho, S. Holt, B. Souffriau, et al., Identification of novel alleles conferring superior production of rose flavor phenylethyl acetate using polygenic analysis in yeast, mBio 8 (2017). https://doi.org/10.1128/mBio.01173-17.

Crossref Google Scholar
[38]

E.D. Guerrero, F. Chinnici, N. Natali, et al., Solid-phase extraction method for determination of volatile compounds in traditional balsamic vinegar, J. Sep. Sci. 31 (2008) 3030-3036. https://doi.org/10.1002/jssc.200800307.

Crossref Google Scholar
[39]

G. Zhao, G. Kuang, J. Li, et al., Characterization of aldehydes and hydroxy acids as the main contribution to the traditional Chinese rose vinegar by flavor and taste analyses, Food Res. Int. 129 (2020) 108879. https://doi.org/10.1016/j.foodres.2019.108879.

Crossref Google Scholar
[40]

Z. Xiao, J.R. Lu, Strategies for enhancing fermentative production of acetoin: a review, Biotechnol. Adv. 32 (2014) 492-503. https://doi.org/10.1016/j.biotechadv.2014.01.002.

Crossref Google Scholar
[41]

S. Al-Dalali, F. Zheng, B.G. Sun, et al., Effects of different brewing processes on the volatile flavor profiles of Chinese vinegar determined by HS-SPME-AEDA with GC-MS and GC-O, LWT-Food Sci. Technol. 133 (2020) 109969. https://doi.org/10.1016/j.lwt.2020.109969.

Crossref Google Scholar
[42]

Y. Zhang, Z.H. Zhang, R. He, et al., Improving soy sauce aroma using high hydrostatic pressure and the preliminary mechanism, Foods 11 (2022) 2190. https://doi.org/10.3390/foods11152190.

Crossref Google Scholar
[43]

X. Qian, X.Q. Xu, K.J. Yu, et al., Varietal dependence of GLVs accumulation and LOX-HPL pathway gene expression in four Vitis vinifera wine grapes, Int. J. Mol. Sci. 17 (2016) 1924. https://doi.org/10.3390/ijms17111924.

Crossref Google Scholar
[44]

A. Hikida, K. Ito, T. Motoyama, et al., Systematic analysis of a dipeptide library for inhibitor development using human dipeptidyl peptidase Ⅳ produced by a Saccharomyces cerevisiae expression system, Biochem. Biophys. Res. Commun. 430 (2013) 1217-1222. https://doi.org/10.1016/j.bbrc.2012.12.073.

Crossref Google Scholar
[45]

N. Ishibashi, K. Kouge, I. Shinoda, et al., A mechanism for bitter taste sensibility in peptides, Agric. Biol. Chem. 52 (1988) 819-827. https://doi.org/10.1080/00021369.1988.10868743.

Crossref Google Scholar
[46]

V.T. Lan, K. Ito, M. Ohno, et al., Analyzing a dipeptide library to identify human dipeptidyl peptidase Ⅳ inhibitor, Food Chem. 175 (2015) 66-73. https://doi.org/10.1016/j.foodchem.2014.11.131.

Crossref Google Scholar
[47]

S. Dhanda, J. Singh, H. Singh, Hydrolysis of various bioactive peptides by goat brain dipeptidylpeptidase-Ⅲ homologue, Cell Biochem. Funct. 26 (2008) 339-345. https://doi.org/10.1002/cbf.1448.

Crossref Google Scholar
[48]

T. Hatanaka, Y. Inoue, J. Arima, et al., Production of dipeptidyl peptidase Ⅳ inhibitory peptides from defatted rice bran, Food Chem. 134 (2012) 797-802. https://doi.org/10.1016/j.foodchem.2012.02.183.

Crossref Google Scholar
[49]

C.J. Platerink, H.G. Janssen, J. Haverkamp, Application of at-line two-dimensional liquid chromatography-mass spectrometry for identification of small hydrophilic angiotensin I-inhibiting peptides in milk hydrolysates, Anal. Bioanal. Chem. 391 (2008) 299-307. https://doi.org/10.1007/s00216-008-1990-3.

Crossref Google Scholar
[50]

N.R.M. Sahab, E. Subroto, R.L. Balia, et al., γ-Aminobutyric acid found in fermented foods and beverages: current trends, Heliyon 6 (2020) e05526. https://doi.org/10.1016/j.heliyon.2020.e05526.

Crossref Google Scholar
[51]

Z.Y. Wang, Y.Y. Liu, G.H. Liu, et al., L-carnitine and heart disease, Life Sci. 194 (2018) 88-97. https://doi.org/10.1016/j.lfs.2017.12.015.

Crossref Google Scholar
[52]

Y. Liang, X. Dai, Y. Cao, et al., The neuroprotective and antidiabetic effects of trigonelline: a review of signaling pathways and molecular mechanisms, Biochimie 206 (2022) 93-104. https://doi.org/10.1016/j.biochi.2022.10.009.

Crossref Google Scholar
[53]

Y.J. Zhang, Y. Zhang, Y. Zhou, et al., A review of pretreatment and analytical methods of biogenic amines in food and biological samples since 2010, J. Chromatogr. A 1605 (2019) 360361. https://doi.org/10.1016/j.chroma.2019.07.015.

Crossref Google Scholar
[54]

X.L. Gao, C. Li, R. He, et al., Research advances on biogenic amines in traditional fermented foods: emphasis on formation mechanism, detection and control methods, Food Chem. 405 (2023) 134911. https://doi.org/10.1016/j.foodchem.2022.134911.

Crossref Google Scholar
[55]

Q. Luo, R. Shi, P. Gong, et al., Biogenic amines in Huangjiu (Chinese rice wine): formation, hazard, detection, and reduction, LWT-Food Sci. Technol. 168 (2022) 113952. https://doi.org/10.1016/j.lwt.2022.113952.

Crossref Google Scholar
[56]

D. Wang, M. Wang, L. Cao, et al., Changes and correlation of microorganism and flavor substances during persimmon vinegar fermentation, Food Biosci. 46 (2022) 101565. https://doi.org/10.1016/j.fbio.2022.101565.

Crossref Google Scholar
[57]

T. Huang, Z.M. Lu, M.Y. Peng, et al., Combined effects of fermentation starters and environmental factors on the microbial community assembly and flavor formation of Zhenjiang aromatic vinegar, Food Res. Int. 152 (2022) 110900. https://doi.org/10.1016/j.foodres.2021.110900.

Crossref Google Scholar
[58]

R. Kou, M. Li, J. Xing, et al., Exploring of seasonal dynamics of microbial community in multispecies fermentation of Shanxi mature vinegar, J. Biosci. Bioeng. 133 (2022) 375-381. https://doi.org/10.1016/j.jbiosc.2022.01.003.

Crossref Google Scholar
[59]

H. Shi, X. Zhou, Y. Yao, et al., Insights into the microbiota and driving forces to control the quality of vinegar, LWT-Food Sci. Technol. 157 (2022) 113085. https://doi.org/10.1016/j.lwt.2022.113085.

Crossref Google Scholar
[60]

E. Debonne, A. Vermeulen, N. Bouboutiefski, et al., Modelling and validation of the antifungal activity of DL-3-phenyllactic acid and acetic acid on bread spoilage moulds, Food Microbiol. 88 (2020) 103407. https://doi.org/10.1016/j.fm.2019.103407.

Crossref Google Scholar
[61]

P. Lavermicocca, F. Valerio, A. Evidente, et al., Purification and characterization of novel antifungal compounds from the sourdough Lactobacillus plantarum strain 21B, Appl. Environ. Microbiol. 66 (2000) 4084-4090. https://doi.org/10.1128/aem.66.9.4084-4090.2000.

Crossref Google Scholar
[62]

Z.M. Wang, Z.M. Lu, J.S. Shi, et al., Exploring flavour-producing core microbiota in multispecies solid-state fermentation of traditional Chinese vinegar, Sci. Rep. 6 (2016) 26818. https://doi.org/10.1038/srep26818.

Crossref Google Scholar
Food Science and Human Wellness
Volume 13 Issue 5,
September 2024
Pages 2765-2778
DOI: 10.26599/FSHW.2022.9250224
Cite this article:
Tong S, Li W, Rao Y, et al. Microbiomics and metabolomics insights into the microbial regulation on the formation of flavor components in the traditional fermentation process of Chinese Hongqu aged vinegar. Food Science and Human Wellness, 2024, 13(5): 2765-2778. https://doi.org/10.26599/FSHW.2022.9250224
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