Journal Home > Volume 11 , Issue 4

The entire fermentation process of traditional Chinese broad bean paste with chili comprises three individual stages: Tianbanzi, chili pei, and paste fermentation (Tianbanzi-chili pei mixture). Three stages share average 77.53% of all bacteria (89 genera), indicating that the similar environment leads to the similar bacterial communities. One, one, and three genera are exclusive to Tianbanzi, chili pei, and paste stages, respectively, due to the special physical and chemical properties for each stage. Total acidity, pH, and NaCl are important endogenous factors that promote the succession of bacterial communities. According to the dynamics of organic acids, reducing sugars, amino acids, and volatile compounds, 60-, 210-, and 180-day are considered the best fermentation periods for Tianbanzi, chili pei, and paste, respectively, to balance time cost and product quality. Three (Tetragenococcus, Lactobacillus, and Pseudomonas), four (Tetragenococcus, Lactobacillus, Bacillus, and Pseudomonas), and five (Tetragenococcus, Lactobacillus, Bacillus, Pseudomonas, and Pediococcus) genera are considered the core functional bacteria of Tianbanzi, chili pei, and paste fermentation, respectively.


menu
Abstract
Full text
Outline
About this article

Unraveling the core functional bacteria and their succession throughout three fermentation stages of broad bean paste with chili

Show Author's information Songfeng Yua,b,1Jia Songa,1Tao HuaJun WangaXiaojing LiuaYu Zhenga,c ( )Lei ShicShoupeng WancMin Wanga( )
State Key Laboratory of Food Nutrition and Safety, Key Laboratory of Industrial Fermentation Microbiology, Ministry of Education, College of Biotechnology, Tianjin University of Science and Technology, Tianjin 300457, China
College of Biosystems Engineering and Food Science, Zhejiang University, Hangzhou 310058, China
Tianjin Limin Condiment Limited Company, Tianjin 300308, China

1 Authors contributed equally to this work.Peer review under responsibility of KeAi Communications Co., Ltd.]]>

Abstract

The entire fermentation process of traditional Chinese broad bean paste with chili comprises three individual stages: Tianbanzi, chili pei, and paste fermentation (Tianbanzi-chili pei mixture). Three stages share average 77.53% of all bacteria (89 genera), indicating that the similar environment leads to the similar bacterial communities. One, one, and three genera are exclusive to Tianbanzi, chili pei, and paste stages, respectively, due to the special physical and chemical properties for each stage. Total acidity, pH, and NaCl are important endogenous factors that promote the succession of bacterial communities. According to the dynamics of organic acids, reducing sugars, amino acids, and volatile compounds, 60-, 210-, and 180-day are considered the best fermentation periods for Tianbanzi, chili pei, and paste, respectively, to balance time cost and product quality. Three (Tetragenococcus, Lactobacillus, and Pseudomonas), four (Tetragenococcus, Lactobacillus, Bacillus, and Pseudomonas), and five (Tetragenococcus, Lactobacillus, Bacillus, Pseudomonas, and Pediococcus) genera are considered the core functional bacteria of Tianbanzi, chili pei, and paste fermentation, respectively.

Keywords: Microbial community, Broad bean paste with chili, Canonical correspondence analysis, Flavor compounds, Core bacteria

References(70)

[1]

J.Y. Jung, S.H. Lee, C.O. Jeon, Kimchi micro flora: history, current status, and perspectives for industrial kimchi production, Appl. Microbiol. Biotechnol.98 (2014) 2385-2393. https://doi.org/10.1007/s00253-014-5513-1.

[2]

M. Kuligowski, K. Pawłowska, I. Jasińskakuligowska, et al., Iso flavone composition, polyphenols content and antioxidative activity of soybean seeds during tempeh fermentation, CyTA-J. Food 15 (2016) 27-33. https://doi.org/10.1080/19476337.2016.1197316.

[3]

M.J. Kim, H.S. Kwak, S.S. Kim, Effects of salinity on bacterial communities, Maillard reactions, iso flavone composition, antioxidation and antiproliferation in Korean fermented soybean paste (doenjang), Food Chem. 245 (2018) 402-409. https://doi.org/10.1016/j.foodchem.2017.10.116.

[4]

Y.S. Cha, Y. Park, M. Lee, et al., Doenjang, a Korean fermented soy food, exerts antiobesity and antioxidative activities in overweight subjects with the PPAR-γ2 C1431T polymorphism: 12-week, double-blind randomized clinical trial, J. Med. Food 17 (2014) 119-127. https://doi.org/10.1089/jmf.2013.2877.

[5]

Y. Murooka, M. Yamshita, Traditional healthful fermented products of Japan, J. Ind. Microbiol. Biot. 35 (2008) 791-798. https://doi.org/10.1007/s10295-008-0362-5.

[6]

X.S. Wang, H. Du, Y. Xu, Source tracking of prokaryotic communities in fermented grain of Chinese strong- flavor liquor, Int. J. Food Microbiol. 244(2017) 27-35. https://doi.org/10.1016/j.ijfoodmicro.2016.12.018.

[7]

C.D. Wu, C.L. Liu, G.Q. He, et al., Characterization of a multiple-stress tolerance Tetragenococcus halophilus and application as starter culture in Chinese horsebean-chili-paste manufacture for quality improvement, Food Sci. Technol. Res. 19 (2013) 855-864. https://doi.org/10.3136/fstr.19.855.

[8]

L. Guan, Analysis of the cultivable bacterial community in jeotgal, a Korean salted and fermented seafood, and identification of its dominant bacteria, Food Microbiol. 28 (2011) 101-113. https://doi.org/10.1016/j.fm.2010.09.001.

[9]

T.W. Kim, J.H. Lee, M.H. Park, et al., Analysis of bacterial and fungal communities in Japanese- and Chinese-fermented soybean pastes using nested PCR-DGGE, Curr. Microbiol. 60 (2010) 315-320.https://doi.org/10.1007/s00284-009-9542-4.

[10]

T.A. NgâOngâOla-Manani, T. Wicklund, A.M. Mwangwela, et al., Identification and characterization of lactic acid bacteria involved in natural and lactic acid bacterial fermentations of pastes of soybeans and soybeanmaize blends using culture-dependent techniques and denaturing gradient gel electrophoresis, Food Biotechnol. 29 (2015) 20-50. https://doi.org/10.1080/08905436.2014.996894.

[11]

L.J. Zhu, Z.H. Fan, H. Kuai, et al., Batch-batch stable microbial community in the traditional fermentation process of huyumei broad bean pastes, Lett.Appl. Microbiol. 65 (2017) 226-233. https://doi.org/10.1111/lam.12765.

[12]

S.J. Jang, Y.J. Kim, J.M. Park, et al., Analysis of micro flora in gochujang, Korean traditional fermented food, Food Sci. Biotechnol. 20 (2011) 1435-1440. https://doi.org/10.1007/s10068-011-0197-0.

[13]

Z.R. Huang, J.L. Hong, J.X. Xu, et al., Exploring core functional microbiota responsible for the production of volatile flavour during the traditional brewing of Wuyi Hong Qu glutinous rice wine, Food Microbiol. 76 (2018)487-496. https://doi.org/10.1016/j.fm.2018.07.014.

[14]

Z.W. Song, H. Du, Y. Zhang, et al., Unraveling core functional microbiota in traditional solid-state fermentation by high-throughput amplicons and metatranscriptomics sequencing, Front. Microbiol. 8 (2017) 1294.https://doi.org/10.3389/fmicb.2017.01294.

[15]

M. Ogasawara, Y. Yamada, M. Egi, Taste enhancer from the longterm ripening of miso (soybean paste), Food Chem. 99 (2006) 736-741.https://doi.org/10.1016/j.foodchem.2005.08.051.

[16]

L. Armada, E. Fernandez, E. Falque, Influence of several enzymatic treatments on aromatic composition of white wines, LWT-Food Sci.Technol. 43 (2010) 1517-1525. https://doi.org/10.1016/j.lwt.2010.06.009.

[17]

J. Seo, H. Gordishdressman, E.P. Hoffman, An interactive power analysis tool for microarray hypothesis testing and generation, Bioinformatics 22(2006) 808-814. https://doi.org/10.1093/bioinformatics/btk052.

[18]

J.G. Caporaso, J. Kuczynski, J. Stombaugh, et al., QIIME allows analysis of high-throughput community sequencing data, Nat. Methods 7 (2010) 335-336. https://doi.org/10.1038/nmeth.f.303.

[19]
M. Bastian, S. Heymann, M. Jacomy, In Gephi: an open source software for exploring and manipulating networks, International AAAI Conference on Weblogs and Social Media (2009) 361-362.
DOI
[20]

Y.J. Choi, S. Yong, M.J. Lee, Changes in volatile and non-volatile compounds of model kimchi through fermentation by lactic acid bacteria, LWT-Food Sci. Technol. 105 (2019) 118-126. https://doi.org/10.1016/j.lwt.2019.02.001.

[21]

G.Y. Jin, Y. Zhu, Y. Xu, Mystery behind Chinese liquor fermentation, Trends Food Sci. Tech. 63 (2017) 18-28. https://doi.org/10.1016/j.tifs.2017.02.016.

[22]

H.L. Liu, B.G. Sun, Effect of fermentation processing on the flavor of Baijiu, J. Agr. Food Chem. 66 (2018) 5425-5432. https://doi.org/10.1021/acs.jafc.8b00692.

[23]

X. Gao, C. Cui, J. Ren, Changes in the chemical composition of traditional Chinese-type soy sauce at different stages of manufacture and its relation to taste, Int. J. Food Sci. Tech. 46 (2011) 243-249. https://doi.org/10.1111/j.1365-2621.2010.02487.x.

[24]

Y. Jia, C. T. Niu, Z. M. Lu, A bottom-up approach to develop a synthetic microbial community model: application for efficient reduced-salt broad bean paste fermentation, Appl. Environ. Microb. 86 (2020) e00306-20.https://doi.org/10.1128/AEM.00306-20.

[25]

C.C. Chou, M.Y. Ling, Biochemical changes in soy sauce prepared with extruded and traditional raw materials, Food Res. Int. 31 (1998) 487-492.https://doi.org/10.1016/S0963-9969(99)00017-4.

[26]

Y.S.C. Shieh, L.R. Beuchat, R.E. Worthington, et al., Physical and chemical changes in fermented peanut and soybean pastes containing Kojis prepared using Aspergillus oryzae and Rhizopus oligosporus, J. Food Sci. 47 (1982)523-529. https://doi.org/10.1111/j.1365-2621.1982.tb10116.x.

[27]

L. Seungjoo, A. Bomi, Comparison of volatile components in fermented soybean pastes using simultaneous distillation and extraction (SDE) with sensory characterisation, Food Chem. 114 (2009) 600-609. https://doi.org/10.1016/j.foodchem.2008.09.091.

[28]

H.Y. Chung, Volatile components in fermented soybean (Glycine max) curds, J. Agr. Food Chem. 47 (1999) 2690-2696. https://doi.org/10.1021/jf981166a.

[29]

J. Zang, Y. Xu, W. Xia, Correlations between microbiota succession and flavor formation during fermentation of Chinese low-salt fermented common carp (Cyprinus carpio L.) inoculated with mixed starter cultures, Food Microbiol. 90 (2020) 103487. https://doi.org/10.1016/j.fm.2020.103487.

[30]

S.H. Jeong, H.J. Lee, J.Y. Jung, Effects of red pepper powder on microbial communities and metabolites during kimchi fermentation, Int. J. Food Microbiol. 160 (2013) 252-259. https://doi.org/10.1016/j.ijfoodmicro.2012.10.015.

[31]

Y.S. Moy, T.J. Lu, C.C. Chou, Volatile components of the enzyme-ripened sufu, a Chinese traditional fermented product of soy bean, J. Biosci. Bioeng.113 (2012) 196-201. https://doi.org/10.1016/j.jbiosc.2011.09.021.

[32]

M. Steinhaus, D. Sinuco, J. Polster, et al., Characterization of the key aroma compounds in Pink Guava (Psidium guajava L.) by means of aroma reengineering experiments and omission tests, J. Agr. Food Chem. 57 (2009)2882-2888. https://doi.org/10.1021/jf803728n.

[33]

Y. Feng, Y. Cai, G. Su, Evaluation of aroma differences between high-salt liquid-state fermentation and low-salt solid-state fermentation soy sauces from China, Food Chem. 145 (2014) 126-134. https://doi.org/10.1016/j.foodchem.2013.07.072.

[34]

Y. Mori, K. Kiuchi, H. Tabei, Flavor components of miso: basic fraction, Agric. Biol. Chem. 47 (1983) 1487-1492. https://doi.org/10.1080/00021369.1983.10865811.

[35]

J. Pérez-Jiménez, F. Saura-Calixto, Macromolecular antioxidants or nonextractable polyphenols in fruit and vegetables: intake in four European countries. Food Res. Int. 74 (2015) 315-323. https://doi.org/10.1016/j.foodres.2015.05.007.

[36]

M. Gómez, J. M. Lorenzo, Effect of fat level on physicochemical, volatile compounds and sensory characteristics of dry-ripened "chorizo" from Celta pig breed, Meat Sci. 95 (2013) 658-666. https://doi.org/10.1016/j.meatsci.2013.06.005.

[37]

L. Belleggia, L. Aquilanti, I. Ferrocino, Discovering microbiota and volatile compounds of surströmming, the traditional Swedish sour herring, Food Microbiol. 91 (2020) 103503. https://doi.org/10.1016/j.fm.2020.103503.

[38]

Y. Xiao, Y. Liu, C. Chen, et al., Effect of Lactobacillus plantarum and Staphylococcus xylosus on flavour development and bacterial communities in Chinese dry fermented sausages, Food Res. Int. 135 (2020) 109247.https://doi.org/10.1016/j.foodres.2020.109247.

[39]

C. Murat, K. Gourrat, H. Jerosch, et al., Analytical comparison and sensory representativity of SAFE, SPME, and Purge and Trap extracts of volatile compounds from pea flour, Food Chem. 135 (2012) 913-920.https://doi.org/10.1016/j.foodchem.2012.06.015.

[40]

M.J. Kim, H.S. Kwak, H.Y. Jung, et al., Microbial communities related to sensory attributes in Korean fermented soy bean paste (doenjang), Food Res.Int. 89 (2016) 724-732. https://doi.org/10.1016/j.foodres.2016.09.032.

[41]

Z.H. Li, J.P. Rui, X.Z. Li, et al., Bacterial community succession and metabolite changes during doubanjiang-meju fermentation, a Chinese traditional fermented broad bean (Vicia faba L.) paste, Food Chem. 218(2017) 534-542. https://doi.org/10.1016/j.foodchem.2016.09.104.

[42]

J.W. Yong, J.J. Young, L.H. Jung, et al., Functional characterization of bacterial communities responsible for fermentation of Doenjang: a traditional Korean fermented soybean paste, Front. Microbiol. 7 (2016) 827.https://doi.org/10.3389/fmicb.2016.00827.

[43]

S. Banerjee, K. Schlaeppi, M.G.A van der Heijden, Keystone taxa as drivers of microbiome structure and functioning, Nat. Rev. Microbiol. 16 (2018)567-576. https://doi.org/10.1038/s41579-018-0024-1.

[44]

S. Wang, Q. Wu, Y. Nie, et al., Construction of synthetic microbiota for reproducible flavor compound metabolism in Chinese light-aroma-type liquor produced by solid-state fermentation, Appl. Environ. Microbiol. 85(2019) e03090-03018. https://doi.org/10.1128/AEM.03090-18.

[45]

I. Stefanini, D. Cavalieri, Metagenomic approaches to investigate the contribution of the vineyard environment to the quality of wine fermentation: potentials and difficulties, Front. Microbiol. 9 (2018) 991.https://doi.org/10.3389/fmicb.2018.00991.

[46]

L. Zhang, Z. Chen, W. Xu, et al., Dynamics of physicochemical factors and microbial communities during ripening fermentation of Pixian Doubanjiang, a typical condiment in Chinese cuisine, Food Microbiol. 86 (2020) 103342.https://doi.org/10.1016/j.fm.2019.103342.

[47]

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.

[48]

Y. Zheng, J. Mou, J.W. Niu, et al., Succession sequence of lactic acid bacteria driven by environmental factors and substrates throughout the brewing process of Shanxi aged vinegar, Appl. Microbiol. Biot. 102 (2018)2645-2658. https://doi.org/10.1007/s00253-017-8733-3.

[49]

N. Udomsil, S. Rodtong, Y.J. Choi, et al., Use of Tetragenococcus halophilus as a starter culture for flavor improvement inflsh sauce fermentation, J. Agr.Food Chem. 59 (2011) 8401-8408. https://doi.org/10.1021/jf201953v.

[50]

S.H. Lee, J.Y. Jung, C.O. Jeon, Effects of temperature on microbial succession and metabolite change during saeu-jeot fermentation, Food Microbiol. 38 (2014) 16-25. https://doi.org/10.1016/j.fm.2013.08.004.

[51]

S.H. Jeong, J.Y. Jung, S.H. Lee, et al., Microbial succession and metabolite changes during fermentation of dongchimi, traditional Korean watery kimchi, Int. J. Food Microbiol. 164 (2013) 46-53. https://doi.org/10.1016/j.ijfoodmicro.2013.03.016.

[52]

J.H. Kang, J.H. Lee, S. Min, et al., Changes of volatile compounds, lactic acid bacteria, pH, and headspace gases in Kimchi, a traditional Korean fermented vegetable product, J. Food Sci. 68 (2003) 849-854. https://doi.org/10.1111/j.1365-2621.2003.tb08254.x.

[53]

Z. Li, L. Dong, Q. Huang, et al., Bacterial communities and volatile compounds in Doubanjiang, a Chinese traditional red pepper paste, J. Appl.Microbiol. 120 (2016) 1585-1594. https://doi.org/10.1111/jam.13130.

[54]

J.Y. Jung, S.H. Lee, C.O. Jeon, Microbial community dynamics during fermentation of doenjang-meju, traditional Korean fermented soybean, Int. J. Food Microbiol. 185 (2014) 112-120. https://doi.org/10.1016/j.ijfoodmicro.2014.06.003.

[55]

S.J. Choi, J.J. Jung, O.J. Che, et al., Comparative genomic and transcriptomic analyses of NaCl-tolerant Staphylococcus sp. OJ82 isolated from fermented seafood, Appl. Microbiol. Biot. 98 (2014) 807-822. https://doi.org/10.1007/s00253-013-5436-2.

[56]

S. Taponen, K. Supré, V. Piessens, et al., Staphylococcus agnetis sp. nov., a coagulase-variable species from bovine subclinical and mild clinical mastitis, Int. J. Syst. Evol. Micr. 62 (2012) 61-65. https://doi.org/10.1099/ijs.0.028365-0.

[57]

D. Ou, H. Li, W. Li, Salt-tolerance aerobic granular sludge: Formation and microbial community characteristics, Bioresource Technol. 249 (2018) 132-138. https://doi.org/10.1016/j.biortech.2017.07.154.

[58]

Y.S. Kim, M.C. Kim, S.W. Kwon, et al., Analyses of bacterial communities in meju, a Korean traditional fermented soybean bricks, by cultivationbased and pyrosequencing methods, J. Microbiol. 49 (2011) 340-348.https://doi.org/10.1007/s12275-011-0302-3.

[59]

X. Zeng, L. He, X. Guo, Predominant processing adaptability of Staphylococcus xylosus strains isolated from Chinese traditional lowsalt fermented whole fish, Int. J. Food Microbiol. 242 (2017) 141-151.https://doi.org/10.1016/j.ijfoodmicro.2016.11.014.

[60]

X. Wang, H. Du, Y. Xu, Source tracking of prokaryotic communities in fermented grain of Chinese strong- flavor liquor, Int. J. Food Microbiol. 244(2017) 27-35. https://doi.org/10.1016/j.ijfoodmicro.2016.12.018.

[61]

A. Martín, B. Colín, E. Aranda, et al., Characterization of micrococcaceae isolated from Iberian dry-cured sausages, Meat Sci. 75 (2007) 696-708.https://doi.org/10.1016/j.meatsci.2006.10.001.

[62]

A. Ruaro, C. Andrighetto, S. Torriani, et al., Biodiversity and characterization of indigenous coagulase-negative Staphylococci isolated from raw milk and cheese of North Italy, Food Microbiol. 34 (2013) 106-111. https://doi.org/10.1016/j.fm.2012.11.013.

[63]

S. Lee, S. Lee, D. Singh, et al., Comparative evaluation of microbial diversity and metabolite profiles in doenjang, a fermented soybean paste, during the two different industrial manufacturing processes, Food Chem. 221(2017) 1578-1586. https://doi.org/10.1016/j.foodchem.2016.10.135.

[64]

L.T. Wang, F.L. Lee, C.J. Tai, et al., Bacillus velezensis is a later heterotypic synonym of Bacillus amyloliquefaciens, Int. J. Syst. Evol. Micr. 58 (2008)671-675. https://doi.org/10.1099/ijs.0.65191-0.

[65]

M. Chang, H.M. Song, H.C. Chang, Isolation of Bacillus velezensis SSH100-10 with antifungal activity from Korean traditional soysauce and characterization of its antifungal compounds, Korean Journal of Food Preservation 19 (2012) 757-766. https://doi.org/10.11002/kjfp.2012.19.5.757.

[66]

D. Ren, P. Chen, W.T. Li, et al., Screening, mutagenesis of nitrite-degrading Lactobacilli in Chinese traditional fermented sauerkraut and its application in the production of sauerkraut, J. Food Safety 36 (2016) 474-481.https://doi.org/10.1111/jfs.12264.

[67]

Z.X. Wang, Y.Y. Shao, Effects of microbial diversity on nitrite concentration in pao cai, a naturally fermented cabbage product from China, Food Microbiol. 72 (2018) 185-192. https://doi.org/10.1016/j.fm.2017.12.003.

[68]

N. Bhaskar, P.V. Suresh, P.Z. Sakhare, et al., Shrimp biowaste fermentation with Pediococcus acidolactici CFR2182: optimization of fermentation conditions by response surface methodology and effect of optimized conditions on deproteination/demineralization and carotenoid recovery, Enzyme Microbiol. Technol. 40 (2007) 1427-1434. https://doi.org/10.1016/j.enzmictec.2006.10.019.

[69]

M. Sparo, G.G. Nuñez, M. Castro, et al., Characteristics of an environmental strain, Enterococcus faecalis CECT7121, and its effects as additive on craft dry-fermented sausages, Food Microbiol. 25 (2008) 607-615.https://doi.org/10.1016/j.fm.2008.01.008.

[70]

L.L. Torre, A.Y. Tamime, D.D. Muir, Rheology and sensory profiling of set-type fermented milks made with different commercial probiotic and yoghurt starter cultures, Int. J. Dairy Technol. 56 (2003) 163-170.https://doi.org/10.1046/j.1471-0307.2003.00098.x.

Publication history
Copyright
Acknowledgements
Rights and permissions

Publication history

Received: 12 March 2020
Revised: 16 August 2021
Accepted: 21 May 2021
Published: 28 April 2022
Issue date: July 2022

Copyright

© 2022 Beijing Academy of Food Sciences. Publishing services by Elsevier B.V. on behalf of KeAi Communications Co., Ltd.

Acknowledgements

Acknowledgement

This work was supported by the National Key R & D Program of China (2016YFD0400505), China Postdoctoral Science Foundation (2018M640241), Tianjin Postdoctoral Foundation (TJQYBSH2018010), Tianjin Municipal Education Commission (TD13-5013, 2018ZD08), and Key Laboratory of Industrial Fermentation Microbiology, Education Ministry of China (2018KF005).

Rights and permissions

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Return