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Monitoring the microbial community succession and diversity of Liangzhou fumigated vinegar during solid-state fermentation with next-generation sequencing

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Abstract

This study reveals the microbial community succession and diversity during the whole solid-fermentation processes of naturally fermented Liangzhou fumigated vinegar (LZFV). Dynamics and diversity of microbial community succession in “Daqu” starter and other fermentation stages (starch saccharification, alcoholic fermentation, and acetic acid fermentation) were monitored using a metagenomic approach involving high-throughput sequencing. Meanwhile, dynamic changes of characteristic flavor compounds of vinegar were determined by gas chromatograph (GC) analysis. The result showed that the microbiota composition exhibited rich diversity. Twenty-five bacterial and 18 fungal genera were found in the whole fermentation process where Lactobacillus, Acetobacter, Aspergillus, Saccharomyces, and Alternaria were the predominant microorganisms. Alpha diversity metrics showed that bacterial diversity in Daqu was greater than that in AF and AAF. By contrast, fungal diversity increased from Daqu to AF and decreased in the initial stage (5–8 days) of AAF then remained relatively steady. Hence, these results could help understand dynamics of microbial community succession in continuous fermentation of traditional Chinese vinegars. The LZFV fermentation is a continuous process with spontaneous growth that affects the dynamics of microbial communities. Continuous changes of micro-environment conditions in substrate affect the diversity and structure of microbiota. Microbial growth and metabolism were closely related to the changes in the physicochemical characteristics of the cultures. The microbial flora composition showed rich diversity, and with the increase in brewing time and the change in micro-ecological environmental conditions; the microbial community showed a complex dynamic changes.

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References

  • An ZG (2011) Microbial succession and metabolism during traditional brewing process of Liangzhou fumigated vinegar. Master degree dissertation. Gansu Agri Univ, Lanzhou (In Chinese)

    Google Scholar 

  • Cao YN, Yuan TZ, Shi PJ, Luo HY, Li N, Bai YG, Yang PL, Zhou ZG, Zhang ZF, Yao B (2010) Properties of a novel α-galactosidase from Streptomyces sp. S27 and its potential for soybean processing. Enzym Microb Technol 47:305–312. https://doi.org/10.1016/j.enzmictec.2010.09.007

    Article  CAS  Google Scholar 

  • Chen FS, Li L, Qu J, Chen CX (2009) Cereal vinegars made by solid-state fermentation in China. In: Solieri L, Giudici P (eds) Vinegars of the world. Springer, Milan, pp 243–259

    Chapter  Google Scholar 

  • Chen QS, Liu AP, Zhao JW, Qin OY (2013) Monitoring vinegar acetic fermentation using a colorimetric sensor array. Sensors Actuators B Chem 183:608–616. https://doi.org/10.1016/j.snb.2013.04.033

    Article  CAS  Google Scholar 

  • Divakar G, Sunitha M, Vasu P, Udayashanker P, Ellaiah P (2006) Optimization of process parameters for alkaline protease production under solid-state fermentation by thermocline happily PEE 14. Indian J Biotechnol 5:80–83

    CAS  Google Scholar 

  • Ercolini D (2013) High-throughput sequencing and metagenomics: moving forward in the cultural-independent analysis of food microbial ecology. Appl Environ Microbiol 79:3148–3155. https://doi.org/10.1128/AEM.00256-13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fett WF, Wijey C, Moreau RA, Osman SF (2000) Production of cutinolytic esterase by filamentous bacteria. Europe PubMed Central Plus 31:25–29

    CAS  Google Scholar 

  • Han QH (2013) Study on the relationship between microbial community and vinegar flavor in the traditional brewing process of Liangzhou fumigated vinegar. Master degree dissertation. Gansu Agri Univ, Lanzhou

    Google Scholar 

  • Haruta S, Ueno S, Egawa I, Hashiguchi K, Fujii A, Nagano M, Igarashi Y (2006) Succession of bacterial and fungal communities during a traditional pot fermentation of rice vinegar assessed by PCR-mediated denaturing gradient gel electrophoresis. Int J Food Microbiol 109:79–87. https://doi.org/10.1016/j.ijfoodmicro.2006.01.015

    Article  CAS  PubMed  Google Scholar 

  • He ZY, Ao ZH, Wu Y, Li GQ, Tao WY (2004) Determination and generant mechanism of tetramethylpyrazine in Zhengjiang vinegar. China Condiment 2:36–39

    CAS  Google Scholar 

  • Illeghems K, De Vuyst L, Papalexandratou Z, Weckx S (2012) Plyogenetic analysis of environmental sequences using MEGAN4. Genome Res 21:1552–1560

    Google Scholar 

  • Jung JY, Lee SH, Kim JM, Park MS, Bae JW, Hahn Y, Madsen EL, Jeon CO (2011) Metagenomic analysis of kimchi, a traditional Korean fermented food. Appl Environ Microbiol 77:2264–2274. https://doi.org/10.1128/AEM.02157-10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Larroche C, Besson I, Gros JB (1999) High pyrazine production by Bacillus subtilis in solid substrate fermentation on ground soybeans. Process Biochem 34:667–674. https://doi.org/10.1016/S0032-9592(98)00141-1

    Article  CAS  Google Scholar 

  • Li K (2014) Microbial community and diversity of fermentated yellow water in Chinese intense flavor liquor cellar. Master degree dissertation. Xihua Univ, Chengdu (In Chinese)

    Google Scholar 

  • Liu W, Xi X, Sudu Q, Kwok L, Guo Z, Hou Q, Zhang H (2015) High-throughput sequencing reveals microbial community diversity of Tibetan naturally fermented yak milk. Ann Microbiol 65:1741–1751. https://doi.org/10.1007/s13213-014-1013-x

    Article  CAS  Google Scholar 

  • Lu ZM, Liu N, Wang LJ, Wu LH, Gong JS, Yu YJ, Li GQ, Shi JS, Xu ZH (2016) Elucidating and regulating the acetoin production role of microbial functional groups in multispecies acetic acid fermentation. Appl Environ Microbiol 82:5860–5868

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mamlouk D, Hidalgo C, Torija MJ, Gullo M (2011) Evaluation and optimisation of bacterial genomic DNA extraction for no-culture techniques applied to vinegars. Food Microbiol 28:1374–1379. https://doi.org/10.1016/j.fm.2011.06.009

    Article  CAS  PubMed  Google Scholar 

  • Miller GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem 31:426–428

  • Nie Z, Zheng Y, Wang M, Han Y, Wang Y, Luo J, Niu D (2013) Exploring microbial succession and diversity during solid-state fermentation of Tianjin duliu mature vinegar. Bioresour Technol 148:325–333. https://doi.org/10.1016/j.biortech.2013.08.152

    Article  CAS  PubMed  Google Scholar 

  • Nie ZQ, Zheng Y, Xie SK, Zhang XL, Song J, Xia ML, Wang M (2017) Unraveling the correlation between microbiota succession and metabolite changes in traditional Shanxi aged vinegar. Sci Rep 7:9240. https://doi.org/10.1038/s41598-017-09850-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Polka J, Rebecchi A, Pisacane V, Morelli L, Puglisi E (2015) Bacterial diversity in typical Italian salami at different ripening stages as revealed by high-throughput sequencing of 16S rRNA amplicons. Food Microbiol 46:342–356. https://doi.org/10.1016/j.fm.2014.08.023

    Article  CAS  PubMed  Google Scholar 

  • Richter CL, Dunn B, Sherlock G, Pugh T (2013) Comparative metabolic footprinting of a large number of commercial wine yeast strains in chardonnay fermentations. FEMS Yeast Res 13:394–410

    Article  CAS  PubMed  Google Scholar 

  • Roh SW, Kim KH, Nam YD, Chang HW, Park EJ, Bae JW (2010) Investigation of archaeal and bacterial diversity in fermented seafood using barcoded pyrosequecing. ISME J 4:1–16

    Article  CAS  PubMed  Google Scholar 

  • Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Simpson EH (1949) Measurement of diversity. Nature 163:688. https://doi.org/10.1038/163688a

    Article  Google Scholar 

  • Thomas KC, Ingledew WM (1990) Fuel alcohol production: effects of free amino nitrogen on fermentation of very-high-gravity wheat mashes. Appl Environ Microbiol 56:2046–2050

  • Wu JH, Hao L, Bai RH (2004) Ecological distribution of microbe in Shanxi super vinegar Duqu. J Shanxi Agar Univ 24:279–282

    Google Scholar 

  • Wu Q, Chen L, Xu Y (2013) Yeast community associated with the solid state fermentation of traditional Chinese Maotai-flavor liquor. Int J Food Microbiol 166:323–330. https://doi.org/10.1016/j.ijfoodmicro

    Article  CAS  PubMed  Google Scholar 

  • Xiao Z, Lu JR, Ma C, Xu P (2009) Formation and identification of trimethylimidazole during tetramethylpyrazine production from glucose by Bacillus strains. Biotechnol Lett 31:1421–1425

    Article  CAS  PubMed  Google Scholar 

  • Xu W, Zhang XJ, Xu HY, Xu ZH, Zhao LP (2007) Analysis of bacterial communities isolated from solid-state fermentation culture of Zhengjiang Henshun vinegar. Microbiol 34:646–649

    CAS  Google Scholar 

  • Xu W, Huang Z, Zhang X, Li Q, Lu Z, Shi J, Ma Y (2011) Monitoring the microbial community during solid-state acetic acid fermentation of Zhenjiang aromatic vinegar. Food Microbiol 28:1175–1181. https://doi.org/10.1016/j.fm.2011.03.011

    Article  CAS  PubMed  Google Scholar 

  • Yao S, Liu Y, Zhang MJ, Zhang X, Li H, Zhao T, Xin CH, Xu L, Zhang BL, Cheng C (2014) Thermoactinomyces daqus sp. nov, a thermophilic bacterium isolated from high-temperature Daqu. Int J Syst Evol Microbiol 64:206–210. https://doi.org/10.1099/ijs.0.055509-0

    Article  CAS  PubMed  Google Scholar 

  • Yao S, Liu Y, Li H, Ge YY, Zhang MJ, Xin CH, Xu L, Cheng C (2015) Bacterial communities during the process of high-temperature Daqu production of roasted sesame-like flavour liquor. J Inst Brew 121:440–448

    Article  CAS  Google Scholar 

  • Yousif NM, Huch M, Schhuster T, Cho GS, Dirar HA, Holzapfel WH, Franz CM (2010) Diversity of lactic acid bacteria from Hussuwa, a traditional African fermented sorghum food. Food Microbiol 27:757–768. https://doi.org/10.1016/j.fm.2010.03.012

    Article  CAS  PubMed  Google Scholar 

  • Zhao FQ (2016) The effects of major functional microbial succession on tetramethylpyrazine during the traditional brewing process of Liangzhou fumigated vinegar. Master degree dissertation. Gansu Agri Univ, Lanzhou (In Chinese)

    Google Scholar 

  • Zhao LQ, Li L (2005) The history, present status, development trend of the production technology of Chinese vinegar. China Condiment 2:15–17

    Google Scholar 

  • Zhao HY, Yun JM (2016) Isolation, identification and fermentation conditions of highly acetoin-producing acetic acid bacterium from Liangzhou fumigated vinegar in China. Ann Microbiol 66:279–288. https://doi.org/10.1007/s13213-015-1106-1

    Article  CAS  Google Scholar 

  • Zheng XW, Tabrizi MR, Nout MJR, Han BZ (2011) Daqu—A traditional Chinese liquor fermentation starter. J Inst Brew 117:82–90

    Article  CAS  Google Scholar 

  • Zhu BF, Xu Y, Fan WL (2010) High-yield fermentative preparation of tetramethylpyrazine by Bacillus sp. using an endogenous precursor approach. J Ind Microbiol Biotechnol 37:179–186. https://doi.org/10.1007/s10295-009-0661-5

    Article  CAS  PubMed  Google Scholar 

  • Zhu QL, Liu S, Gao P, Luan FS (2014) High-throughput sequencing technology and its application. J Northeast Agric Univ 21:84–96

    CAS  Google Scholar 

Download references

Funding

This study was supported by the Ministry of Science and Technology, P. R. China, under the Nature Science Foundation of China (NSFC) (NO. 31360405), and the Gansu Province Key Laboratory of Food Science and Technology, Gansu Agricultural University, is gratefully acknowledged.

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Correspondence to Jianmin Yun.

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Yun, J., Zhao, F., Zhang, W. et al. Monitoring the microbial community succession and diversity of Liangzhou fumigated vinegar during solid-state fermentation with next-generation sequencing. Ann Microbiol 69, 279–289 (2019). https://doi.org/10.1007/s13213-018-1418-z

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