Skip to main content
Log in

Diversity and dynamics stability of bacterial community in traditional solid-state fermentation of Qishan vinegar

  • Original Article
  • Published:
Annals of Microbiology Aims and scope Submit manuscript

Abstract

Qishan vinegar is a typical Chinese fermented cereal product that is prepared using traditional solid-state fermentation (SSF) techniques. The final qualities of the vinegar produced are closely related to the multiple bacteria present during SSF. In the present study, the dynamics of microbial communities and their abundance in Daqu and vinegar Pei were investigated by the combination of high throughput sequencing and quantitative PCR. Results showed that the Enterobacteriales members accounted for 94.7%, 94.6%, and 92.2% of total bacterial sequences in Daqu Q3, Q5, and Q10, respectively. Conversely, Lactobacillales and Rhodospirillales dominated during the acetic acid fermentation (AAF) stage, corresponding to the quantitative PCR results. Lactobacillus, Acetobacter, Weissella, Leuconostoc and Bacillus were the dominant and characteristic bacterial genera of Qishan vinegar during AAF process. Redundancy analysis suggested that Lactobacillales and Rhodospirillales had a positive correlation with humidity and acidity, respectively. These results confirmed that the bacterial community structure could be affected by physiochemical factors, which determined the unique bacterial composition at different fermentation stages and showed batch-to-batch consistency and stability. Therefore, the conformity of bacterial community succession with physiochemical parameters guaranteed the final quality of Qishan vinegar products. This study provided a scientific perspective for the uniformity and stability of Qishan vinegar, and might aid in controlling the manufacturing process.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Bokulich NA, Subramanian S, Faith JJ et al (2013) Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nat Methods 10:57–59

    Article  CAS  PubMed  Google Scholar 

  • Bokulich NA, Amiranashvili L, Chitchyan K et al (2015) Microbial biogeography of the transnational fermented milk matsoni. Food Microbiol 50:12–19

    Article  PubMed  Google Scholar 

  • Carranza P, Grunau A, Schneider T et al (2010) A gel-free quantitative proteomics approach to investigate temperature adaptation of the food-borne pathogen Cronobacter turicensis 3032. Proteomics 10:3248–3261

    Article  CAS  PubMed  Google Scholar 

  • Chen JC, Chen QH, Qin G, Sue R, Hui R, He GQ, Gu Q (2010) Simultaneous determination of acetoin and tetramethylpyrazine in traditional vinegars by HPLC method. Food Chem 122:1247–1252

    Article  CAS  Google Scholar 

  • Chen Q, Liu B, Wang J, Che J, Liu G, Guan X (2017) Diversity and dynamics of the bacterial community involved in pig manure biodegradation in a microbial fermentation bed system. Ann Microbiol 67:1–10

    Article  Google Scholar 

  • Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998

    Article  CAS  PubMed  Google Scholar 

  • Fraqueza MJ (2015) Antibiotic resistance of lactic acid bacteria isolated from dry-fermented sausages. Int J Food Microbiol 212:76–88

    Article  CAS  PubMed  Google Scholar 

  • Gao C, Wang A, Wu W, Yin Y, Zhao Y (2014) Enrichment of anodic biofilm inoculated with anaerobic or aerobic sludge in single chambered air-cathode microbial fuel cells. Bioresour Technol 167:124–132

    Article  CAS  PubMed  Google Scholar 

  • González-Arenzana L, López R, Santamaría P, López-Alfaro I (2013) Dynamics of lactic acid bacteria populations in Rioja wines by PCR-DGGE, comparison with culture-dependent methods. Appl Microbiol Biotechnol 97:6931–6941

    Article  PubMed  Google Scholar 

  • Gou M, Wang H, Yuan H, Zhang W, Tang Y, Kida K (2015) Characterization of the microbial community in three types of fermentation starters used for Chinese liquor production. J Inst Brew 121:620–627

    Article  CAS  Google Scholar 

  • Ivone VM, Conceição E, Nunes OC, Manaia CM (2013) Bacterial diversity from the source to the tap: a comparative study based on 16S rRNA gene-DGGE and culture-dependent methods. FEMS Microbiol Ecol 83:361–374

    Article  Google Scholar 

  • Kim SH, Cho HK, Shin HS (2012) Physicochemical properties and antioxidant activities of commercial vinegar drinks in Korea. Food Sci Biotechnol 21:1729–1734

    Article  CAS  Google Scholar 

  • Kittelmann M, Stamm WW, Follmann H, Trüper HG (1989) Isolation and classification of acetic acid bacteria from high percentage vinegar fermentation. Appl Microbiol Biotechnol 30:47–52

    Article  CAS  Google Scholar 

  • Li P, Li S, Cheng L, Luo L (2014) Analyzing the relation between the microbial diversity of DaQu and the turbidity spoilage of traditional Chinese vinegar. Appl Microbiol Biotechnol 98:6073–6084

    Article  CAS  PubMed  Google Scholar 

  • Li P, Aflakpui FWK, Yu H, Luo L, Lin W (2015a) Characterization of activity and microbial diversity of typical types of Daqu for traditional Chinese vinegar. Ann Microbiol 65:2019–2027

    Article  Google Scholar 

  • Li P, Liang H, Lin W, Feng F, Luo L (2015b) Microbiota dynamics associated with environmental conditions and potential roles of Cellulolytic communities in traditional Chinese cereal starter solid-state fermentation. Appl Environ Microbiol 81:5144–5156

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li S, Li P, Liu X, Luo L, Lin W (2016a) Bacterial dynamics and metabolite changes in solid-state acetic acid fermentation of Shanxi aged vinegar. Appl Microbiol Biotechnol 100:1–17

    Article  CAS  Google Scholar 

  • Li Z, Li H, Bian K (2016b) Microbiological characterization of traditional dough fermentation starter (Jiaozi) for steamed bread making by culture-dependent and culture-independent methods. Int J Food Microbiol 234:9–14

    Article  CAS  PubMed  Google Scholar 

  • Liang H, Ye D, Li P, Su T, Wu J, Luo L (2016) Evolution of bacterial consortia in an integrated tannery wastewater treatment process. RSC Adv 6:87380–87388

    Article  CAS  Google Scholar 

  • Liljeberg H, Björck I (1998) Delayed gastric emptying rate may explain improved glycaemia in healthy subjects to a starchy meal with added vinegar. Eur J Clin Nutr 52:368–371

    Article  CAS  PubMed  Google Scholar 

  • Liu D, Zhang R, Wu H et al (2011) Changes in biochemical and microbiological parameters during the period of rapid composting of dairy manure with rice chaff. Bioresour Technol 102:9040–9049

    Article  CAS  PubMed  Google Scholar 

  • Ministry of Light Industry of China (1993) General methods of determination for industrial enzymes (QB/T 1803-1993). China Light Industry Press, Beijing

    Google Scholar 

  • Morales ML, Tesfaye W, Garciaparrilla MC, Casas JA, Troncoso AM (2001) Sherry wine vinegar: physicochemical changes during the acetification process. J Sci Food Agric 81:611–619

    Article  CAS  Google Scholar 

  • Moreau MM, Eades SC, Reinemeyer CR, Fugaro MN, Onishi JC (2014) Illumina sequencing of the V4 hypervariable region 16S rRNA gene reveals extensive changes in bacterial communities in the cecum following carbohydrate oral infusion and development of early-stage acute laminitis in the horse. Vet Microbiol 168:436–441

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Ooijkaas L (2004) Chinese vinegar and its solid-state fermentation process. Food Rev Int 20:407–424

    Article  Google Scholar 

  • Peiffer JA, Spor A, Koren O et al (2013) Diversity and heritability of the maize rhizosphere microbiome under field conditions. Proc Natl Acad Sci USA 110:6548–6553

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peng Q, Yang Y, Guo Y, Han Y (2015) Analysis of bacterial diversity during acetic acid fermentation of Tianjin Duliu aged vinegar by 454 pyrosequencing. Curr Microbiol 71:195–203

    Article  CAS  PubMed  Google Scholar 

  • Sun W, Xiao H, Peng Q, Zhang Q, Li X, Han Y (2016) Analysis of bacterial diversity of Chinese Luzhou-flavor liquor brewed in different seasons by Illumina Miseq sequencing. Ann Microbiol 66:1293–1301

    Article  Google Scholar 

  • Tesfaye W, Morales ML, García-Parrilla MC, Troncoso AM (2002) Wine vinegar: technology, authenticity and quality evaluation. Trends Food Sci Technol 13:12–21

    Article  CAS  Google Scholar 

  • Thomas L, Larroche C, Pandey A (2013) Current developments in solid-state fermentation. Biochem Eng J 81:146–161

    Article  CAS  Google Scholar 

  • Trcek J, Mahnic A, Rupnik M (2016) Diversity of the microbiota involved in wine and organic apple cider submerged vinegar production as revealed by DHPLC analysis and next-generation sequencing. Int J Food Microbiol 223:57–62

    Article  CAS  PubMed  Google Scholar 

  • Unden G, Zaunmüller T (2009) Metabolism of sugars and organic acids by lactic acid bacteria from wine and must. In: König H, Unden G, Fröhlich J (eds)Biology of microorganisms on grapes, in must and in wine. Springer, Berlin, pp 135–147

  • Visintin S, Alessandria V, Valente A, Dolci P, Cocolin L (2016) Molecular identification and physiological characterization of yeasts, lactic acid bacteria and acetic acid bacteria isolated from heap and box cocoa bean fermentations in West Africa. Int J Food Microbiol 216:69–78

    Article  CAS  PubMed  Google Scholar 

  • Wang Z, Lu Z, Yu Y, Li G, Shi J, Xu Z (2015) Batch-to-batch uniformity of bacterial community succession and flavor formation in the fermentation of Zhenjiang aromatic vinegar. Food Microbiol 50:64–69

    Article  CAS  PubMed  Google Scholar 

  • Wang Z, Lu Z, Shi J, Xu Z (2016) Exploring flavour-producing core microbiota in multispecies solid-state fermentation of traditional Chinese vinegar. Sci Rep 6:26818

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang X, Ban S, Hu B, Qiu S, Zhou H (2017) Bacterial diversity of Moutai-flavour Daqu based on high-throughput sequencing method. J Inst Brew 123:138–143

    Article  CAS  Google Scholar 

  • Williams RT, Crawford RL (1983) Effects of various physiochemical factors on microbial activity in pea. Can J Microbiol 29:1430–1437

    Article  Google Scholar 

  • Wu J, Ma Y, Zhang F, Chen F (2012) Biodiversity of yeasts, lactic acid bacteria and acetic acid bacteria in the fermentation of “Shanxi aged vinegar”, a traditional Chinese vinegar. Food Microbiol 30:289–297

    Article  CAS  PubMed  Google Scholar 

  • Wu L, Lu Z, Zhang X, Wang Z, Yu Y, Shi J, Xu Z (2016) Metagenomics reveals flavour metabolic network of cereal vinegar microbiota. Food Microbiol 62:23–31

    Article  PubMed  Google Scholar 

  • Xu W, Xu Q, Chen J, Lu Z (2011a) Ligustrazine formation in Zhenjiang aromatic vinegar: changes during fermentation and storing process. J Sci Food Agric 91:1612–1617

    Article  CAS  PubMed  Google Scholar 

  • Xu W, Huang Z, Zhang X et al (2011b) Monitoring the microbial community during solid-state acetic acid fermentation of Zhenjiang aromatic vinegar. Food Microbiol 28:1175–1181

    Article  CAS  PubMed  Google Scholar 

  • Yang K, Yue Q, Kong J, Zhao P, Gao Y, Fu K, Gao B (2016) Microbial diversity in combined UAF-UBAF system with novel sludge and coal cinder ceramic fillers for tetracycline wastewater treatment. Chem Eng J 285:319–330

    Article  CAS  Google Scholar 

  • Zheng X, Yan Z, Nout MJR et al (2014) Microbiota dynamics related to environmental conditions during the fermentative production of Fen-Daqu, a Chinese industrial fermentation starter. Int J Food Microbiol 182-183:57–62

    Article  CAS  PubMed  Google Scholar 

  • Zhong F, Wu J, Dai Y, Yang L, Zhang Z, Cheng S, Zhang Q (2015) Bacterial community analysis by PCR-DGGE and 454-pyrosequencing of horizontal subsurface flow constructed wetlands with front aeration. Appl Microbiol Biotechnol 99:1499–1512

    Article  CAS  PubMed  Google Scholar 

  • Zhu W, Nie Y, Xu Y (2017) The incidence and distribution of ochratoxin a in Daqu, a Chinese traditional fermentation starter. Food Control 78:222–229

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This project was supported by the National Natural Foundation of China (No. 31271924).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Lixin Luo or Weifeng Lin.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Electronic supplementary material

ESM 1

(DOCX 2569 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gan, X., Tang, H., Ye, D. et al. Diversity and dynamics stability of bacterial community in traditional solid-state fermentation of Qishan vinegar. Ann Microbiol 67, 703–713 (2017). https://doi.org/10.1007/s13213-017-1299-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13213-017-1299-6

Keywords

Navigation