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Dynamics and Diversity of a Microbial Community During the Fermentation of Industrialized Qingcai Paocai, a Traditional Chinese

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Dynamics and Diversity of a Microbial Community During the Fermentation of Industrialized Qingcai Paocai, a Traditional Chinese Annals of Microbiology (2018) 68:111–122 https://doi.org/10.1007/s13213-017-1321-z ORIGINAL ARTICLE Dynamics and diversity of a microbial community during the fermentation of industrialized Qingcai paocai, a traditional Chinese fermented vegetable food, as assessed by Illumina MiSeq sequencing, DGGE and qPCR assay Huipeng Liang1,2 & Liguo Yin3 & Yahao Zhang2 & Cong Chang2 & Wenxue Zhang2 Received: 4 July 2017 /Accepted: 20 December 2017 /Published online: 6 January 2018 # Springer-Verlag GmbH Germany, part of Springer Nature and the University of Milan 2018 Abstract Paocai is a traditional Chinese fermented food and typically produced via spontaneous fermentation. We have investigated the microbial community utilized for the fermentation of industrialized Qingcai paocai using the combination of Illumina MiSeq sequencing, PCR-mediated denaturing gradient gel electrophoresis (PCR-DGGE) and quantitative PCR (qPCR) assay. Three main phyla, namely Firmicutes, Proteobacteria and Bacteroidetes, were identified by both MiSeq sequencing and PCR-DGGE. The dominant genera observed in the fermentation were Lactobacillus, Pseudomonas, Vibrio and Halomonas.Mostgenera affiliated with Proteobacteria or Bacteroidetes were detected more often during the earlier part of the fermentation, while Lactobacillus (affiliated with Firmicutes) was dominant during the later fermentation stages. Fungal community analysis re- vealed that Debaryomyces, Pichia and Kazachstania were the main fungal genera present in industrialized Qingcai paocai, with Debaryomyces being the most dominant during the fermentation process. The quantities of dominant genera Lactobacillus and Debaryomyces were monitored using qPCR and shown to be 109–1012 and 106–1010 copies/mL, respectively. During the later fermentation process of industrialized Qingcai paocai, Lactobacillus and Debaryomyces were present at 1011 and 108 copies/mL, respectively. These results facilitate further understanding of the unique microbial ecosystem during the fermentation of indus- trialized Qingcai paocai and guide future improvement of the fermentation process. Keywords Qingcai paocai . Illumina MiSeq sequencing . PCR-DGGE . qPCR . Fermentation Introduction materials (Yan et al. 2008). It is mildly salted, and paocai brine contains lactic acid. Paocai is one of the typical representatives Paocai is a traditional Chinese fermented vegetable that is of traditional fermented foods in China (especially in Sichuan commonly produced by the spontaneous fermentation of raw province) and is commonly served as a side dish or as an appetizer. In recent years, paocai has been recognized as a Electronic supplementary material The online version of this article functional food with several health benefits (Yan et al. (https://doi.org/10.1007/s13213-017-1321-z) contains supplementary 2008). Generally, industrialized paocai is made from only a material, which is available to authorized users. single type of vegetable without the addition of seasonings, while homemade paocai is made from a variety of vegetables * Wenxue Zhang (e.g. cabbage, radish, cucumber and cowpea) with the addition [email protected] of seasonings (e.g. red pepper, garlic, ginger). Industrialized paocai is produced by stacking fresh vegetables with salt and 1 National Engineering Research Center of Seafood, School of Food Science and Technology, Dalian Polytechnic University, then allowing natural fermentation at ambient temperature for Dalian 116034, People’sRepublicofChina at least 3 months. The quality of industrialized paocai is un- 2 College of Light Industry, Textile and Food Engineering, Sichuan stable and not uniform due to the many factors that influence University, Chengdu 610065, People’s Republic of China the fermentation process, such as the type and quality of the 3 College of Life Science and Food Engineering, Yibin University, raw vegetables, salt concentration and production season. The Yibin 644007, People’s Republic of China spontaneous fermentation of vegetables is mainly affected by 112 Ann Microbiol (2018) 68:111–122 the presence of microorganisms at different stages of the fer- mentation process and is highly dependent on the lactic acid bacteria (LAB) that occur naturally in the raw materials (Tanganuratetal.2009;Liuetal.2011), including Lactobacillus, Pediococcus, Leuconostoc, Weissella, Enterococcus and Lactococcus. To improve both the production technology and the quality of industrialized paocai, it is necessary to explore the structure of the microbial community during the fermentation process of industrialized paocai. The conventional culture method is often time-consuming and intensive, but numerous powerful molecular ecological methods have recently been developed and widely used to analyze the microbial community in the field of food more efficiently and rapidly (Hong et al. 2014; Luo et al. 2014; Iwobi et al. 2015). These methods have over- come the shortcomings of conventional culture methods. PCR-mediated denaturing gradient gel electrophoresis (PCR-DGGE) is a classical molecular ecological technique that has been widely applied to directly reveal and rapidly monitor the microbial community during the fermentation Fig. 1 Schematic flow diagram of the production process of Chinese process (Nie et al. 2013, 2015;Liangetal.2016a). industrialized paocai However, these methods also have many limitations for the monitoring of microbial communities because they produce 2015, industrialized Qingcai paocai samples in different fer- limited amounts of information. With the advent of next- mentation stages were collected from a local Chinese paocai generation sequencing technology, a thorough investigation factory (Sichuan Liji Paocai Condiment Co., Ltd., Meishan, of the complete microfloral community during the fermenta- China), which is located in Sichuan province, China. Four tion process became possible. Illumina MiSeq sequencing has samples for each fermentation time were collected from dif- been used to analyze the diversity of the microbial community ferent locations in the fermentation pit, and each set of four in many foods (Jeong et al. 2013;Lietal.2016a). However, to samples were then thoroughly mixed for subsequent analysis. date, no relevant studies on the microbial diversity of indus- The pH values were measured in 50-mL samples of paocai trialized paocai have been performed. Quantitative PCR brine using a pH meter (PHS-3C; Shanghai Electronics (qPCR) has emerged as a specific and sensitive technique that Science Instrument Co., Ltd., Shanghai, China). To determine allows for the quantification of the target organism in different the total titratable acidity (TTA), we first diluted 25 mL of samples (Paul et al. 2015; Liang et al. 2016b). In the study paocai brine sample with cooled boiled water to a volume of reported here, qPCR was used as a complementary method to 250 mL, then titrated the diluted sample using 0.1 M NaOH to quantify dominant microorganisms during the fermentation of a final pH of 8.2. The TTAwas expressed as follows: C × (V1 - industrialized paocai. V0) × n × F × 1000/V, where C represents the concentration of The primary aim of this study was to characterize the mi- NaOH (in mol/L); V1 represents the volume of the 0.1 M crobial community during the fermentation of industrialized NaOH used for sample determination (in mL); V0 represents paocai using Illumina MiSeq sequencing, PCR-DGGE and the 0.1 M NaOH used for the blank control (boiled distilled qPCR techniques. The results provide a deeper understanding water) determination (in mL); n represents the dilution factor; of the microecosystem and lay a foundation for improvements F represents the factor appropriate for lactic acid (0.009); V in standard manufacturing systems and production processes represents the volume of the diluted sample (in mL). of industrialized paocai. DNA extraction and PCR-DGGE analysis of the microbial community Materials and methods Total DNA was extracted from 10 mL of homogenized paocai Sample collection and physico-chemical analysis brine sample using an E.Z.N.A.® DNA kit (Omega Bio-Tek Inc., Norcross, GA), according to the manufacturer’sproto- In this study the vegetable used to make industrialized paocai cols. The DNA preparations were stored at − 20 °C until was Qingcai (Brassica chinensis var. chinensis). A schematic further use. PCR cycling was performed in a MyCycler™ flow sheet of the production process is shown in Fig. 1.In Thermal cycler (Bio-Rad, Hercules, CA). The reaction Ann Microbiol (2018) 68:111–122 113 volume (50 μL) contained 2 × PCR Mix (TIANGEN Biotech, qPCR analysis of dominant microorganisms Beijing, China), 20 pmol primers, template DNA and distilled water. The 16S ribosome RNA (rRNA) and 18S rRNA gene Quantitative PCR was performed in a Lightcycler® Nano were amplified using primers reported in previous studies System (Roche, Basel, Switzerland) to quantify the dominant (Muyzer et al. 1993;Harutaetal.2006); these former primers microorganisms during the fermentation of industrialized contained a GC clamp at the 5′ end. Qingcai paocai. The primers F-lac (5′-GCA GCA GTA DGGE was performed in 8% polyacrylamide gels, with a GGG AAT CTT CCA-3′), R-lac (5′-GCA TTY CAC CGC linear gradient of 30–55% and 20–40% denaturant for both TAC ACA TG-3′), DerbaF1 (5′-CTT TCG CCC TGT GGT the bacterial and fungal community using the D-Code™ GTT TG-3′) and DerbaR1 (5′-GCG TCA AAA AAA GAA Universal Mutation Detection System (Bio-Rad). The electro- CAA CAC C-3′) were used to amplify the 16S rRNA
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