Article pubs.acs.org/JAFC
Insights into the Biogenic Amine Metabolic Landscape during Industrial Semidry Chinese Rice Wine Fermentation Xiaole Xia,*,† Qingwen Zhang,† Bin Zhang,‡ Wuji Zhang,† and Wu Wang† †
The Key Laboratory of Industrial Biotechnology, Ministry of Education, School of Biotechnology, Jiangnan University, Wuxi, Jiangsu 214122, P.R. China ‡ Nantong Baipu Chinese Rice Wine Co., Ltd., Nantong, Jiangsu 226500, P.R. China
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S Supporting Information *
ABSTRACT: Inspired by concerns about food safety, the metabolic landscape of biogenic amines (BAs) was elucidated during industrial semidry Chinese rice wine fermentation. The main fermentation process represented the largest contribution to BA formation, which corresponded to 69.1% (54.3 mg/L). Principal component analysis revealed that total acid and ethanol were strongly correlated with BAs, indicating that BA formation favored acidic and stressful conditions. Other than putrescine (PUT), spermidine (SPD), and spermine (SPM), 5 BAs exhibited strong relationships with the precursor amino acids (R2 > 0.85). PUT was mainly decarboxylated from arginine (89.6%) whereas SPD (100%) and SPM (83.1%) were obtained from ornithine. Interestingly, some SPD could convert back to PUT (24.3%). All 8 BAs showed good relationships with lactic acid bacteria (LAB) (R2 around 0.75). Moreover, among the five main LAB genera, Lactobacillus had a positive correlation with BA formation. KEYWORDS: biogenic amines, semidry Chinese rice wine, industrial fermentation, principal component analysis, Lactobacillus, decarboxylation
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fermentation proceed in parallel rather than sequentially.11 Similar to that found in other types of rice wine, the indigenous bacteria, together with the abundant precursor amino acids available during fermentation, have raised concerns about the accumulation of BAs in Chinese rice wine.12 Lu et al. analyzed 14 Chinese rice wines from four wine-making regions of China and detected HIS in all samples, followed by spermine (SPM), CAD, TYR, and spermidine (SPD). The mean level of BAs was 107 mg/L and ranged from 39.3 to 241 mg/L.13 Zhong et al. analyzed 39 samples from different manufacturers and showed that the most prominent BA was serotonin, followed by PUT, TYR, CAD, and HIS. The total BA contents varied, ranging from 29.3 to 260 mg/L, whereas that of semidry Chinese rice wine is 102 mg/L on average.14 This value is higher than those of wine, beer, and Turkish cereal wine and lower than that of Korean rice wine.15,16 Some studies have quantified the levels of BAs during the production of Chinese rice wines.17 Zhang et al. found that the BA content in the seed starter varied over a large range (16.43− 87.72 mg/L). Moreover, in the first two days, the BA content increased sharply and then more gradually, and the content reached a maximum value on day six.18 Compared to wine, few studies have addressed the BA metabolic landscape during fermentation, particularly its interactions with metabolites and microorganisms.19 It has been commonly accepted that BAs are mainly decarboxylated by a decarboxylase derived from lactic acid bacteria (LAB), particularly Lactobacillus.20 However, in a correlation analysis of bacteria community succession and the
INTRODUCTION Biogenic amines (BAs) are present in varying concentrations in food and are mainly formed by amino acid decarboxylation.1 It is commonly accepted that high concentrations of BAs represent a health hazard because of their undesirable physiological effects, particularly when alcohol is present.2 At elevated levels (100 mg/L), these compounds, mainly cadaverine (CAD) and putrescine (PUT), also exert an impact on the organoleptic properties of fermented foods.3 The European Union (EU) has established regulations for histamine (HIS) levels, and many wine importers in the EU require a BA analysis.4 Currently, public health and the technological and economic significance of BAs support the hypothesis that their contents should become a wine quality index.5 Additionally, the presence of BAs in food may serve as an indicator of undesired microbial activity and for the evaluation of good manufacturing practices (GMP).6 In wine, HIS and tyramine (TYR) are considered the most toxic products and are particularly relevant for food safety; PUT and CAD are known to potentiate these effects. Moreover, these amines cannot be inactivated by the thermal treatments used in food processing and preparation.7 Various studies have shown that BA formation in wines is related to the grape variety, type of vinification, wine pH, malolactic fermentation, aging, and their interactions.8 Chinese rice wine (CRW) is a traditional fermented alcoholic beverage that is rich in amino acids (AA), oligosaccharides, and microelements.9 Commonly, Chinese rice wines are classified into four types based on their total sugar levels; some differences also exist in their production techniques.10 Semidry Chinese rice wine is a kind of CRW in which sugar content is between 15.1 to 40.0 g/L. Wheat Qu, Chinese koji, steamed rice, and water are mixed to initiate a so-called parallel fermentation, during which starch saccharification and alcoholic © 2016 American Chemical Society
Received: Revised: Accepted: Published: 7385
April 25, 2016 September 6, 2016 September 13, 2016 September 13, 2016 DOI: 10.1021/acs.jafc.6b01523 J. Agric. Food Chem. 2016, 64, 7385−7393
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Journal of Agricultural and Food Chemistry
with the same volume of steamed rice, 200% water, and 5% wheat Qu, which has an amylase activity higher than 500U/g, and then entered the so-called main fermentation process, which typically consisted of incubation at 28−30 °C for 6−7 days with intermittent oxygen filling. Subsequently, postfermentation occurred at room temperature for approximately 10 days. After fermentation, the fermentation mash was filtered by pressing, clarification, and sterilization. Eleven samples were taken from each batch, as summarized in Scheme 1. Triplicate samples were collected, filtered, and stored at 4 °C. The method of Zhang et al.18 was used for the preparation of liquid samples and the derivatization of all of the extracted solutions. BA Determination. A 5 mL aliquot of each sample was vortexed with 15 mL of 0.1 M hydrochloric acid to obtain a homogeneous mixture. After centrifugation (6000g, 10 min, 4 °C), the aqueous layer was collected, diluted to 25 mL with 0.1 M hydrochloric acid, and stored under refrigeration. For analysis, 2 mL of the extract was added to 0.2 mL of 1,7-diaminoheptane (100 mg/L in 0.1 M hydrochloric acid) as an internal standard, and then the mixture was subjected to derivatization with dansyl chloride and determination by reversedphase HPLC (RP-HPLC) with ultraviolet (UV) detection as described previously.25 Detection of Microorganisms and Metabolites. To count the LAB, the samples were serially diluted 10-fold with distilled water, and 100 μL of each dilution was spread on a 1% (w/v) deMan−Rogosa− Sharpe agar (MRS agar, Oxoid, U.K.) plate. The agar plates were incubated at 37 °C for 20 h under aerobic conditions. Yeast and mold were cultured on 3 M yeast and mold count plates (3 M, MN, United States) in a 20 °C incubator for 68 h under aerobic conditions. The numbers of viable LAB and yeast were determined by calculating the colony forming units (cfu)/mL. The total sugar, acid, alcohol, and amino acid contents of the fermentation mash were measured according to the National Standard of the People’s Republic of China for Chinese rice wine.26 Analysis of LAB Using 16S rDNA. Ten milliliters of the fermentation broth were centrifuged at 17000g for 6 min at 4 °C to collect the microbial cells. The resulting pellet was used to extract the total DNA with the Promega Wizard Genomic DNA Purification Kit according to the manufacturer’s instructions. Polymerase chain reaction (PCR) was used to amplify the 16S rDNA V3−V4 region using the universal primers 341F (5′-CCTACGGGNGGCWGCAG3′) and 805R (5′-GACTACHVGGGTATCTAA TCC-3′).27 The amplified PCR products were sequenced with Illumina MiSeq to generate millions of reads by Personalbio (Shanghai Personal Biotechnology Co., Shanghai, China). The operational taxonomical units (OTUs), which were defined according to a 3% distance level, were phylogenetically classified, and a taxonomy file describing the complete taxonomic information on each sequence in the RDP database from domain to genus was created. Statistical Analysis. Three batches of each Chinese rice wine (obtained by three separate fermentation trials) were analyzed in triplicate. Pearson’s correlation test and t test were conducted using Origins 7.5 (OriginLab, MA, United States). For univariate statistics, analysis of variance (ANOVA) was performed using SPSS statistical software version 12.0 (SPSS Inc., Chicago, IL, United STates). When ANOVA revealed P < 0.01, the data were further analyzed using Duncan’s test for multiple comparisons. For multivariate analysis, principal component analysis (PCA) was carried out to identify any possible patterns and outliers between samples.28
changes in the BA levels during Chinese rice wine fermentation, Liu et al. found that Lactobacillus might not be the main BA producer.21 Currently, few reliable methods that can be used to detect limiting BA formation in fermented alcoholic beverages exist. Guo et al. reported that the knockout of some specific genes in Saccharomyces cerevisiae decreased BA formation by ́ 25.5%.22 Garcia-Ruiz demonstrated that some LAB isolated from fermented foods can degrade BAs by producing amine oxidase enzymes.23 Callejón identified a multicopper oxidase from LAB that can degrade amines in wine.24 Hence, the risk mitigation options, which are based on analyzing and controlling those factors and interactions, should be systematically considered and ranked in Chinese rice wine fermentation. The objective of this work, which represents a preliminary part of a wider research project aimed at the control of BA formation in Chinese rice wine, is to identify the BA metabolic landscape during industrial semidry Chinese rice wine fermentation. In particular, the interactions and relationships between BAs, metabolites, and microorganisms are investigated and analyzed. On the basis of these results, potential protocols for limiting and reducing BAs and enhancing the quality of Chinese rice wine are discussed.
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MATERIALS AND METHODS
Materials and Standards. BA standards (2-phenylamine (PHE), PUT, CAD, HIS, TYR, tryptamine (TRY), SPD, and SPM) were purchased from Sigma-Aldrich (United States). Acetonitrile, acetone, and dansyl chloride for high-performance liquid chromatography (HPLC) were purchased from Merck (Germany), and ultrapure water was obtained from a Milli-Q system (Millipore, United States). Other reagents used in this study were analytical grade and purchased from local companies. Rice, Chinese koji, and wheat Qu were prepared by Nantong Baipu Chinese Rice Wine Co., Ltd. (China). Production and Sampling of Semidry Chinese Rice Wine. The industrial fermentation of Chinese rice wine was performed at Baipu Chinese Rice Wine (Nantong, China). As shown in Scheme 1,
Scheme 1. Fermentation and Sampling Processes of Semidry Chinese Rice Winea
a
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RESULTS BA Analysis during Industrial Fermentation. To date, few studies have analyzed the BAs formed during fermentation, and no studies on the BA metabolic landscape on the industrial scale have been reported. It has been commonly accepted that BAs are mainly produced in the steeping and canning periods. No biogenic amines were detected in rice, Chinese koji, or wheat Qu in accordance with previous work.18
The numbers in the scheme are the sampling points.
rice was processed by washing and water steeping at 25−30 °C for 2 days, and then the steeped rice was steamed, which was considered the beginning of fermentation. The seed starter is unique to Chinese rice wine fermentation; its preparation involves mixing steamed rice and 0.5−1% (w/w) Chinese koji, which has an amylase activity higher than 100U/g and is cultured at approximately 25 °C for 48 h. This process is known as canning and saccharification. The seed starter was mixed 7386
DOI: 10.1021/acs.jafc.6b01523 J. Agric. Food Chem. 2016, 64, 7385−7393
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decrease to less than 0.3 mg/L·d, and the concentrations of all 8 BAs exhibited only small increases after day 7. Among the 8 BAs, the highest formation ratio was exhibited by PUT, followed by TYR and HIS, which displayed similar concentrations. Figure 2B shows that PUT was the most abundant BA at the end of fermentation (35.8 mg/L and 45.54%). This finding differs from that in wine, in which TYR and HIS are the most toxic BAs. Here, the concentrations of these species were 25.0 and 6.14 mg/L, and the final proportions were 31.84 and 7.82%, respectively. Among the 8 BAs, the highest formation ratio was exhibited by PUT, followed by TYR and HIS, which displayed similar concentrations. Changes in Microorganisms and Metabolites and Their Correlations with BAs. The above result revealed that the BA concentrations exhibited the same trend as the LAB and ethanol, similar to the results reported in other studies.29 However, the exact correlation between BA formation and other metabolites and microorganisms remained unknown. Shen et al. reported a PCA of these factors during the aging of Chinese rice wine, and separation was found to be common, similar to the result of their previous study.30 Figure 3 shows the PCA performed on 8 variables (ethanol, total acid, total amino acids, pH, LAB, BA, yeast, and mold), which were significantly different in 11 samples from different fermentations. All of the data were autoscaled to prevent variables with high intensities from being considered more important than those with low intensities before PCA. The first two PCs accounted for 88.2% of the total variance in the raw data (PC1 69.7% and PC2 18.5%). The separation between samples of various fermentation statuses was quite satisfactory. Overall, the pattern recognition revealed that PC1 clearly classified the 11 samples into two groups: canning and fermentation. However, PC2 accounted for minor separation and classified samples into four groups: steeping, canning, main fermentation, and postfermentation; these groups perfectly match the brewing status. Pereira et al. reported factors governing BA formation, including the presence of an amino acid decarboxylase, the amount of free amino acid substrates, and appropriate reaction conditions.31 As shown in Figure 3, total acid and ethanol had good, positive relationships with BA formation, which was similar to total amino acids and LAB. These findings confirmed that amino acid decarboxylation
A different result was found in our work. As shown in Figure 1, unlike previous reports, BA formation was mainly detected in
Figure 1. Changes in the microorganism, alcohol, and BA levels during fermentation.
two periods, canning and the beginning of the main fermentation period. A level of 38.1 mg/L was generated in the first 1.5 days, and 45.7 mg/L was generated on day 5. The main fermentation stage had the largest contribution to total BA formation: 69.1% (54.3 mg/L); only 7.4 mg/L was produced during postfermentation. The final BA concentration was 78.5 mg/L, lower than the previously reported value of 102 mg/L. This difference may have occurred because we discarded the seriflux, which is not part of the traditional method.17 The trend of the changes in the total BA levels over time was similar to those of the LAB and ethanol levels but different from those of mold and yeast. The mold and yeast grew rapidly in the first 3 and 6 days and then decreased sharply to 104 cfu/mL. According to Xie et al., the changes in microorganism composition lead to different functions at different fermentation time points.29 Figure 2A shows that the fluctuation trends of the formation ratio of BAs during fermentation in 8 BAs are similar. The highest BA formation ratio was 11.4 mg/L·d on day 5, and the next highest was 6.3 mg/L·d in the first 1.5 days, which give the major contribution. The formation ratios were −5.7 and −1.2 mg/L·d on days 3 and 4 when 200% water and then 100% steamed rice were added to the vat. The ratios of BA formation
Figure 2. (A) Changes in the formation ratio of BAs during fermentation. (B) Proportion of BAs at the end of fermentation. 7387
DOI: 10.1021/acs.jafc.6b01523 J. Agric. Food Chem. 2016, 64, 7385−7393
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conditions and that the amino acids and LAB are direct contributors. Therefore, BA formation during industrial Chinese rice wine fermentation may be related to metabolic activity, which was directly related to the decarboxylase activity. Hence, its relationships with amino acids and LAB were further investigated in detail. Correlation between BAs and Amino Acids. Chinese rice wine contains seven different essential amino acids, and the total amino acid concentration is much higher than that of other liquors, which is considered advantageous.13 BAs are mainly produced via the decarboxylation of amino acids; each BA has one specific precursor amino acid, except for PUT, SPM, and SPD, which have two precursors: arginine (ARG) and ornithine (ORN).34 Figure 5 shows that the levels of all BAs are strongly correlated with those of their precursor amino acids throughout the fermentation process. All R2 values were approximately 0.85, except for those relating SPD to ARG and ORN, which were 0.70 and 0.72, respectively. Additionally, the initial concentrations of the PUT, TYR, and HIS were high, similar to the result described above. This finding confirmed that the formation of all eight BAs mainly resulted from the decarboxylation of their precursor amino acids during fermentation. Multivariate linear stepwise regression was used to investigate the relationships of SPD, SPM, and PUT with their precursors, as shown in Table 1. On the basis of these results, we determined the metabolic networks for PUT, SPD, and SPM with ORN and ARG, as shown in Figure 6. PUT is mainly formed via two principal pathways: (i) direct decarboxylation of ORN and (ii) decarboxylation from ARG via agmatine. The first is usually more efficient because it is a one-step reaction.35 During industrial Chinese rice wine fermentation, both pathways appeared to have similar decarboxylation efficiencies, and the coefficients relating PUT to ORN and ARG were 0.05 and 0.07, respectively. Regarding the relationships of PUT with SPD and SPM, SPD was approximately twofold higher than SPM during
Figure 3. PCA of the BA, microorganism, and metabolite concentrations during the main fermentation process.
favors acidic and other stressful media, resulting in increased pH and membrane energization.32 Figure 4 shows that the R2 values of all four factors exceeded 0.80, which is rather good. The coefficients were different, with the lowest obtained for ethanol and the highest for the total amino acids: 0.0006 and 0.022, respectively. As shown in Figures 4C and D, the initial BA concentration was rather high (around 20 mg/L), suggesting that formation initiates at the very beginning of the process. This finding is opposite to that in wine, in which BAs are produced at concentrations of less than 4 mg/L before malolactic fermentation.33 This result confirmed that the decarboxylate reaction favors acidic and stressful
Figure 4. Correlations between the total BAs and the following variables: (A) total acid, (B) ethanol, (C) LAB, and (D) total amino acids. 7388
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Figure 5. Correlation between BAs and amino acids.
Table 1. Equations of SPD, SPM, and PUT with Their Precursors number 1
BA with their precursors
2
SPD, SPM, and PUT with ORN and ARG PUT with ORN and ARG
3
SPM with ORN and ARG
4
SPD with ORN and ARG
equation
R2
y = 8.20 + 0.05X1 + 0.07X2 y = 8.22 + 0.028X1 + 0.073X2 y = 0.003 + 0.005X1 + 0.0002X2 y = −0.022 + 0.017X1 − 0.001X2
0.83 0.81 0.98 0.97
Figure 6. Metabolic network of PUT, SPD, and SPM with ORN and ARG.
the fermentation process. The coefficient relating SPD to ARG was −0.001, indicating that it could convert back to PUT. In 7389
DOI: 10.1021/acs.jafc.6b01523 J. Agric. Food Chem. 2016, 64, 7385−7393
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correspond to approximately 30 and 5%, respectively. As shown in Figure 7B, PCA was performed on the 5 LAB genera and BAs, which differed significantly in the 11 samples from different fermentation statuses. The first two PCs accounted for 80.8% of the total variance in the raw data (PC1 45.4% and PC2 35.4%). The separation between samples of various fermentation statuses was quite satisfactory. Overall, the pattern recognition revealed that PC1 and PC2 clearly classified the 11 samples into three groups: beginning, high metabolic activity, and low metabolic activity; these match the BA metabolic status. Furthermore, only Lactobacillus were found to have a positive relationship with the BAs, in which the R value of 0.15 is consistent with previous reports. Within microbial groups, in many cases the capacity to produce biogenic amines is a strainspecific characteristic. Then, to assess the incidence of specific bacteria with BA-producing potential, high-throughput DNA sequencing of the metagenome should be employed, as in other fermented foods.
conclusion, PUT was mainly decarboxylated from ARG (89.6%), whereas SPD (>100%) and SPM (83.1%) were decarboxylated from ORN, and the ARG levels were 3.40-fold higher than those of ORN. Interestingly, some SPD could convert back to PUT (24.3%). It may because some polyamine oxidases are involved in the spermidine degradation.36 Unlike wine, lower amounts of SPD were produced in many samples compared with those in the control, whereas SPM was drastically increased in most of the samples compared with the amount in the control.37 Correlation between the BAs and LAB. Table 2 shows that the concentrations of all 8 BAs exhibited good correlations Table 2. Correlation between the BAs and Lactic Acid Bacteria BA 2-phenylamine putrescine cadaverine histamine tyramine tryptamine spermidine spermine
equation y y y y y y y y
= = = = = = = =
0.50x + 0.54 4.01x + 7.08 0.48x + 0.59 0.642x + 1.04 2.53x + 6.49 0.11x + 0.12 0.11x + 0.09 0.065x + 0.047
R2 0.85 0.77 0.78 0.74 0.74 0.63 0.61 0.70
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DISCUSSION Concern regarding food safety has raised interest in analyzing BAs in Chinese rice wine in recent years. BA concentration of Chinese rice wine is approximately two times that of wine, which may be because CRW has a high level of amino acids and LAB, in accordance with previous reports.13 Although many related studies have been published, the relationship between the vinification conditions and BA formation in wine is not well understood.21 Here, the whole landscape of BA metabolism during industrial Chinese rice wine fermentation was determined. Unlike previous reports, the main fermentation process was found to be the major contributor to BA formation, possibly because the steeping water was discarded, which is used in the traditional brewing process. Moreover, the proportion of seed starter was 50% of the final volume, providing enough leavening power for fermentation. In addition, the detailed description about the relation between BA formation and various variables was analyzed. The formation of all eight BAs was found to be strongly related to amino acids and LAB, which favored acidic and other stressful conditions. Specifically, the metabolic network relating PUT, SPM, and SPD with their precursors ARG and ORN was established. Interestingly, PUT is mainly produced from ARG,
with the LAB throughout the fermentation process. Most of the R2 values were approximately 0.75, lower than those for amino acids; PHE was the highest with an R2 value of 0.85, whereas the lowest was SPD with an R2 value of 0.61. The initial concentrations of PUT, TYR, and HIS were high with concentrations of 5.23, 6.84, and 0.93 mg/L, but those of the other BAs were low. This difference could be explained by the observation that the LAB had different capacities for producing different amines, and this capacity was associated with the specific fermentation status. Additionally, other bacteria can produce BAs at the beginning of the process. As shown in Figure 7A, analyzing the LAB in detail revealed that Streptococcus, Lactococcus, Lactobacillus, Leuconostoc, and Pediococcus are the five main genera present during Chinese rice wine fermentation. Except at the beginning, Streptococcus is the most abundant LAB and represents approximately 60% of the LAB, followed by Lactococcus and Lactobacillus, which
Figure 7. (A) Changes of the main LAB during fermentation. (B) PCA of the BA concentration and main LAB throughout the fermentation process. Labels: str, Streptococcus; lat, Lactococcus; lac, Lactobacillus; leu, Leuconostoc; ped, Pediococcus. 7390
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Figure 8. (A) Correlations between the formation ratio of BAs with amino acids and LAB during fermentation. (B) Changes in the formation ratios of microorganisms, alcohol, and BAs during the main fermentation process.
the mainstays of current research. The absence of decarboxylase activity should be a criterion for the selection of strains intended for fermentation to obtain a BA-free product. Further, we can use some exist BA degradation strains, especially Lactobacillus casei, which can degrade BAs in wine and cheese fermentation.43 For industrial Chinese rice wine fermentation, high-quality raw materials and optimal technological conditions also are crucial factors to ensure proper performance and reduced BA accumulation. Discarding the seriflux and focusing on the main fermentation, which is the major step in BA formation, may be good strategies, particularly for control of the metabolic activity of LAB via an optimized brewing method. The proteolytic capacities of the strains to be used in these fermentations should also be studied, particularly to control the formation of toxic BA precursors.
whereas SPD and SPM are produced from ORN, and SPD can convert back to PUT. This may be related to their function because the production of polyamines such as PUT could interfere with physiological functions in bacteria such as osmotic stress, oxidative stress responses, and bacterial crosstalk.38 Although we confirmed that the LAB and amino acids are direct contributors to BA formation, the detailed mechanism by which BAs are formed remains unclear. The European Food Safety Authority (EFSA) Panel on Biological Hazards (BIOHAZ) (2011) concluded that the accumulation of BAs in fermented foods is a complex process that is affected by multiple factors and their interactions, the combinations of which are numerous, variable, and product-specific.39 As shown in Figures 8A and B, although the concentration of amino acids and lactic acid is high, interestingly, the formation ratio decreases after the main fermentation, indicating that the amino acid decarboxylase activity also decreases after day seven. As shown in Figure 8B, the trend of the BA formation ratio is similar to those of the acid, ethanol, LAB, and amino acids. This finding is similar to that of Pessione et al., who showed that amino acid decarboxylation could occur in wine when the bacterial population is in the exponential growth stage under stressful conditions.40 The exact relationships with environmental factors, specific LAB species, and decarboxylase activity were investigated. O’Sullivan reported the dominant species with TYR- and HISproducing potential using high-throughput DNA sequencing.41 PCR primers and DNA probes were designed to detect HIS decarboxylase in wine, which determines HIS synthesis. Additionally, some studies have demonstrated that acidic and stressful conditions induce decarboxylase expression.42 In Chinese rice wine, the initial concentration of BAs is approximately 15 mg/L, and the concentrations of both metabolites and microorganisms are rather low. These results suggest that studies should be performed in a standard system using selected strains to eliminate variables from the natural system and obtain a better understanding of BA formation. The described works above are ongoing in our lab and will published soon. It is important to identify mechanisms to reduce the final BA content, especially the toxic BAs, in Chinese rice wine. Selection and addition strains, which free or reduce BAs, are
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ASSOCIATED CONTENT
S Supporting Information *
The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.jafc.6b01523. Changes in the levels of each BA during fermentation (Figure S1) and correlation between the BAs and lactic acid (Figure S2) (PDF)
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AUTHOR INFORMATION
Corresponding Author
*E-mail:
[email protected], Phone: 008651085326829. Funding
This work was supported by grants from the Key research and development program of Jiangsu Province (BE 2016331), the National Natural Science Foundation of China (31301540), and the Priority Academic Program Development of Jiangsu Higher Education Institutions. Notes
The authors declare no competing financial interest.
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ACKNOWLEDGMENTS We thank Xinhua Jin and Meifang Xia from Nantong Baipu Chinese Rice Wine Co., Ltd., for their assistance with the industrial fermentation. 7391
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DOI: 10.1021/acs.jafc.6b01523 J. Agric. Food Chem. 2016, 64, 7385−7393
