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Article

Changes in the Phytochemical and Bioactive Compounds and the Antioxidant Properties of Wolfberry during Vinegar Fermentation Processes

by
Ting Xia
,
Xiao Qiang
,
Beibei Geng
,
Xiaodong Zhang
,
Yiming Wang
,
Shaopeng Li
,
Yuan Meng
,
Yu Zheng
* and
Min Wang
*
State Key Laboratory of Food Nutrition and Safety, Key Laboratory of Industrial Fermentation Microbiology, College of Biotechnology, Tianjin University of Science and Technology, Tianjin 300457, China
*
Authors to whom correspondence should be addressed.
Int. J. Mol. Sci. 2022, 23(24), 15839; https://doi.org/10.3390/ijms232415839
Submission received: 28 November 2022 / Revised: 6 December 2022 / Accepted: 8 December 2022 / Published: 13 December 2022
(This article belongs to the Special Issue Bioactive Phytochemicals and Functional Food Ingredients in Fruits and Vegetables 2022)
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Abstract

:
Wolfberry (Lycium barbarum L.), as a kind of functional fruit, has various nutritional and bioactive components, which exhibit healthy benefits. However, wolfberry is not easy to preserve, and the intensive processing of wolfberry needs to be developed. In the present study, the changes in the phytochemical and bioactive compounds, as well as the antioxidant properties of wolfberry, were evaluated in the brewed processes. We found that the sugar contents were significantly decreased, and the total acids values were significantly increased during the fermentation processes. The sugar and fat contents were low in the wolfberry fruit vinegar after fermentation, which is of benefit to human health. In addition, amino acids were examined during the fermentation processes, and histidine, proline, and alanine were found to be the main amino acids in vinegar. The total phenolics and flavonoids contents were significantly increased by 29.4% and 65.7% after fermentation. 4-Hydroxy benzoic acid, 3-hydroxy cinnamic acid, and chlorogenic acid were the primary polyphenols in the wolfberry fruit vinegar. Moreover, the antioxidant activity of wolfberry fruit vinegar was significantly increased compared with that of wolfberry fruit after the fermentation processes. Polysaccharides and polyphenolics were strongly correlated with the antioxidant activity during the fermentation processes. The findings suggest that wolfberry fruit vinegar has a high antioxidant capability, and could be a beneficial food in the human diet.

1. Introduction

Lycium barbarum L. is known as wolfberry (goji berry), which belongs to the Solanaceae family. It has been used as a functional food and traditional Chinese medicine for thousands of years [1]. The wolfberry fruit planted in Zhongning is of a high quality, and is the only wolfberry cultivar that has been recorded in the Pharmacopoeia of the People’s Republic of China [2]. It has been reported that wolfberry has abundant nutrients and functional components, including polysaccharides, polyphenol, flavonoids, and amino acids [1,3]. The beneficial effects of wolfberry include antioxidation, hypoglycemic, and hypolipidemic properties, as well as anti-aging and the improvement of immunity [4].
Most of wolfberry fruits are produced into dried berries after harvest because the large yield of fruit is difficult to preserve [5]. The dried berries brown easily after exposure to air [6]. In order to maintain a better appearance quality and taste, deep processing of wolfberry fruits is necessary. Earlier studies have displayed that the processing products of wolfberry fruits are primarily wolfberry juice and wine, as well as being added into other food products, such as candies, cookies, and milk [7,8]. Brewed vinegar is an alternative strategy to promote the transformation of wolfberry, which needs further development.
Vinegar is used as a condiment worldwide, and is a type of functional food that is of benefit to the human body [9]. It is rich in nutrients and biological substances, including sugars, polyphenolic compounds, amino acids, organic acids, and melanoidins [10]. Many studies have reported that vinegar can prevent various diseases, such as diabetes, hypertension, infection, and inflammation [11]. The compositions and functions of vinegar are tightly related to the original materials and the fermentation processes [12]. Fruit vinegar is brewed through two steps, namely alcohol and acetic acid fermentation. In the alcohol fermentation process, yeast uses sugar to produce alcohol, and then the produced alcohol is used by acetic acid bacteria to produce acetic acid in the acetic acid fermentation process [13]. Fruit vinegar such as balsamic vinegar and sherry vinegar is mainly produced in European countries [14,15]. The raw materials of fruit vinegar are derived from grapes, apples, persimmons, and coconuts, among others [13,16]. However, the functional compounds during fermentation processes in fruit vinegar produced by wolfberry are still unclear.
In this study, fresh wolfberry was used as a raw material to ferment wolfberry fruit vinegar. The physicochemical parameters were determined during the fermentation processes. Meanwhile, nutritional and functional components were examined during the fermentation processes. Furthermore, the relationship between the antioxidant activity and functional components was revealed. The findings will provide an opportunity to make a functional fermentation food with raised economic added value.

2. Results and Discussion

2.1. Physicochemical Parameters of Wolfberry Fruit Vinegar during Fermentation

The changes in the physicochemical parameters during the fermentation processes are shown in Table 1. The pH values were not significantly altered between wolfberry fruit wine (WFW) and wolfberry fruit juice (WFJ) (p > 0.05). However, the pH value in wolfberry fruit vinegar (WFV) was 3.38 ± 0.08, which was significantly decreased compared with that in WFW (p < 0.05). Proper acidity can improve the taste and flavor of fruit vinegar [17]. In this study, there were no significant differences in the total acids between WFJ and WFW (p > 0.05). Nevertheless, the total acids value in WFV was 6.72 ± 0.12 g/100 mL, which was significantly increased compared with that in WFW (p < 0.05). It has been reported that acetic acid and other acids are produced during the acetic acid fermentation process [7]. Therefore, the increase in total acid value in WFV was caused by these acids.
In addition, the main non-volatile acids in fruit vinegars were lactic acid, citric acid, succinic acid, and malic acid, which modulated the irritation of acetic acid and provided a good dietary source of antioxidants [10,16]. In this study, the non-volatile acid contents were gradually increased during the fermentation process, which made the WFV taste softer. It is well-known that soluble solids are an important index to evaluate food quality [18]. The soluble solid content was significantly decreased to 8.42 ± 0.26 g/100 mL in WFW and 8.66 ± 0.28 g/100 mL in WFV, which was mainly due to the conversion from sugar into ethanol by active dry wine yeast [19]. The content of reducing sugar in WFJ sharply decreased from 12.08 ± 0.32 g/100 mL to 1.31 ± 0.11 g/100 mL in WFW, and then slightly increased to 1.42 ± 0.14 g/100 mL in WFV. This was mainly due to the reducing sugar used by the yeast during alcohol fermentation [20].

2.2. Nutritional Components of Wolfberry Fruit Vinegar during Fermentation

As shown in Table 2, the sugar content was decreased during alcohol fermentation. There was no significant difference between the WFW and WFV (p > 0.05). The decrease in sugar content during alcohol fermentation was related to the fact that sugar is decomposed by yeast and converted into ethanol [21]. The fat content values were very low in the fermentation stages, which were not significantly changed during the fermentation processes (p > 0.05). Low-sugar and low-fat diets are of benefit to human health [22]. These data reveal that the contents of sugar and fat were low in WFV.
Meanwhile, 15 amino acids were measured in WFJ (Table 3). The highest amount of amino acid in the WFJ sample was proline, followed by serine and histidine. Proline was also the predominant amino acid in WFW, followed by histidine. In WFV, the top two amino acids were histidine and proline. In general, histidine was significantly increased, while proline and alanine were significantly decreased during the fermentation processes (p < 0.05). Previous research has shown that proline was the amino acid in the greatest amount in Balsamic Vinegar of Modena (BVM), followed by alanine and threonine [23]. Another study reported that there were 16 amino acids in pear vinegars, and glutamic acid was the most dominant, followed by alanine and aspartic acid [24]. Amino acids in vinegar are mostly taken from raw materials and proteins are produced by microbial breakdown [25]. Therefore, the main amino acids in WFV were different from the fruit vinegars in other studies, which was may due to different raw materials and fermentation conditions [26].

2.3. Bioactive Components of Wolfberry Fruit Vinegar during Fermentation

As shown in Table 4, polysaccharide was the predominant bioactive component in WFJ. Wolfberry polysaccharide is a glycoconjugate, which has various biological functions, such as enhancing immunity, antioxidation, anti-inflammation, lowering blood glucose properties [3]. The polysaccharide content was significantly decreased to 7.26 ± 0.26 mg/mL in WFW, and then significantly rose to 8.94 ± 0.27 mg/mL in WFV (p < 0.05). Additionally, the betaine contents (2.68–2.94 mg/mL) showed no significant difference during the fermentation processes (p > 0.05), and betaine can adjust the taste and flavor of fruit vinegars [27]. The carotenoid content decreased from 0.58 ± 0.08 mg/mL to 0.42 ± 0.02 mg/mL along throughout the entire fermentation processes, which was mainly due to the oxidation reaction and degradation in the fermentation stages [28].
Moreover, the total phenolics content (TPC) and total flavonoids content (TFC) were the significant compounds in foods and plants, which have the capacity for free radical scavenging [29]. TPC was not significantly changed in WFW (p > 0.05), and was significantly increased to 2.42 ± 0.05 mg GAE/mL in WFV (p < 0.05). The increase in TPC during acetic fermentation was mainly attributed to combined polyphenols with sugars and organic acids to release free polyphenols [30]. TFC was enhanced to 1.63 ± 0.01 mg RE/mL in WFW (p < 0.05). There was no discernible difference in TFC contents between WFW and WFV (p > 0.05). Yang et al. reported that the TPC and TFC were 0.20 mg GAE/mL and 0.08 mg RE/mL in jujube juice, respectively. TPC and TFC were significantly increased to 0.28 mg GAE/mL and 0.09 mg RE/mL in jujube vinegar, respectively [31]. Wang et al. reported that the TPC was 0.53 mg GAE/mL during alcohol fermentation, and increased to 0.67 mg GAE/mL during acetic fermentation (p < 0.05). TFC was increased from 0.11 mg RE/mL to 0.13 mg RE/mL during the process of fermentation (p < 0.05) [16]. These results in previous studies indicated that TPC and TFC were increased during the fermentation processes, which were in line with our data.

2.4. Polyphenolic Compounds of Wolfberry Fruit Vinegar during Fermentation

Eighteen polyphenolic compounds were detected during the fermentation processes (Table 5). The top three polyphenolic compounds in WFJ were 4-hydroxy cinnamic acid, phloroglucinol, and 3-hydroxy cinnamic acid. Meanwhile, 4-hydroxyphenethyl alcohol was the predominant polyphenolic component in WFW, followed by phloroglucinol and 3-hydroxy cinnamic acid. In addition, 4-hydroxy benzoic acid was the highest polyphenolic in WFV, followed by 3-hydroxy cinnamic acid and chlorogenic acid. Moreover, the 4-hydroxyphenethyl alcohol content was increased first during alcohol fermentation (p < 0.05), and then decreased slightly during acetic acid fermentation (p > 0.05). Chlorogenic acid and 3-(4-hydroxy-3-methoxyphenyl) propionic acid gradually increased along throughout the entire fermentation (p < 0.05). Previous studies have shown that gallic acid, chlorogenic acid, and caffeic acid are the main polyphenolic compounds in the juice, wine, and vinegar of hawthorn [32]. Another study reported that tyrosol, protocatechuic acid, and gallic acid were the main polyphenolic compounds during the pomegranate vinegar fermentation processes [33]. Fruit raw materials are the primary source of polyphenolic components in fruit vinegar, and different fruit vinegars have different polyphenolic compounds [34]. In this study, the polyphenolic compounds in wolfberry vinegar were different from those in other fruit vinegars, mainly due to the different raw materials and production processes [10].
Furthermore, the polyphenolic compounds of WFJ, WFW, and WFV were characterized by PCA (Figure 1). The results showed that two PCs explained 97.1% of the variability (eigenvalues > 1), and the contribution rates of PC1 and PC2 were 59.7% and 37.4%, respectively. The polyphenolic compounds in the WFV sample were mainly found to be the positive for PC1, while those in the WFJ and WFW samples were found to be negative for PC1. In addition, the polyphenolic compounds in WFJ and WFV had positive values for PC2, while those in WFW were negative for PC2. PCA can be used to analyze and distinguish the different samples in the different fermentation stages, which had different distributions on the analysis graph [35]. The polyphenolic compounds in different samples during the fermentation process could be separated well, indicating the differentiated antioxidant characteristics.

2.5. Antioxidant Activities of Wolfberry Fruit Vinegar during Fermentation

As shown in Table 6, the antioxidant activity in WFW was lower than that in WFJ. This might be as a result of the massive reproduction of yeast, which lead to the loss of antioxidant components during alcohol fermentation [36]. Then, the antioxidant activity was significantly enhanced in WFV compared with that in WFW. It has been reported that the antioxidant activity of papaya vinegar was increased with the accumulation of acetic acid during the progress of fermentation [37]. Moreover, the values of the antioxidant activity in WFV were 27.87 ± 0.37 mM Trolox/L for 1,1-diphenyl-2-picrylhydrazyl (DPPH), 21.92 ± 0.28 mM Trolox/L for 2,2′-azinobis (3-ethlybenzothiazoline)-6-sulfonic acid (ABTS), and 8.76 ± 0.23 mM Trolox/L for the ferric ion reducing antioxidant power (FRAP), respectively, which were the highest in the fermentation processes. Özdemir et al. reported that the antioxidant activities were decreased in alcohol fermentation, and then raised during acetic acid fermentation by DPPH and FRAP [4]. Its antioxidant trend was similar to that in our study.
On the other hand, the correlation analysis between the functional ingredients and antioxidant activities is shown in Figure 2. The correlation coefficients between the contents of wolfberry polysaccharide and the antioxidant activities of DPPH and FRAP were 0.90, TPC and the antioxidant activities of DPPH were 0.94 in the fermentation process of WFV. These results indicate that wolfberry polysaccharides and total phenols exhibit a very strong correlation with the antioxidant activities. Several studies reported that the wolfberry polysaccharides and phenolic compounds showed antioxidant characteristics through scavenging the free radicals [29]. Collectively, polysaccharide and TPC were the main bioactive components, which contributed to the antioxidant activity in the fermentation processes.

3. Materials and Methods

3.1. Raw Materials and Chemicals

Wolfberry fruits were acquired from the Ningxia Zhongning Goji Industry Innovation Research Institute (Ningxia, China) in 2020. Active dry wine yeast was provided by Angel Yeast Co., Ltd. (Beijing, China). A. pasteurianus AC2005 was sourced from the Bioengineering College of Tianjin University of Science and Technology. DPPH, Folin–Ciocalteu reagent, rutin, and gallic acid standards were purchased from Sinopharm Chemical Reagent Co., Ltd. (Shanghai, China). The ABTS and FRAP assay kits were provided by the Beyotime Institute of Biotechnology (Shanghai, China).

3.2. Production of Wolfberry Fruit Vinegar

The fresh wolfberry fruits were washed and crushed into a homogenate using a pulping machine (Zhejiang Jinda Electric Machinery Co., Ltd., Zhejiang, China), and mixed with sterile drinking water (1:4, w/v). After filtering through a multi-layer filter cloth, 0.005% vitamin C and 1% citric acid were added to the filtrate to exert antioxidant activities. In the alcoholic fermentation process, the inoculation of the aforementioned activated yeast was 0.20% (106 log CFU/mL) in the juice, and WFJ (1L) was fermented at 22 °C for 6 days in the incubator with a facultative anaerobic condition. The fermentation was terminated when there were no bubbles in the fermentation broth, and the obtained supernatant was WFW (about 850 mL). During the acetic acid fermentation process, A. pasteurianus were inoculated to acetic acid bacteria medium and cultured at 30 °C for 24 h to obtain acetic acid bacteria seed liquid. The WFW was inoculated with the acetic acid bacteria activated liquid of 10% (106–107 log CFU/mL) in the wine, and was fermented under aerobic conditions in a shaker at 180 r/min and 30 °C for 5 days, and the fermentation was stopped when the acetic acid content was stabilized (Figure 3). The obtained WFV was about 830 mL. To reduce the batch-to-batch variation of WFV, three batches of wolfberry fruits were collected in the same year.

3.3. Determination of the Physicochemical and Nutritional Components

The total acids, non-volatile acid, and reducing sugar were measured by acid–base titration, single boiling distillation units, and direct titration, in accordance with the Chinese National Standard methodology, respectively. A handheld refractometer was used to detect the content of the soluble solids. The sugar contents were determined using the phenol sulfuric acid method. In accordance with GB 5009.5-2016, the protein and fat were determined through the Kjeldahl method and Soxhlet extraction methodology, respectively.

3.4. Determination of the Amino Acids

The amino acids of the samples were determined using an amino acid automatic analyzer (S-433D; SYKAM, Munich, Germany). The analyzer functioned using a LCAK06/Na (4.6 mm × 150 mm) column. The mobile phase was an hydrochloric acid buffer with a 0.45 mL/min flow rate. The column oven temperature and the capacity of the injection were 30–70 °C and 50 μL, respectively. The ninhydrin reagents derivatized amino acids at 130 °C for 60 min, and were detected at 570 nm and 440 nm, respectively. The results were presented in milligrams per liter (mg/L) of samples.

3.5. Determination of the Functional Components

3.5.1. Determination of the TPC

TPC was measured by the Folin–Ciocalteu technique [38]. Briefly, diluted samples were combined with Folin–Ciocalteu reagent (1:4, v/v). After being incubated for 5 min, 10% Na2CO3 and distilled water (1:5, v/v) were added to the samples in 96-well plates. The combination was kept in the dark for 2 h. The absorbance was determined at 765 nm using a microplate reader, and the data were presented in mg gallic acid equivalent per mL (mg GAE/mL).

3.5.2. Determination of the TFC

TFC was measured using the colorimetric assay technique. Briefly, the diluted sample and 5% NaNO2 (2:1, v/v) were combined and maintained for 6 min in dark. Then, 20% NaOH and 5% Al(NO3)3 (4:1, v/v) were added and maintained for 6 min. Finally, the combined solution was placed in a 96-well plate and maintained for 15 min. The absorbance was detected at 510 nm using a microplate reader, and the data were presented in mg rutin equivalents per mL (mg RE/mL).

3.5.3. Determination of the Polysaccharide

The polysaccharide content was determined using the phenol-sulfuric acid technique method. The samples were added into 5% phenol solution and concentrated sulfuric acid (1:5, v/v) at 40 °C water bath. After incubating for 10 min, the mixture, the blank of distilled water, and standard solution of glucose were placed in a 96-well plate. The absorbance was measured at 490 nm using a microplate reader.

3.5.4. Determination of the Betaine

The betaine content in the samples was determined through a betaine assay kit. Briefly, the sample and 80% methanol (1:5, v/v) were combined, and then centrifuged at 10,000 rpm for 15 min. The mixture was maintained in a water bath at 60 °C for 30 min, and the supernatant was placed in a 70 °C water bath. Then, the betaine extract was diluted and measured using a microplate reader at 525 nm.

3.5.5. Determination of the Carotenoids

The samples were mixed with solvents (n-hexane:acetone:toluene:ethanol = 10:7:7:6) and 40% KOH methanol solution (1:100:5, v/v/v). The mixture was placed in a 35 °C water bath for 12 h dark, and then extracted using diethyl ether. The extraction was added to deionized water and the underlying liquid was discarded following three uses. Finally, the extraction was passed through anhydrous sodium sulfate and diluted with diethyl ether. The absorbance was measured at 450 nm.

3.6. Determination of the Polyphenolic Compounds

The samples were centrifuged at 7104× g for 15 min, and the supernatant was ultrafiltered through a 10 kDa ultrafiltration cup (Shanghai Xuanyi Environmental Protection Technology Co., Ltd., Shanghai, China). The filtrate was purified using AB-8 microporous resin. Deionized water was used to remove impurities, and was eluted with 90% ethanol. Finally, the extract solution was evaporated and concentrated.
The polyphenolic compounds in the samples were detected through GC-MS with a Rtx-5MS column (30 m × 0.25 mm i.d., 0.25 μm). The flow rate of the purity helium was 1 mL/min, and the injector temperature was 300 °C. The oven temperature conditions were held at 80 °C for 2 min, and increased to 315 °C (5 °C/min) and maintained for 11 min. The temperature of the interface and ion source were 220 °C and 200 °C, respectively. The mass-to-charge ratio was 35–1000 m/z.

3.7. Antioxidant Activity Analyses

In the DPPH assay, the samples were diluted 30-fold with PBS. The diluted samples (20 μL) were mixed in 96-well plates with DPPH solution (180 μL). After 30 min at room temperature (in the dark), the samples were measured by microplate readers to read the absorbance at 517 nm and the results were represented as the trolox equivalent antioxidant capacity (TEAC).
In the ABTS assay, the samples were diluted 30-fold with PBS. The diluted samples (10 μL) and ABTS+ radical cation solution (200 μL) were combined in 96-well plates and incubated for 6 min (at room temperature). The samples were determined using a microplate reader to detect the absorbance at 734 nm, and the results were represented as TEAC.
In the FRAP assay, the samples were diluted 20-fold with PBS. The diluted samples (5 μL) and FRAP solution (180 μL), which were constituted by an acetate buffer (300 mM), FeCl3 (20 mM), and tripyridyltriazine (10 mM), and were placed in 96-well plates and incubated at 37 °C for 3–5 min (in the dark). The samples were detected using a microplate reader to measure the absorbance at 593 nm, and the results were represented as TEAC.

3.8. Statistical Analysis

The data were given as mean ± standard deviation (S.D., n = 3). Statistical analysis was performed using the GraphPad Prism 8.0.1 software (GraphPad Software Inc., San Diego, CA, USA), and SPSS 24.0 for Windows (SPSS Inc., Chicago, IL, USA). The Pearson’s correlation test was applied to the related correlation analyses. p < 0.05 suggested a significant difference.

4. Conclusions

In the study, it was found that goji berry fruit vinegar as a nutritious and functional product has a high antioxidant activity that could increase the economic added value. The changes in nutritional and bioactive compounds and the antioxidant activity of WFJ, WFW, and WFV were determined during the fermentation processes. Firstly, the phytochemical compounds were determined during the fermentation processes. The pH values were decreased and the total acids values were increased. Additionally, the sugar and fat contents were at low levels after fermentation. Histidine, proline, and alanine were the top three amino acids in WFV. TPC and TFC were significantly increased in the entire fermentation process. 4-Hydroxy benzoic acid, 3-hydroxy cinnamic acid, and chlorogenic acid were the important polyphenols compounds in WFV. Finally, the antioxidant activity of WFV was significantly enhanced after the fermentation processes. The anti-active ingredients of polysaccharide and TPC had a very strong correlation with the antioxidant activity in the fermentation process.

Author Contributions

Conceptualization, T.X. and X.Q.; formal analysis, B.G.; software, X.Z. and Y.W.; investigation, S.L. and Y.M.; resources, Y.Z.; supervision, T.X. and M.W.; validation, M.W.; writing—original draft, T.X. and X.Q.; writing—review and editing, T.X. and X.Q. All authors have read and agreed to the published version of the manuscript.

Funding

This study was financially supported by the Key Research and Development Program of Ningxia, grant number 2022BBF02010, the General project of Ningxia Zhongning wolfberry Industry Innovation Research Institute, grant number ZNGQCX-B-2019001, and the Innovation fund of Haihe Laboratory of Synthetic Biology, the Tianjin Science and Technology Commission, grant number 21ZYJDJC00030.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The authors confirm that the data supporting the findings of this study are available within the article.

Acknowledgments

We thank the Ningxia Zhongning Goji Industry Innovation Research Institute (Ningxia, China) and for supplying the samples, and Ningxia University professor Sijun Yue for the scientific advice.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Yao, R.; Heinrich, M.; Weckerle, C.S. The genus Lycium as food and medicine: A botanical, ethnobotanical and historical review. J. Ethnopharmacol. 2018, 212, 50–66. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  2. Cheng, J.; Zhou, Z.W.; Sheng, H.P.; He, L.J.; Fan, X.W.; He, Z.X.; Sun, T.; Zhang, X.; Zhao, R.J.; Gu, L.; et al. An evidence-based update on the pharmacological activities and possible molecular targets of Lycium barbarum polysaccharides. Drug Des. Dev. Ther. 2014, 9, 33–78. [Google Scholar]
  3. Liu, W.; Xu, J.; Zhu, R.; Zhu, Y.; Zhao, Y.; Chen, P.; Pan, C.; Yao, W.; Gao, X. Fingerprinting profile of polysaccharides from Lycium barbarum using multiplex approaches and chemometrics. Int. J. Biol. Macromol. 2015, 78, 230–237. [Google Scholar] [CrossRef] [PubMed]
  4. Özdemir, N.; Pashazadeh, H.; Zannou, O.; Koca, L. Phytochemical content, and antioxidant activity, and volatile compounds associated with the aromatic property, of the vinegar produced from rosehip fruit (Rosa canina L.). LWT—Food Sci. Technol. 2021, 154, 112716. [Google Scholar] [CrossRef]
  5. Yuan, G.; Ren, J.; Ouyang, X.; Wang, L.; Wang, M.; Shen, X.; Zhang, B.; Zhu, B. Effect of raw material, pressing and glycosidase on the volatile compound composition of wine made from goji berries. Molecules 2016, 21, 1324. [Google Scholar] [CrossRef] [Green Version]
  6. Zhao, Q.S.; Dong, B.T.; Chen, J.J.; Zhao, B.; Wang, X.D.; Wang, L.W.; Zha, S.H.; Wang, Y.C.; Zhang, J.H.; Wang, Y.L. Effect of drying methods on physicochemical properties and antioxidant activities of wolfberry (Lycium barbarum) polysaccharide. Carbohyd. Polym. 2015, 127, 176–181. [Google Scholar] [CrossRef]
  7. Gao, Q.; Song, Y.; Liang, Y.; Li, Y.; Chang, Y.; Ma, R.; Cao, X.; Wang, S. Dynamics of physicochemical properties, functional compounds and antioxidant capacity during spontaneous fermentation of Lycium ruthenicum murr. (Qinghai-Tibet Plateau) natural vinegar. Foods 2022, 11, 1344. [Google Scholar] [CrossRef]
  8. Vidović, B.B.; Milinčić, D.D.; Marčetić, M.D.; Djuriš, J.D.; Ilić, T.D.; Kostić, A.Ž.; Pešić, M.B. Health benefits and applications of goji berries in functional food products development: A review. Antioxidants 2022, 11, 248. [Google Scholar] [CrossRef]
  9. Xia, T.; Zhang, B.; Duan, W.H.; Zhang, J.; Wang, M. Nutrients and bioactive components from vinegar: A fermented and functional food. J. Funct. Foods 2020, 64, 103681. [Google Scholar] [CrossRef]
  10. Liu, Q.; Tang, G.Y.; Zhao, C.N.; Gan, R.Y.; Li, H.B. Antioxidant activities, phenolic profiles, and organic Acid contents of fruit vinegars. Antioxidants 2019, 8, 78. [Google Scholar] [CrossRef] [Green Version]
  11. Xia, T.; Duan, W.; Zhang, Z.; Li, S.; Zhao, Y.; Geng, B.; Zheng, Y.; Yu, J.; Wang, M. Polyphenol-rich vinegar extract regulates intestinal microbiota and immunity and prevents alcohol-induced inflammation in mice. Food Res. Int. 2021, 140, 110064. [Google Scholar] [CrossRef] [PubMed]
  12. Cantadori, E.; Brugnoli, M.; Centola, M.; Uffredi, E.; Colonello, A.; Gullo, M. Date fruits as raw material for vinegar and non-alcoholic fermented beverages. Foods 2022, 11, 1972. [Google Scholar] [CrossRef] [PubMed]
  13. Luzón-Quintana, L.M.; Castro, R.; Durán-Guerrero, E. Biotechnological processes in fruit vinegar production. Foods 2021, 10, 945. [Google Scholar] [CrossRef]
  14. Giovanni, M. Balsamic vinegar of modena: From product to market value: Competitive strategy of a typical Italian product. Brit. Food J. 2004, 106, 722–745. [Google Scholar]
  15. Durán-Guerrero, E.; Castro, R.; García-Moreno, M.V.; Rodríguez-Dodero, M.D.C.; Schwarz, M.; Guillén-Sánchez, D. Aroma of sherry products: A review. Foods 2021, 10, 753. [Google Scholar] [CrossRef] [PubMed]
  16. Wang, D.H.; Wang, M.Y.; Cao, L.W.; Wang, X.T.; Sun, J.R.; Yuan, J.F.; Gu, S.B. Changes and correlation of microorganism and flavor substances during persimmon vinegar fermentation. Food Biosci. 2022, 46, 101565. [Google Scholar] [CrossRef]
  17. Xu, S.; Ma, Z.; Chen, Y.; Li, J.; Jiang, H.; Qu, T.; Zhang, W.; Li, C.; Liu, S. Characterization of the flavor and nutritional value of coconut water vinegar based on metabolomics. Food Chem. 2022, 369, 130872. [Google Scholar] [CrossRef]
  18. Burdon, J.; Pidakala, P.; Martin, P.; Billing, D.; Boldingh, H. Fruit maturation and the soluble solids harvest index for ‘Hayward’ kiwifruit. Sci. Hortic. 2016, 213, 193–198. [Google Scholar] [CrossRef]
  19. Crozier, A.; Borges, G. (Poly) phenolic constituents and the beneficial effects of moderate red wine consumption. J. Wine Res. 2011, 22, 131–134. [Google Scholar] [CrossRef]
  20. Akyüz, E.; Başkan, K.S.; Tütem, E.; Apak, R. High performance liquid chromatographic method with post-column detection for quantification of reducing sugars in foods. J. Chromatogr. A 2021, 1660, 462664. [Google Scholar] [CrossRef]
  21. Liu, S.; Laaksonen, O.; Kortesniemi, M.; Kalpio, M.; Yang, B. Chemical composition of bilberry wine fermented with non-Saccharomyces yeasts (Torulaspora delbrueckii and Schizosaccharomyces pombe) and Saccharomyces cerevisiae in pure, sequential and mixed fermentations. Food Chem. 2018, 266, 262–274. [Google Scholar] [CrossRef] [PubMed]
  22. DiNicolantonio, J.J.; Lucan, S.C.; O’Keefe, J.H. The evidence for saturated fat and for sugar related to coronary heart disease. Prog. Cardiovasc. Dis. 2016, 58, 464–472. [Google Scholar] [CrossRef] [PubMed]
  23. Chinnici, F.; Durán-Guerrero, E.; Riponi, C. Discrimination of some European vinegars with protected denomination of origin as a function of their amino acid and biogenic amine content. J. Sci. Food Agric. 2016, 96, 3762–3771. [Google Scholar] [CrossRef] [PubMed]
  24. Park, Y.O. Quality characteristics of fermented vinegars using pear. KJFP 2016, 23, 778–787. [Google Scholar] [CrossRef] [Green Version]
  25. Ferreira, I.M.; Guido, L.F. Impact of wort amino acids on beer flavour: A review. Fermentation 2018, 4, 23. [Google Scholar] [CrossRef] [Green Version]
  26. Carlavilla, D.; Moreno-Arribas, M.V.; Fanali, S.; Cifuentes, A. Chiral MEKC-LIF of amino acids in foods: Analysis of vinegars. Electrophoresis 2006, 27, 2551–2557. [Google Scholar] [CrossRef]
  27. Wang, X.; Wang, J.; Kamal, G.M.; Jiang, B.; Sun, P.; Zhang, X.; Liu, M. Characterization and comparison of commercial Chinese cereal and European grape vinegars using 1H-NMR spectroscopy combined with multivariate analysis. Chin. J. Chem. 2016, 34, 1183–1193. [Google Scholar] [CrossRef]
  28. Geng, J.Y.; Zhao, L.; Zhang, H.L. Formation mechanism of isoprene compounds degraded from carotenoids during fermentation of goji wine. Food Qual. Saf. 2021, 5, fyaa033. [Google Scholar] [CrossRef]
  29. Sun, Y.; Rukeya, J.; Tao, W.; Sun, P.; Ye, X. Bioactive compounds and antioxidant activity of wolfberry infusion. Sci. Rep. 2017, 7, 40605. [Google Scholar] [CrossRef] [Green Version]
  30. Dey, T.B.; Chakraborty, S.; Jain, K.K.; Sharma, A.; Kuhad, R.C. Antioxidant phenolics and their microbial production by submerged and solid state fermentation process: A review. Trends Food Sci. Technol. 2016, 53, 60–74. [Google Scholar]
  31. Yang, Y.Y.; Xu, M.D.; Wang, J.H. Change analysis of polyphenols and flavonoids in the process of jujube vinegar brewing. China Condiment. 2012, 37, 56–59. [Google Scholar]
  32. Özdemir, G.B.; Özdemir, N.; Ertekin-Filiz, B.; Gökırmaklı, Ç.; Kök-Taş, T.; Budak, N.H. Volatile aroma compounds and bioactive compounds of hawthorn vinegar produced from hawthorn fruit (Crataegus tanacetifolia (lam.) pers.). J. Food Biochem. 2022, 46, e13676. [Google Scholar] [CrossRef] [PubMed]
  33. Kharchoufi, S.; Gomez, J.; Lasanta, C.; Castro, R.; Sainz, F.; Hamdi, M. Benchmarking laboratory-scale pomegranate vinegar against commercial wine vinegars: Antioxidant activity and chemical composition. J. Sci. Food Agric. 2018, 98, 4749–4758. [Google Scholar] [CrossRef] [PubMed]
  34. Ho, C.W.; Lazim, A.M.; Fazry, S.; Zaki, U.K.H.H.; Lim, S.J. Varieties, production, composition and health benefits of vinegars: A review. Food Chem. 2017, 221, 1621–1630. [Google Scholar] [CrossRef] [PubMed]
  35. Gewers, F.L.; Ferreira, G.R.; De-Arruda, H.F.; Silva, F.N.; Comin, C.H.; Amancio, D.R.; Costa, L.F. Principal component analysis: A natural approach to data exploration. ACM Comput. Surv. 2018, 54, 9–22. [Google Scholar] [CrossRef]
  36. Morata, A.; Gómez-Cordovés, M.C.; Colomo, B.; Suárez, J.A. Pyruvic acid and acetaldehyde production by different strains of Saccharomyces cerevisiae: Relationship with vitisin A and B formation in red wines. J. Agric. Food Chem. 2003, 51, 7402–7409. [Google Scholar] [CrossRef]
  37. Ching, T.K.; Chin, W.H.; Ling, J.W.A.; Lazim, A.; Fazry, S.; Lim, S.J. Chemical changes and optimisation of acetous fermentation time and mother of vinegar concentration in the production of vinegar-like fermented papaya beverage. Sains Malays. 2018, 47, 2017–2026. [Google Scholar] [CrossRef]
  38. Singleton, V.L.; Orthofer, R.; Lamuela-Raventós, R.M. Analysis of total phenols and other oxidation substrates and antioxidants by means of folin-ciocalteu reagent. Methods Eezymol. 1999, 299, 152–178. [Google Scholar]
Ijms 23 15839 g001 550
Figure 1. Principal component analysis of the polyphenolic compounds in the fermentation processes.
Figure 1. Principal component analysis of the polyphenolic compounds in the fermentation processes.
Ijms 23 15839 g001
Ijms 23 15839 g002 550
Figure 2. Correlation analysis of bioactive ingredients and antioxidant activity during the fermentation processes: (a) polysaccharide, (b) betaine (c) total phenolics content, (d) total flavonoids content, and (e) carotenoids.
Figure 2. Correlation analysis of bioactive ingredients and antioxidant activity during the fermentation processes: (a) polysaccharide, (b) betaine (c) total phenolics content, (d) total flavonoids content, and (e) carotenoids.
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Ijms 23 15839 g003 550
Figure 3. Vinegar production processes of wolfberry fruit.
Figure 3. Vinegar production processes of wolfberry fruit.
Ijms 23 15839 g003
Table
Table 1. Contents of the physicochemical parameters in the fermentation processes of wolfberry fruit vinegar.
Table 1. Contents of the physicochemical parameters in the fermentation processes of wolfberry fruit vinegar.
ProductspH ValueTotal Acids (g/100 mL)Non-Volatile Acid
(g/100 mL)		Soluble Solids Content (g/100 mL)Reducing Sugar (g/100 mL)
WFJ4.48 ± 0.16 a0.56 ± 0.04 b0.42 ± 0.05 c16.26 ± 0.24 a12.08 ± 0.32 a
WFW4.20 ± 0.12 a0.60 ± 0.07 b0.56 ± 0.02 b8.42 ± 0.26 b1.31 ± 0.11 c
WFV3.38 ± 0.08 b6.72 ± 0.12 a0.84 ± 0.13 a8.66 ± 0.28 b1.42 ± 0.14 b
WFJ: wolfberry fruit juice, WFW: wolfberry fruit wine, WFV: wolfberry fruit vinegar. a, b, c: values in the same row with different lowercase letters present statistically significant differences (p < 0.05).
Table
Table 2. Contents of nutrients of wolfberry fruit vinegar in the fermentation processes.
Table 2. Contents of nutrients of wolfberry fruit vinegar in the fermentation processes.
ProductsSugar (g/100 mL)Protein (g/100 mL)Fat (g/100 mL)
WFJ15.63 ± 0.24 a0.49 ± 0.08 a0.10 ± 0.02 a
WFW1.98 ± 0.15 b0.38 ± 0.06 a0.09 ± 0.04 a
WFV2.46 ± 0.12 b0.46 ± 0.04 a0.12 ± 0.02 a
WFJ: wolfberry fruit juice, WFW: wolfberry fruit wine, WFV: wolfberry fruit vinegar. a, b: values in the same row with different lowercase letters present statistically significant differences (p < 0.05).
Table
Table 3. Types and contents of amino acids in wolfberry fruit vinegar in the fermentation processes.
Table 3. Types and contents of amino acids in wolfberry fruit vinegar in the fermentation processes.
CompoundAmino Acid Content (mg/L)
WFJWFWWFV
Proline722.10 ± 18.72 a552.36 ± 26.88 b439.51 ± 18.34 c
Serine505.62 ± 18.92 a40.28 ± 5.42 b38.60 ± 3.53 b
Histidine353.41 ± 5.78 c433.79 ± 5.25 b543.65 ± 4.38 a
Alanine312.36 ± 16.97 a79.15 ± 12.65 b75.62 ± 8.97 b
Aspartic acid135.14 ± 4.38 a12.46 ± 2.45 b11.74 ± 2.50 b
Arginine107.59 ± 27.80 a68.87 ± 3.33 a66.54 ± 4.51 a
Glutamic acid73.59 ± 8.58 a50.53 ± 8.48 b43.38 ± 0.41 b
Cysteine54.78 ± 3.38 a42.04 ± 3.13 b45.03 ± 1.40 b
Phenyllalanine46.31 ± 14.73 a51.08 ± 15.29 a50.33 ± 9.82 a
Lysine40.80 ± 7.10 a6.83 ± 1.43 b4.89 ± 1.12 b
Valine36.91 ± 0.59 a--
Leucine31.66 ± 2.81 c24.28 ± 0.36 b42.46 ± 1.75 a
Threonine29.50 ± 2.45 a21.85 ± 2.32 b25.41 ± 4.29 a b
Isoleucine8.70 ± 2.74 a-11.51 ± 0.58 a
Glycine5.31 ± 0.41 b18.16 ± 4.15 a10.47 ± 2.53 a b
WFJ: wolfberry fruit juice, WFW: wolfberry fruit wine, WFV: wolfberry fruit vinegar. a, b, c: values in the same row with different lowercase letters present statistically significant differences (p < 0.05). -: not detected.
Table
Table 4. Contents of nutrients of wolfberry fruit vinegar in the fermentation processes.
Table 4. Contents of nutrients of wolfberry fruit vinegar in the fermentation processes.
ProductsPolysaccharide
(mg/mL)		Betaine
(mg/mL)		Carotenoids
(mg/mL)		TPC
(mg GAE/mL)		TFC
(mg RE/mL)
WFJ8.58 ± 0.15 a2.94 ± 0.12 a0.58 ± 0.08 a1.87 ± 0.01 b1.02 ± 0.05 b
WFW7.26 ± 0.26 b2.68 ± 0.14 a0.46 ± 0.04 b1.88 ± 0.02 b1.63 ± 0.01 a
WFV8.94 ± 0.27 a2.88 ± 0.22 a0.42 ± 0.02 b2.42 ± 0.05 a1.69 ± 0.02 a
WFJ: wolfberry fruit juice, WFW: wolfberry fruit wine, WFV: wolfberry fruit vinegar. TPC: Total phenolic compounds. TFC: Total flavonoids compounds. a, b: values in the same row with different lowercase letters present statistically significant differences (p < 0.05).
Table
Table 5. Types and contents of polyphenols in wolfberry fruit vinegar in the fermentation processes.
Table 5. Types and contents of polyphenols in wolfberry fruit vinegar in the fermentation processes.
NoPolyphenolic CompoundsContents (mg/mL)
WFJWFWWFV
14-Hydroxy cinnamic acid0.408 ± 0.017 a0.116 ± 0.010 b0.131 ± 0.005 b
24-Hydroxyphenethyl alcohol0.004 ± 0.001 c0.337 ± 0.015 a0.216 ± 0.024 b
3Phloroglucinol0.349 ± 0.005 a0.329 ± 0.008 a0.105 ± 0.004 b
44-Hydroxy benzoic acid0.100 ± 0.005 b0.079 ± 0.008 b0.317 ± 0.011 a
53-Hydroxy cinnamic acid0.339 ± 0.008 a0.195 ± 0.012 b0.311 ± 0.011 a
6Chlorogenic acid0.026 ± 0.005 c0.096 ± 0.020 b0.222 ± 0.008 a
73-(4-Hydroxy-3-methoxyphenyl) propionic acid-0.159 ± 0.007 b0.222 ± 0.008 a
84-Hydroxy benzaldehyde0.005 ± 0.001 c0.015 ± 0.002 b0.022 ± 0.001 a
92-Hydroxybenzoic Acid0.098 ± 0.008 a0.044 ± 0.003 c0.059 ± 0.002 b
10Ferulic acid0.212 ± 0.001 a0.094 ± 0.004 c0.134 ± 0.005 b
113-(4-Hydroxymethyl) propionic acid0.141 ± 0.010 a b0.104 ± 0.009 b0.151 ± 0.005 a
12Caffeic acid0.063 ± 0.009 b0.077 ± 0.005 b0.143 ± 0.005 a
13vanillic acid0.042 ± 0.002 b0.051 ± 0.006 b0.097 ± 0.003 a
143-(4-Hydroxyphenyl)-2-hydroxypropionic acid0.034 ± 0.003 a0.018 ± 0.007 a0.038 ± 0.001 a
154-Hydroxyphenylacetic acid0.030 ± 0.002 a0.015 ± 0.002 b0.028 ± 0.001 a
163,4-Dihydroxyphenylpropionic acid0.014 ± 0.001 b0.014 ± 0.002 b0.027 ± 0.001 a
173-Hydroxy-4-methoxycinnamic acid0.006 ± 0.001 c0.037 ± 0.001 b0.062 ± 0.002 a
18Protocatechuic acid0.005 ± 0.001 b0.007 ± 0.001 b0.022 ± 0.001 a
WFJ: wolfberry fruit juice, WFW: wolfberry fruit wine, WFV: wolfberry fruit vinegar. Values in the same row with different superscripted alphabet are significantly different at p < 0.05. -: not detected.
Table
Table 6. Antioxidant activity of wolfberry fruit vinegar in the fermentation processes.
Table 6. Antioxidant activity of wolfberry fruit vinegar in the fermentation processes.
ProductsDPPH (mM Trolox/L)ABTS (mM Trolox/L)FRAP (mM Trolox/L)
WFJ25.71 ± 0.52 b20.59 ± 0.46 b8.26 ± 0.16 b
WFW24.84 ± 0.06 c19.57 ± 0.33 c7.82 ± 0.18 c
WFV27.87 ± 0.37 a21.92 ± 0.28 a8.76 ± 0.23 a
WFJ: wolfberry fruit juice, WFW: wolfberry fruit wine, WFV: wolfberry fruit vinegar. Values in the same row with different super-scripted alphabet are significantly different at p < 0.05.
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Xia, T.; Qiang, X.; Geng, B.; Zhang, X.; Wang, Y.; Li, S.; Meng, Y.; Zheng, Y.; Wang, M. Changes in the Phytochemical and Bioactive Compounds and the Antioxidant Properties of Wolfberry during Vinegar Fermentation Processes. Int. J. Mol. Sci. 2022, 23, 15839. https://doi.org/10.3390/ijms232415839

AMA Style

Xia T, Qiang X, Geng B, Zhang X, Wang Y, Li S, Meng Y, Zheng Y, Wang M. Changes in the Phytochemical and Bioactive Compounds and the Antioxidant Properties of Wolfberry during Vinegar Fermentation Processes. International Journal of Molecular Sciences. 2022; 23(24):15839. https://doi.org/10.3390/ijms232415839

Chicago/Turabian Style

Xia, Ting, Xiao Qiang, Beibei Geng, Xiaodong Zhang, Yiming Wang, Shaopeng Li, Yuan Meng, Yu Zheng, and Min Wang. 2022. "Changes in the Phytochemical and Bioactive Compounds and the Antioxidant Properties of Wolfberry during Vinegar Fermentation Processes" International Journal of Molecular Sciences 23, no. 24: 15839. https://doi.org/10.3390/ijms232415839

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