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. 2018 Mar 30;55(6):2240–2250. doi: 10.1007/s13197-018-3141-y

Comparison of physicochemical indexes, amino acids, phenolic compounds and volatile compounds in bog bilberry juice fermented by Lactobacillus plantarum under different pH conditions

Ming Wei 1, Shaoyang Wang 1,2, Pan Gu 1, Xiaoyu Ouyang 1, Shuxun Liu 1, Yiqing Li 1, Bolin Zhang 1, Baoqing Zhu 1,✉
PMCID: PMC5976609  PMID: 29892124

Abstract

This study aimed to investigate the effect of Lactobacillus plantarum strains on quality improvement of bog bilberry juice. Bog bilberry juice with different pH conditions was fermented by Lactobacillus B7 or C8-1 strain. Physicochemical index, amino acids, phenolic compounds, and volatiles of these fermented juices were compared. Results indicated that Lactobacillus plantarum strains preferred to metabolize malic acid and reducing sugar in non-pH-adjusted juice (NJ, pH 2.65), whereas quinic and citric acids were largely consumed in pH-adjusted juice (AJ, pH 3.50). Shikimic acid and aromatic amino acids were significantly accumulated in pH-adjusted juice, and phenolic compounds in both juices were significantly reduced. These strains enhanced the composition and concentration of volatiles compounds in non-pH-adjusted juice and improved the floral and fruity flavors. However, concentration and complexity of volatiles were reduced in pH-adjusted juices.

Keywords: Bog bilberry juice, Lactic acid fermentation, Lactobacillus plantarum, Phenolic compounds, Volatile compounds

Introduction

Vaccinium uliginosum L, also known as bog bilberry, is a low-bush wild shrub distributed in cool regions of the northern hemisphere. Bog bilberry fruit contains numerous antioxidant compounds, such as phenolic compounds (Wang et al. 2014). It has been confirmed that consumption of bog bilberry fruits can decrease the risks of cardiovascular diseases, cancer, tumor, mutagenic activity, and diabetes (Pascual-Teresa et al. 2013). Compared to other berry fruits, high acids-to-sugar ratio in bog bilberry negatively affects their consumption as fresh fruits (Liu et al. 2015). Lactic acid fermented fruits and vegetables have gained much attention in the food industry since fermented fruits and vegetables could improve their sensory features. It has been reported that lactic acid fermentation has been applied to tomatoes, capers, pineapple, peppers, cabbages, carrots, and French beans with different lactic acid bacteria, such as Lactobacillus, Leuconostoc, Weissella, Enterococcus, and Pediococcus spp. (Di Cagno et al. 2013). However, no study has been carried out in bog bilberry juice.

Lactic acid fermentation of fruits can convert glucose and other hexoses into lactate. Meanwhile, the energy released during the conversion could help the growth of bacteria in fruits (Fugelsang and Edwards 2006). More importantly, the nutrition alterations during lactic acid fermentation can result in a significant improvement on the sensory attributes of fermented food products. For instance, organic acids play an important role in the sour taste of fruits (Mikulic-Petkovsek et al. 2012), while malic acid possesses a harsh mouthfeel. Lactic acid fermentation can convert malic acid into lactic acid, significantly reducing the harshness of fruits (Boulton et al. 1999). Moreover, some organic acids can be further metabolized into aromatic compounds during fermentation (Gonzalez-Bello 2016). These aromatic compounds can play important roles in enhancing the fermented aroma of fermented food products (Helinck et al. 2004).

Lactobacillus plantarum is an acid-tolerant bacterium that widely exists in fermented plant foods. It has been widely applied in the fermentation industry due to its beneficial properties to fermented food products (Di Cagno et al. 2015). For example, lactic acid fermented food products exhibit a low level of lactose, which can benefit the consumption of consumers with the lactose intolerance (Di Cagno et al. 2013). L. plantarum has also been confirmed to be a good candidate for the development of probiotics. It can effectively reduce the allergenicity of food products and further improve the intestinal permeability compared to other microbes (Gobbetti et al. 2010).

Most of the previous studies have indicated that pH condition and lactic acid bacterial were the key factors that affect the performance of fruit lactic acid fermentation (Filannino et al. 2015, 2014; Mousavi et al. 2013). Compared to other fruits, bog bilberry fruits have high levels of organic acids with a low pH value (Colak et al. 2016). This could inhibit the growth of lactic acid bacteria during fermentation (Fugelsang and Edwards 2006). This could weaken the fermentation efficacy, which limits the sensory improvement of bog bilberry juice after fermentation. Different lactic acid bacterial strains have different adaptability, which could significantly alter the metabolic pathways of nutrients during lactic acid fermentation process (Di Cagno et al. 2015). This study aimed to investigate the effect of pH conditions and bacterial strains on the composition alteration of bog bilberry juice. The findings from this study could provide technical supports on the improvement of bog bilberry juice production.

Materials and methods

Juice

Wild bog bilberry fruits under a ripen stage were provided by Xinganlieshen Original Products Ltd. (Hulunbeir City, Inner Mongolia, China) in 2013. After cold-chain transportation to our lab, the berries were immediately crushed into juices and then filtered through 0.45 µm membranes. The juice had a 2.65 pH and was stored at − 20 °C before lactic acid fermentation. Before inoculation, the juice was divided into two portions. One portion of the juice was kept at its original pH, whereas the other portion was adjusted to pH 3.50 using NaOH solid power. Both juices were pasteurized at 85 °C for 15 min.

Bacterial revitalization, inoculation, and fermentation

Lactobacillus plantarum B7 and C8-1 were used for bog bilberry juice fermentation. L. plantarum B7 and C8-1 were isolated from sourdough and pickle in our lab (Beijing Key Laboratory of Forestry Food Processing and Safety, Beijing Forestry University, Beijing, China), respectively. The bacteria were plated onto the MRS agar plates and incubated at 37 °C for 48–72 h for enumeration according to a reference method (De Man et al. 1960). When the cell number in each strain medium reached ca. 109 CFU/mL, the strain (10 mL) was inoculated into 90-mL bog bilberry juice and transferred into a 100-mL capacity bottle. The lactic acid fermentation was carried out at 23 °C for 14 days. The juices before and after the fermentation process were sampled. Each fermentation was performed in duplicate.

Physicochemical indexes

Reducing sugar content and juice color intensity were determined using WineScan™ auto analyzer (FOSS Co., Ltd., Denmark). A PHS-3C pH meter (INESA Instrument Ltd., Shanghai, China) was used to measure the pH value of the juice. Organic acids in the juice were analyzed according to our published HPLC method (Wei et al. 2014). The quantitation of organic acids was carried out using external standards.

Amino acids

The derivatization of amino acids in the juice was carried out by mixing 500 µL of the juice with 10 µL of 1.00 g/L 2-aminoadipic acid (internal standard), 15 µL of diethyl ethoxymethylenemalonate, 375 µL of methanol, and 875 µL of 1 mol/L borate buffer (pH 9.0). The mixture was sonicated for 30 min and then incubated at 70 °C in a water bath for 2 h (Gómez Alonso et al. 2007). After the derivatization, the derivatized amino acids were separated on a Venusil XSB-C18 column (4.6 × 250 mm, 5 µm, Bonna-Agela Technologies, Tianjin, China). The mobile phase consisted of (A) acetonitrile: methanol, (4:1, v/v) and (B) 25 mM acetate buffer with 0.02% sodium azide (pH 5.8). The flow rate was set at 0.9 mL/min and the injection volume was 20 µL. The elution program was as follows: 90% B for 20 min; 90–83% B for 10.5 min; 83% B for 3 min; 83–73% B for 31.5 min; 73–28% B for 8 min; 28–18% B for 5 min; 28–0% B for 4 min; 0% B for 3 min; 0–90% B for 5 min; and 90% B for 3 min. The detection wavelength was 280 nm. External amino acid standards were derivatized using the same protocol and used for the quantitation.

Phenolic compounds

Anthocyanins and non-anthocyanin phenolic compounds were analyzed on an Agilent 1200 HPLC system coupled with a MSD Trap VL mass spectrometer (Agilent Technologies, Santa Clara, CA, USA) according to a published method (Gao et al. 2015). Before the injection, the juice was filtered through 0.45 µm microfiltration membranes. Anthocyanins were separated on a reverse C18 column (250 × 4.6 mm, 5 µm, Kromasil, Sweden) under a flow rate of 1.0 mL/min. A 50 µL sample was injected into HPLC system, and the mobile phase consisted of (A) water: formic acid: acetonitrile (92:2:6, v/v/v) and (B) water: formic: acetonitrile (44:2:54, v/v/v). The elution was programmed as follows: 0–10% B for 1 min; 10–25% B for 17 min; 25% B for 2 min; 25–40% B for 10 min; 40–70% B for 5 min; and 70–100% B for 5 min. The detection wavelength was 525 nm and a positive electrospray ionization was used. Non-anthocyanin phenolic compounds were separated on a reverse Zorbax SB-C18 column (50 × 3 mm, 1.8 µL, Agilent Technologies, Santa Clara, CA, USA) under a flow rate of 1.0 mL/min. A 2 µL sample was injected and the mobile phase consisted of (A) acetic acid: acetonitrile (1:99, v/v) and (B) acetic acid: water (1:99, v/v). The elution gradient was as follows: 0–5% B for 5 min; 5–8% B for 5 min; 8–12% B for 5 min; 12–18% B for 5 min; 18–22% B for 2 min; 22–35% B for 2 min; and 35–100% B for 4 min. The detection wavelength was 280 nm and a negative electrospray ionization mode was used. The nebulizer pressure, dry gas flow rate, and capillary voltage were set at 35 psi, 10 mL/min, and 325 °C, respectively. The full scan mode from m/z 100 to 1500 was used to record mass spectrum of anthocyanins and non-anthocyanin phenolic compounds. Malvidin-3-O-glucoside, catechin, quercetin, gallic acid, caffeic acid, and chlorogenic acid were used as the external standard to quantify anthocyanins, flavanols, flavonols, hydroxybenzoic acids, hydroxycinnamic acids, and chlorogenic acid, respectively.

Volatile compounds and sensory contribution

Volatile compounds in the juice were extracted using solid-phase micro-extraction according to a published method with minor modifications (Zhang et al. 2007). Briefly, 5 mL of the juice was mixed with 15 mL of NaCl in a vial tightly capped with a PTFE-silicon septum, and then heated at 40 °C for 30 min under an agitation speed of 400 rpm. Afterwards, a 50/30 μm DVB/Carboxen/PDMS fiber (Supelco, USA) was inserted into the headspace of the vial and adsorbed the volatiles for 30 min at 40 °C under the same agitation. Afterwards, the fiber was desorbed in the GC injector for 25 min. The volatile compounds were separated using a HP-INNOWAX column (0.25 μm film sickness, 60 m × 0.25 mm, J & W Scientific, USA) on an Agilent 6890 GC coupled with an Agilent 5975 mass spectrometry (Agilent Technologies, Santa Clara, CA, USA). The flow rate of carrier gas (helium) was 1 mL/min, and the oven temperature was programmed as follows: 50 °C for 1 min; raising at 3 °C/min to 220 °C; and 220 °C for 5 min. Electron impact mode was set at 70 eV with a mass scan range of m/z 20 to 450 under a selective ion mode. The volatiles were identified by comparing their mass spectrum with the available reference standard and further confirmed by the retention index on NIST and Wiley Mass Spectrometry. Volatiles were quantified using their corresponding external standard and calibrated by 4-methyl-2-pentanol as the internal standard. If the standard was not available, the quantitation of the volatiles was carried out using the external standard that possessed the similar structure or carbon atoms. Sensory contribution of the volatile in the juice was estimated using their odor activity value (OAV). OAV was calculated by the concentrations of volatiles in the juice over their odor threshold.

Statistical analyses

Data were expressed as the mean ± standard deviation of duplicate tests. One-way analysis of variance (ANOVA) was used to evaluate the significant differences among the mean value of each compound at p ≤ 0.05 on SPSS Statistics 23 (IBM, NY, USA).

Results and discussion

Physicochemical properties

Before the fermentation, the reducing sugar content was lower in the AJ than the NJ (Table 1). The fermentation resulted in a dramatic decrease on the reducing sugar content in the NJ, whereas the decrease on the reducing sugar content in the AJ was relatively slight.

Table 1.

Physicochemical indexes of bog bilberry juice with different pH conditions fermented by Lactobacillus plantarum B7 and C8-1

Compound Before inoculation After fermentation
pH 2.65 pH 3.50 pH 2.65 pH 3.50
B7 C8-1 B7 C8-1
Reducing sugar (g/L)
Fructose (g/L) 19.60 ± 0.00a 16.35 ± 0.07b 8.70 ± 0.00d 8.75 ± 0.07d 12.90 ± 0.99c 12.90 ± 0.28c
Glucose (g/L) 12.60 ± 0.00a 11.00 ± 0.00b 3.00 ± 0.00d 3.00 ± 0.14d 9.00 ± 0.85c 9.35 ± 0.35c
Total 32.20 ± 0.00a 27.35 ± 0.07b 11.70 ± 0.00d 11.75 ± 0.07d 21.90 ± 1.84c 22.25 ± 0.63c
Organic acids (g/L)
Quinic acid 6.84 ± 0.36a 6.49 ± 0.02a 6.41 ± 0.08a 6.77 ± 0.45a 1.83 ± 0.01b 1.39 ± 0.01b
Malic acid 3.45 ± 0.14a 3.70 ± 0.03a 0.29 ± 0.03c 0.56 ± 0.11c 1.38 ± 0.25b 1.33 ± 0.02b
Citric acid 3.41 ± 0.07a 3.50 ± 0.00a 2.82 ± 0.05b 2.78 ± 0.11b tr nd
Shikimic acid 0.02 ± 0.01b 0.03 ± 0.00b 0.03 ± 0.00b 0.02 ± 0.01b 0.88 ± 0.01a 0.87 ± 0.02a
Lactic acid nd nd 2.49 ± 0.14c 2.44 ± 0.35c 13.93 ± 0.30a 13.29 ± 0.31b
Acetic acid nd nd 0.25 ± 0.08b 0.29 ± 0.02b 2.24 ± 0.15a 2.30 ± 0.02a
Total 13.73 ± 0.28b 13.72 ± 0.01b 12.29 ± 0.13c 12.86 ± 0.81bc 20.27 ± 0.68a 19.16 ± 0.28a
pH
pH 2.65 ± 0.00b 3.50 ± 0.00a 2.58 ± 0.01c 2.63 ± 0.01b 3.47 ± 0.00a 3.50 ± 0.01a
Color attributes
Color intensity 9.80 ± 0.00a 9.55 ± 0.07b 9.60 ± 0.00b 9.60 ± 0.00b 9.20 ± 0.00c 9.25 ± 0.07c
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Data are the mean ± standard deviation (n = 2). “nd”, not detected; “tr”, trace. Means in the same row with different superscript letters (a–d) are significantly different (p < 0.05)

The AJ and the NJ exhibited the similar content of organic acids before the fermentation. However, the composition of organic acids appeared to be significantly different in these juices after the fermentation. An increase on the total organic acids content was observed in the AJ fermented by both strains, whereas a content decrease took place in the NJ. Quinic acid was the predominant organic acid in the juice. It naturally exists in gooseberries, pears, cherries, blackberries, and strawberries (Whiting 1958). It can be produced through shikimate pathway (Dewick 1998), and it is a key precursor to form aromatic rings in fruits (Hulme 1958). A significant decrease on the quinic acid level was observed in the AJ fermented by these strains. Meanwhile, shikimic acid was dramatically accumulated in the juice after the fermentation. However, the NJ did not show the significant differences on the quinic or shikimic acid level throughout the fermentation (Table 1). It has been reported that L. plantarum had the capability to degrade quinic acid as an electron acceptor, instead of sugar, to provide energy during fermentation (Filannino et al. 2015). Quinic acid could also be converted into shikimic acid (Ghosh et al. 2012). In this study, only the strains fermented juice (pH 3.50) showed the degradation of quinic acid and the accumulation of shikimic acid. Extremely low pH condition in the juice might inhibit this conversion. Regarding malic acid, a dramatic concentration decrease was observed in the juice after the fermentation by both strains. Similar results were also reported in other lactic acid bacteria fermented fruit juice (Filannino et al. 2014). Meanwhile, the concentration of lactic acid was enhanced in the juices after the fermentation. It was proposed that malic acid, during the lactic acid fermentation, was converted into lactic acid through the decarboxylation reaction under the activity of L. plantarum. This reaction could soften the mouthfeel of juice (Fugelsang and Edwards 2006). It should be noted that pH condition also affected the conversion ability of strains since the lactic acid level in the AJ after the fermentation was much higher than in the NJ. This was consistent with the previous study (Filannino et al. 2014). Similarly, acetic acid was produced more in the AJ compared with the NJ, whereas citric acid concentration decreased significantly. These was because that citric acid was metabolized into acetic acid by L. plantarum (Nilchian et al. 2016), and this metabolism depended on the pH condition of the juices.

No significant changes were observed in the pH of the juice before and after the fermentation by these strains (Table 1). Nevertheless, the AJ and the NJ showed the decreases in their color intensities after the fermentation. This might be caused by the alteration of the anthocyanins composition (Liu et al. 2015).

Amino acids

The bog bilberry juice contained 22 free amino acids (including 7 essential amino acids) and ammonium amine (Table 2). Regarding the essential amino acids, most of the aromatic amino acids and branched-chain amino acids showed a significant concentration increase after the fermentation. Meanwhile, the levels of valine, isoleucine, leucine, and lysine were much higher in the AJ. It has been reported that lactic acid bacteria could metabolize aromatic and branched-chain amino acids to produce energy, which could result in a concentration decrease of these amino acids during fermentation (Filannino et al. 2014). This was not consistent with our result. In this study, the consumption of quinic acid by these L. plantarum strains produced the energy for the bacterial growth. As a result, the biosynthesis of aromatic amino acids was promoted in the juice (Dewick 1998). In terms of the branched-chain amino acids, lysine and threonine were found to be higher in the AJ. This indicated that these strains might possess a high peptidase ability in a high pH condition during the lactic acid fermentation, which significantly enhanced the biosynthesis of the branched-chain amino acids through the peptide metabolisms (Pritchard and Coolbear 1993). Additionally, most nonessential amino acids also increased on their concentration in the juice after the fermentation.

Table 2.

Concentration of amino acids in bog bilberry juice with different pH conditions fermented by Lactobacillus plantarum B7 and C8-1

Compound (mg/L) Before inoculation After fermentation
pH 2.65 pH 3.50 pH 2.65 pH 3.50
B7 C8-1 B7 C8-1
Essential Amino Acids
Aromatic amino acids
 Phenylalanine 0.79 ± 0.20b 0.81 ± 0.22b 4.77 ± 0.48a 4.26 ± 0.06a 5.66 ± 1.24a 3.97 ± 1.29a
Branched-chain amino acids
 Valine 1.03 ± 0.29b 1.03 ± 0.30b 1.49 ± 0.01b 1.17 ± 0.27b 5.13 ± 0.11a 4.76 ± 0.95a
 Leucine 0.74 ± 0.18b 0.75 ± 0.16b 3.98 ± 1.20b 3.11 ± 0.42b 8.40 ± 1.32a 9.23 ± 0.99a
 Isoleucine 0.33 ± 0.08b 0.71 ± 0.44b 1.02 ± 0.19b 0.57 ± 0.33b 5.31 ± 0.25a 5.61 ± 0.48a
Others
 Lysine 1.53 ± 0.04c 1.61 ± 0.09bc 1.51 ± 0.28c 1.47 ± 0.21c 8.52 ± 4.21ab 9.34 ± 0.70a
 Threonine 1.08 ± 0.25a 1.20 ± 0.25a 2.45 ± 0.18ab 1.62 ± 1.02ab 4.62 ± 2.64a 3.05 ± 0.92ab
 Methionine 0.62 ± 0.13a 0.69 ± 0.17a 0.70 ± 0.02a 0.60 ± 0.01a 0.76 ± 0.11a 0.71 ± 0.02a
Nonessential amino acids
 γ-Aminobutyric acid 5.68 ± 0.72a 5.61 ± 0.71a 8.45 ± 0.82a 8.03 ± 1.11a 6.00 ± 0.65a 6.38 ± 2.51a
 Arginine 2.56 ± 0.13c 2.70 ± 0.26c 7.95 ± 0.12b 5.68 ± 0.68bc 13.91 ± 2.22a 13.23 ± 1.33a
 Asparaginate 1.59 ± 0.29a 1.75 ± 0.25a 0.34 ± 0.07bc 0.30 ± 0.12c 0.99 ± 0.33abc 1.30 ± 0.30ab
 Cysteine 1.48 ± 0.16a 1.51 ± 0.27a 0.37 ± 0.52b 0.53 ± 0.75ab nd nd
 Glycine 1.36 ± 0.21c 1.33 ± 0.02c 12.33 ± 0.43ab 8.50 ± 2.88b 17.42 ± 1.66a 17.20 ± 0.91a
 α-Alanine 1.35 ± 0.29b 1.36 ± 0.29b 6.12 ± 0.06a 5.00 ± 1.18a 5.27 ± 0.91a 4.70 ± 1.19a
 Ornithine 0.86 ± 0.31a 0.89 ± 0.30a 1.98 ± 0.10a 1.82 ± 0.04a 1.57 ± 0.25a 2.08 ± 1.34a
 Tyrosine 0.69 ± 0.02b 0.61 ± 0.05b 1.26 ± 0.00a 1.27 ± 0.11a 0.88 ± 0.15ab 1.13 ± 0.27ab
 Glutamic acid 0.44 ± 0.62a 0.95 ± 0.04a nd 1.98 ± 2.81a 0.45 ± 0.64a 1.59 ± 2.25a
 Serine 0.42 ± 0.07b 1.12 ± 0.08ab 0.88 ± 0.04ab 1.05 ± 0.03ab 1.69 ± 0.26a 0.59 ± 0.83b
 β-Alanine 0.30 ± 0.07c 0.32 ± 0.10bc 0.24 ± 0.01c 0.29 ± 0.05c 1.39 ± 0.66a 0.26 ± 0.02c
 Proline 0.13 ± 0.18b 0.84 ± 0.80ab 2.13 ± 0.11ab 1.49 ± 0.59ab 3.26 ± 0.90a 2.09 ± 0.83ab
 Glutamine nd 1.72 ± 0.27a 0.95 ± 0.15c 1.10 ± 0.04bc 1.57 ± 0.11ab 1.61 ± 0.37a
 Histidine nd 1.55 ± 0.23ab nd nd 2.38 ± 0.07b 1.24 ± 1.75ab
 Aspartic acid nd tr 0.44 ± 0.62a 0.65 ± 0.34a nd 0.33 ± 0.02a
 Total 22.98 ± 1.65c 29.05 ± 2.58c 59.34 ± 0.26b 50.48 ± 4.50b 95.18 ± 10.15a 90.39 ± 16.08a
Ammonium amine
 NH4+ 0.63 ± 0.19b 1.24 ± 0.17b 1.54 ± 0.37b 1.19 ± 0.26b 22.51 ± 1.74a 21.38 ± 3.33a
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Data are the mean ± standard deviation (n = 2). “nd”, not detected; “tr”, trace. Means in the same row with different superscript letters (a–c) are significantly different (p < 0.05)

The L. plantarum strains preferred to metabolize quinic acid, citric acid, and malic acid in the AJ during the fermentation. Meanwhile, the consumption of the reducing sugar in the AJ was inhibited. However, the major energy source in the NJ resulted from malic acid and the reducing sugar. The consumption of the reducing sugar in this juice was much higher than that in the AJ, and the rapid consumption of malic acid during the fermentation could inhibit the activity of the L. plantarum strains to metabolize other nutrients. Besides, the lower malic acid level in the NJ might be due to the greater energy requirement in acidic environment, since the decarboxylation of organic acids can supply extra ATP to sustain a proton balance inside and outside the cell membrane (Guchte et al. 2002).

Phenolic compounds

Anthocyanins are the major colorants in fruits that play an important role in the appearance of fruit juice (Pascual-Teresa et al. 2013). Before the fermentation, the major anthocyanins in the juice included malvidin-3-O-glucoside, petunidin-3-O-glucoside, and delphinidin-3-O-glucoside. Our result was consistent with the previous report (Wang et al. 2014). The fermentation decreased the anthocyanin levels in all the juices (Table 3). It has been reported that β-glucosidase released by L. plantarum can easily cleave anthocyanins into anthocyanidins and sugar moieties. Sugar moieties can be further metabolized by L. plantarum as the carbohydrate source (Mousavi et al. 2013). Moreover, anthocyanidins could interact with other phenolic compounds to form large polymers (Baranowski and Nagel 1983). As a result, the concentration of anthocyanins after the lactic acid fermentation was reduced, causing a decrease on the juice color intensity.

Table 3.

Concentration of phenolic compounds in bog bilberry juice with different pH conditions fermented by Lactobacillus plantarum B7 and C8-1

Compound (mg/L) Before Inoculation After Fermentation
pH 2.65 pH 3.50 pH 2.65 pH 3.50
B7 C8-1 B7 C8-1
Anthocyanins
Malvidin-3-O-glucoside 110.64 ± 0.16a 108.28 ± 16.40a 37.24 ± 5.72b 30.98 ± 5.96b 40.24 ± 2.94b 36.68 ± 3.80b
Petunidin-3-O-glucoside 96.34 ± 0.64a 100.58 ± 3.44a 31.26 ± 4.46b 25.28 ± 3.96b 26.60 ± 0.72b 24.32 ± 2.52b
Delphinidin-3-O-glucoside 64.38 ± 0.92a 64.98 ± 8.86a 19.32 ± 2.68b 16.64 ± 2.90b 13.38 ± 0.64b 11.36 ± 0.96b
Cyaniding-3-O-glucoside 13.58 ± 0.40a 13.24 ± 1.62a 3.74 ± 0.56b 2.92 ± 0.44b 4.60 ± 0.02b 4.14 ± 0.30b
Peonidin-3-O-glucoside 9.20 ± 0.08a 9.18 ± 0.98a 2.70 ± 0.38b 2.26 ± 0.38b 3.46 ± 0.22b 3.12 ± 0.20b
Total 294.12 ± 2.14a 296.24 ± 31.30a 94.28 ± 13.78b 78.08 ± 13.64b 88.28 ± 4.56b 79.62 ± 7.76b
Phenolic acids
Protocatechuic acid 40.38 ± 0.64a 42.04 ± 0.24a 2.24 ± 0.40b 1.70 ± 0.08b 2.76 ± 0.68b 2.12 ± 0.30b
Chlorogenic acid 30.26 ± 0.20a 29.88 ± 0.04ab 20.14 ± 1.50abc 19.12 ± 2.92bc 18.12 ± 1.34c 22.32 ± 5.76abc
Gallic acid 2.44 ± 0.00b 3.04 ± 0.24a tr tr tr tr
Caffeic acid 2.30 ± 0.08a 2.44 ± 0.18a 1.30 ± 0.40b 0.96 ± 0.76b tr tr
4-Hydroxycinniamic acid 1.12 ± 0.04a 0.64 ± 0.90a tr tr tr tr
2-Hydroxybenzoic acid tr tr 0.16 ± 0.02 0.16 ± 0.10 0.14 ± 0.06 0.14 ± 0.08
Total 76.50 ± 0.56a 78.04 ± 1.62a 23.88 ± 2.32b 21.92 ± 3.88b 21.02 ± 2.08b 24.58 ± 5.40b
Flavonols
Myricetin-3-O-galactoside 124.20 ± 0.04a 121.58 ± 1.30a 71.12 ± 5.10b 65.72 ± 10.72b 79.16 ± 6.28b 76.72 ± 11.52b
Quercetin-3-O-galactoside 101.86 ± 0.18a 103.18 ± 0.16a 52.68 ± 3.42b 48.22 ± 7.94b 80.72 ± 5.06a 80.18 ± 10.10a
Quercetin-3-O-glucuronide 29.66 ± 0.04a 29.50 ± 0.10a 14.68 ± 1.24b 13.08 ± 2.74b 17.46 ± 1.62b 16.80 ± 2.68b
Syringetin-3-O-galactoside 12.54 ± 0.12a 13.12 ± 0.58a 8.02 ± 0.40b 7.52 ± 1.26b 7.56 ± 0.56b 7.28 ± 1.06b
Quercetin 5.10 ± 0.90b 1.72 ± 0.22c 20.92 ± 2.52a 19.90 ± 0.01a tr tr
Myricetin 4.90 ± 0.26a 4.20 ± 0.06a 4.52 ± 0.36a 4.06 ± 1.02a 0.84 ± 0.26b 0.72 ± 0.02b
Isorhamnetin-3-O-galactoside 3.52 ± 0.08a 3.90 ± 0.04a 1.42 ± 0.14b 1.22 ± 0.34b 2.16 ± 0.30b 2.12 ± 0.34b
Syringetin-3-O-glucoside 3.12 ± 0.10a 2.82 ± 0.46ab 1.94 ± 0.12b 1.80 ± 0.36b 1.84 ± 0.14b 1.76 ± 0.24b
Myricetin-3-O-glucoside 1.96 ± 0.26a 1.76 ± 0.42a 0.52 ± 0.22b 0.40 ± 0.26b 1.40 ± 0.18ab 1.38 ± 0.32ab
Total 286.88 ± 1.96a 281.70 ± 0.32a 177.88 ± 13.60b 161.92 ± 24.62b 191.14 ± 14.40b 186.94 ± 26.28b
Flavanols
Epicatechin 26.30 ± 0.96a 28.70 ± 1.36a 2.18 ± 0.94b 0.86 ± 1.00b 3.96 ± 0.02b 2.80 ± 0.14b
Epigallocatechin 23.38 ± 0.80a 23.78 ± 0.90a 6.50 ± 0.84b 5.40 ± 0.46b 6.00 ± 0.02b 4.68 ± 0.16b
Gallocatechin 2.22 ± 0.12a 2.32 ± 0.26a 0.48 ± 0.20bc 0.28 ± 0.02c 0.88 ± 0.08b 0.64 ± 0.02bc
Catechin 1.12 ± 0.16a 1.44 ± 0.10a 0.10 ± 0.06b 0.06 ± 0.02b 0.26 ± 0.36b 0.40 ± 0.02b
Total 53.00 ± 1.78a 56.22 ± 2.46a 9.26 ± 2.06b 6.58 ± 1.46b 11.08 ± 0.48b 8.52 ± 0.08b
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Data are the mean ± standard deviation (n = 2). “nd”, not detected; “tr”, trace. Means in the same row with different superscript letters (a–c) are significantly different (p < 0.05)

Protocatechuic and chlorogenic acids were the dominant phenolic acids in the juice. After the fermentation, protocatechuic acid showed a dramatic concentration decrease in all the juices. Similar evolution of protocatechuic acid was also observed in lactic acid fermentation of cherry juice (Filannino et al. 2015). Chlorogenic acid also exhibited a concentration decrease. It has been reported that L. plantarum could release decarboxylase and esterase, and these enzymes can degrade a wide range of phenolic acids (Di Cagno et al. 2015). However, the other phenolic acids remained at a low level in the juices during the fermentation process.

The bog bilberry juices contained the abundant amount of myricetin-3-O-galactoside and quercetin-3-O-galactoside before the fermentation. This was consistent with the previous study in bog bilberry wine (Liu et al. 2015). These two flavonols showed a dramatic concentration decrease in all the juices. Quercetin-3-O-galactoside remained the similar concentration in the AJ after the fermentation. However, the alteration on the concentration of quercetin was differentiated by the pH adjustment. A significant concentration increase of quercetin was observed in the NJ, whereas the AJ showed a reduced level. Compared with a previous study (Filannino et al. 2015), lactic acid fermentation of cherry juice did not cause the concentration alteration of quercetin. It has been reported that β-glycosidase produced by L. plantarum strains can hydrolyze glycosylated flavonols into their aglycones (Di Cagno et al. 2015), and low pH condition in the NJ might enhance the activity of β-glycosidase.

Epicatechin and epigallocatechin were the major flavanols in the bog bilberry juice. Both compounds showed a concentration decrease after the fermentation. Their concentration decrease might result from their oxidation, interactions with anthocyanins, or the metabolism by L. plantarum (Tabasco et al. 2011). However, the other flavanols did not significantly change on their level in the juice after the fermentation.

Volatile compounds

A total of 29 volatile compounds were detected in these bog bilberry juices before the fermentation. It was observed that the concentration of α-terpineol and ethyl octanoate in the juice decreased after adjusting the juice pH from 2.65 to 3.50 (Table 4). After the fermentation by these two strains, 32 volatile compounds were detected in the NJ, whereas the AJ juice contained 28 volatiles. The juice pH appeared to play an important role in affecting the evolution of the volatile compounds during the fermentation. For example, almost all the volatile compounds exhibited a significant concentration increase in the NJ by these two strains, whereas the concentrations of terpenoids, esters and acids decreased in the AJ.

Table 4.

Concentration of volatile compounds in bog bilberry juice with different pH conditions fermented by Lactobacillus plantarum B7 and C8-1

Compound (μg/L) Before inoculation After fermentation
pH 2.65 pH 3.50 pH 2.65 pH 3.50
B7 C8-1 B7 C8-1
Terpenoids
α-Terpineol 4.28 ± 0.66b 2.98 ± 0.16c 5.93 ± 0.18a 5.22 ± 0.03ab 2.53 ± 0.09c 2.76 ± 0.01c
Linalool 2.69 ± 0.91ab 3.37 ± 0.33a 2.94 ± 0.36ab 2.28 ± 0.04ab 1.66 ± 0.10b 1.58 ± 0.06b
6-Methyl-5-hepten-2-one 1.52 ± 0.32a 1.59 ± 0.06a 1.76 ± 0.21a 1.63 ± 0.07a 1.35 ± 0.01a 1.45 ± 0.08a
Citronellyl formate nd nd 1.18 ± 0.04 0.57 ± 0.81 1.18 ± 0.02 1.16 ± 0.01
Total 8.49 ± 0.57bc 7.94 ± 0.56cd 11.81 ± 0.36a 9.70 ± 0.82b 6.72 ± 0.21d 6.95 ± 0.16d
Alcohols
Phenylethyl alcohol 663.48 ± 46.43b 617.49 ± 15.47b 1731.21 ± 93.00a 1775.80 ± 8.84a 459.67 ± 9.07c 463.40 ± 6.83c
(Z)-3-Hexen-1-ol 75.51 ± 8.84bc 63.76 ± 0.75c 258.14 ± 18.03a 265.64 ± 37.99a 127.70 ± 13.37bc 142.05 ± 0.94b
1-Hexanol 42.79 ± 2.13b 36.13 ± 1.76b 68.98 ± 3.10a 66.86 ± 2.96a 25.07 ± 1.93c 26.02 ± 0.02c
1-Heptanol 10.98 ± 0.06b 9.78 ± 0.52b 16.14 ± 0.37a 15.21 ± 0.92a 4.56 ± 0.04c 4.60 ± 0.08c
1-Octen-3-ol 1.01 ± 0.05a 0.93 ± 0.05ab 0.85 ± 0.02bc 0.76 ± 0.03c 0.50 ± 0.01d 0.49 ± 0.01d
1-Octanol 0.31 ± 0.00b 0.29 ± 0.00bc 0.68 ± 0.03a 0.62 ± 0.02a 0.26 ± 0.01bc 0.24 ± 0.00c
3-Octanol 0.10 ± 0.02a 0.08 ± 0.00a 0.03 ± 0.04a nd nd nd
2-Ethyl-1-hexanol tr tr 1.58 ± 0.83a 1.14 ± 0.33a 0.97 ± 0.10a 0.84 ± 0.10a
Benzyl alcohol nd nd 135.42 ± 10.01a 134.47 ± 6.14a 99.19 ± 6.27a 97.46 ± 2.51a
1-Dodecanol nd nd 0.64 ± 0.01a 0.64 ± 0.00a nd nd
2-Heptanol nd nd nd nd 2.16 ± 0.00a 2.26 ± 0.11a
Total 794.17 ± 57.28b 728.45 ± 12.39b 2213.67 ± 83.17a 2261.13 ± 24.67a 720.07 ± 30.79b 737.35 ± 10.60b
Acids
Octanoic acid 1538.15 ± 280.98b 1156.53 ± 13.95bc 3921.58 ± 449.01a 4013.15 ± 454.80a 655.34 ± 108.56c 722.93 ± 30.91c
Hexanoic acid 147.01 ± 7.05b 132.57 ± 0.36b 272.10 ± 8.54a 266.00 ± 12.95a 136.89 ± 16.86b 123.18 ± 1.06b
Pentanoic acid nd nd nd nd 17.39 ± 1.35a 16.24 ± 0.05a
Total 1685.16 ± 288.03b 1289.09 ± 14.30bc 4193.69 ± 457.55a 4279.15 ± 467.74a 809.63 ± 90.35c 862.35 ± 32.02c
Esters
Ethyl nonanoate 19.50 ± 0.99b 18.42 ± 0.82b 24.37 ± 4.17ab 28.46 ± 6.90a nd nd
Ethyl octanoate 18.05 ± 1.13b 8.69 ± 1.32c 26.24 ± 1.29a 25.03 ± 0.40a 4.66 ± 0.06d 4.60 ± 0.01d
Ethyl laurate 10.00 ± 1.06a 9.61 ± 0.70a 6.07 ± 8.59a 13.39 ± 3.07a nd 8.98 ± 0.09a
Isopentyl acetate 7.65 ± 1.80b 7.27 ± 0.32b 30.34 ± 2.54a 27.51 ± 4.15a nd nd
Ethyl hexanoate 3.86 ± 0.87b 3.26 ± 0.19b 7.79 ± 0.24a 7.62 ± 1.51a nd nd
Ethyl butanoate 1.82 ± 0.25b 1.63 ± 0.06b 2.43 ± 0.25a 2.58 ± 0.36a nd nd
Methyl salicylate 1.67 ± 0.05b 1.54 ± 0.04b 2.35 ± 0.07a 2.13 ± 0.10a 2.09 ± 0.22a 1.76 ± 0.07b
Isobutyl acetate 1.60 ± 2.26b 3.23 ± 0.03b 5.98 ± 0.35ab 2.99 ± 4.23ab 9.85 ± 0.60a nd
Ethyl phenylacetate 0.60 ± 0.02b 0.54 ± 0.02b 1.00 ± 0.06a 0.94 ± 0.07a nd nd
Total 64.74 ± 4.18b 54.20 ± 3.39b 106.57 ± 9.06a 110.66 ± 0.65a 16.60 ± 0.75c 15.35 ± 0.02c
Aldehyde/Ketones
Benzaldehyde 41.78 ± 4.50cd 39.20 ± 0.85d 55.49 ± 1.09ab 62.28 ± 0.79a 47.72 ± 2.41bcd 48.47 ± 1.83bc
Nonanal 0.55 ± 0.78a 1.18 ± 0.03a 1.17 ± 0.01a 0.59 ± 0.83a 1.06 ± 0.01a 1.04 ± 0.00a
Total 42.33 ± 3.72d 40.39 ± 0.87d 56.67 ± 1.10b 62.86 ± 0.04a 48.78 ± 2.41c 49.51 ± 1.83c
Others
Styrene 23.23 ± 10.85a 9.40 ± 0.71ab 5.09 ± 0.56b 5.63 ± 0.41ab 4.78 ± 0.07b 3.87 ± 0.02b
Cyclohexene 1.71 ± 0.13a 1.46 ± 0.03ab 1.63 ± 0.07ab 1.73 ± 0.08a 1.40 ± 0.00b 1.40 ± 0.00b
Naphthalene 1.48 ± 0.05b 5.21 ± 0.22a 1.65 ± 0.19b 1.72 ± 0.17b 1.56 ± 0.00b 1.58 ± 0.08b
β-Methylnaphthalene 1.44 ± 0.00b 3.42 ± 0.01a 1.56 ± 0.01b 1.67 ± 0.01b 1.40 ± 0.00b 1.46 ± 0.00b
α-Methylnaphthalene 0.70 ± 1.00a 1.92 ± 0.04a 0.73 ± 1.03a 1.45 ± 0.03a nd 1.40 ± 0.01a
Total 28.58 ± 9.62a 21.40 ± 1.17ab 10.64 ± 2.04c 12.20 ± 0.67bc 9.13 ± 0.07c 9.71 ± 0.12c
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Data are the mean ± standard deviation (n = 2). nd, not detected; tr trace. Means in the same row with different superscript letters (a–d) are significantly different (p < 0.05)

Odor active value (OAV) is basically used to evaluate the contribution of the individual volatile compound to the overall aroma in foods. A volatile with its OAV value above 1 is normally considered to significantly contribute its flavor notes to the overall aroma (Zhang et al. 2007). A total of 9 volatile compounds in the juices exhibited its OAV above 1, including 4 alcohols, 1 acid, 3 esters, and 1 aldehyde (Table 5). These volatile compounds were thus suggested to have a significant impact on the overall aroma in the juices. It was the pH condition of the juice, instead of the strains, that significantly affected the evolution of these volatiles in the juice during the fermentation. For example, phenylethyl alcohol exhibits the floral note, whereas 1-heptanol can provide the oily flavor to juice (Lee et al. 2008). Both alcohols significantly increased the concentration in the NJ. However, the OAV of these two alcohols were reduced in the AJ after the fermentation. This indicated that these volatile compounds did not exert the significant contribution to the overall aroma of the AJ. Octanoic acid provides juice with the chemical flavor (Coelho et al. 2015), and its concentration was detected below its threshold in the AJ and NJ before the fermentation. However, the fermentation in the NJ resulted in its OVA above 1, indicating that octanoic acid significantly contributed its flavor note to the overall aroma in the juice. The AJ after the fermentation contained octanoic acid with its concentration below its threshold. Ethyl butanoate, isopentyl acetate, and ethyl hexanoate were the major esters in the juices with their OAV above 1, and these esters contributed the fruity aroma to the juice regarding their aromatic feature (Wu et al. 2016). A dramatic increase on the OAV of these esters occurred in the NJ after the fermentation, whereas their aroma contributions were neglectable in the AJ. Nonanal is an aldehyde with the fruity note (Wen et al. 2014). Its OAV value remained similar after the fermentation by these strains. These results indicated that the NJ after the fermentation significantly improved the floral and fruity notes. However, the overall aroma of the AJ after the fermentation was significantly weakened.

Table 5.

Odor activity value (OAV) of main aromatic compound in bog bilberry juice with different pH conditions fermented by Lactobacillus plantarum B7 and C8-1

Compound Threshold[1]* (μg/L) Aroma description Aroma series Before inoculation After fermentation
pH 2.65 pH 3.50 pH 2.65 pH 3.50
B7 C8-1 B7 C8-1
Alcohols
(Z)-3-Hexen-1-ol 70 Grassy-green Green 1.08c 0.91c 3.69a 3.79a 1.82b 2.03b
1-Octen-3-ol 1 Earthy, mushroom, vegetable-like Chemical, Green 1.01a 0.92b 0.84c 0.76d 0.49e 0.49e
1-Heptanol 3 Oily, planty Chemical 3.66b 3.26c 5.38a 5.07a 1.52d 1.53d
Phenylethyl alcohol 750 Soft, like roses, jasmine Floral 0.88b 0.82b 2.31a 2.37a 0.61c 0.61c
Acids
Octanoic acid 3000 Faint, fruity-acid, irritating Chemical 0.51b 0.39bc 1.31a 1.34a 0.22c 0.24c
Esters
Ethyl butanoate 1 Strawberry, fruity Fruity 1.82b 1.63b 2.43a 2.58a nd nd
Isopentyl acetate 2 Banana, pear, fruity, sweet Fruity 3.64b 3.83b 15.17a 13.75a nd nd
Ethyl hexanoate 1 Fruity, green apple Fruity, Green 3.86b 3.26b 7.79a 7.62a nd nd
Aldehyde/Ketones
Nonanal 1 Fruity Fruity 0.55a 1.18a 1.17a 0.59a 1.06a 1.04a
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*Reference [1] http://www.leffingwell.com/odorthre.htm. Values in the same row with different superscript letters (a–e) are significantly different (p < 0.05). Aroma series is classified according to aroma description. Volatile compound with OAV above 1 is qualified

It has been confirmed that amino acids and phenolic compounds can be converted into aromatic compounds by lactic acid bacteria (Helinck et al. 2004). As a result, the fermented flavor notes can be incorporated into the overall aroma of the fermented foods to enhance the aromatic complexity (Chen and Liu 2016). In addition, the flavorless bound form volatiles are mainly present in foods. Hydrolysis could result in the release of their aglycones, which could further improve the overall aroma in foods (Ugliano et al. 2003). In this study, L. plantarum possesses the β-glucosidase activity, and this could enhance the release of the volatile aglycones from their precursors in the juices. These volatiles can further be metabolized by L. plantarum to yield other compounds (Boido et al. 2002). For example, in this study, quercetin-3-O-galactoside significantly decreased its concentration in the NJ after the fermentation. Meanwhile, the juice showed a significant increase on the concentration of quercetin. These indicated that quercetin-3-O-galactoside was hydrolyzed into quercetin and galactose moiety. This was because that malic acid was completely consumed in the NJ. The L. plantarum strains required more reducing sugar and energy compared to the strains in the AJ. As a result, these strains hydrolyzed more glycosidically conjugated phenolic and aromatic compounds to obtain monosaccharide (e.g. galactose) for their energy needs. This could explain why more volatile compounds were yielded in the NJ after the fermentation by these strains. In the AJ, the consumption of reducing sugar was relatively slow by these strains during the fermentation process. The L. plantarum strains did not require monosaccharides as the energy source in the juice, which lowered the hydrolysis process of the glycosidically conjugated phenolic and aromatic compounds. This resulted in the AJ with lower concentration of the volatile compounds after the fermentation.

Conclusion

In conclusion, malic acid and reducing sugar were mainly consumed by two L. plantarum strains in juice without pH adjustment after fermentation. These strains preferred to metabolize quinic acid and citric acid in pH adjusted juice, and resulted in more release of shikimic acid, lactic acid, acetic acid, and aromatic amino acids. Phenolic compounds decreased on their concentration in juices after fermentation. Juice without pH adjustment exhibited an enhancement on volatile complexity and concentration.

Acknowledgements

This study was financially supported by the grand of China Forestry Administration 948 Project (No. 2015-4-49) and the Fundamental Research Funds for the Central Universities (Nos.YX2015-15 and 201610022032). The authors sincerely thanked Dr. Changqing Duan and his team at the Center of Viticulture and Enology at the China Agricultural University for the help on analyses of phenolic and volatile compounds. The authors sincerely thanked Dr. Zheng Li in the Food Science and Human Nutrition Department at the University of Florida for the language editing and the discussion suggestion of the manuscript.

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