Study on fermentation kinetics, antioxidant activity and flavor characteristics of <i>Lactobacillus plantarum</i> CCFM1050 fermented wolfberry pulp

Hailong Liu; Na Li; Yutong Wang; Tianyu Cheng; Hua Yang; Qiang Peng; Hailong Liu; Na Li; Yutong Wang; Tianyu Cheng; Hua Yang; Qiang Peng

doi:10.48130/fia-0024-0012

As a superfruit, wolfberry has extremely high nutritional value, and how to enhance the accessibility of its nutrients is the core of current research. This study focused on exploring the kinetic model of Lactobacillus plantarum CCFM1050 fermentation of wolfberry and the potential alterations of antioxidant activity and volatile flavor compounds induced by lactic acid fermentation. we monitored cell counts, product formation, and substrate changes over a 72-h period of wolfberry fermentation. A kinetic model was developed to illustrate cell growth, substrate consumption, and product accumulation during wolfberry pulp fermentation. Phenolic substance analysis revealed a significant increase in total phenol and flavonoid content in wolfberry pulp during fermentation, reaching 1.16 and 1.15 times, respectively, compared to pre-fermentation levels. The elevated levels of phenolic substances led to a substantial increase in DPPH and ABTS free radical scavenging rates in fermented wolfberry pulp, reaching 67.16% and 32.10%, respectively. Volatile components of samples were analyzed using the HS-GC-IMS method, and fingerprints of wolfberry pulp before and after fermentation were established. A total of 51 compounds were identified, including 12 alcohols, seven aldehydes, two acids, eight esters, and 12 ketones, contributing to an enhanced flavor profile in the fermented wolfberry pulp. This study is helpful for understanding the kinetic changes in the lactic acid fermentation of wolfberry, the changes of antioxidant active substances and VOCs, and provides guidance for the industrial processing of wolfberry.

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Introduction

Wolfberry (Lycium chinense Miller) is a deciduous shrub in the Solanaceae family, found in China and other parts of Asia. Its fruit, bright orange-red oval berries measuring 1−2 cm in length, is traditionally used as an herb and functional food in Asian countries. Polysaccharides, flavonoids, and polyphenols are recognized as the primary bioactive constituents of wolfberry, showcasing a range of effects including anti-aging^[1], neuroprotection, hypoglycemic, and hypolipidemic properties^[2], immune modulation, anti-tumor activity^[3], and cellular protection^[4]. As a result, the consumption of wolfberry is anticipated to mitigate the risks associated with certain diseases and conditions linked to oxidative stress, while simultaneously enhancing antioxidant defense mechanisms. To optimize the absorption efficiency of polyphenols and other beneficial substances in wolfberries within the human body and fully harness their antioxidant functions, the adoption of innovative technologies becomes imperative^[5]. Lactic acid fermentation emerges as a widely employed technique in the processing of functional foods, renowned for its capacity to significantly enhance various nutritional components. This method holds promise for enhancing the bioavailability and beneficial effects of wolfberry constituents, thereby potentially maximizing their health-promoting properties.

Fermentation by lactic acid bacteria (LAB) has the potential to enhance a variety of bioactive compounds within the substrate^[6], making it a promising alternative for the processing of wolfberry. The organic acids, esters, and other substances produced during fermentation can boost the antioxidant capacity of wolfberry pulp^[5], providing beneficial effects on human health post-consumption. Prebiotic compounds, identified as 'selective fermentation agents facilitating specific changes in the composition and/or functioning of gut microbiota, beneficial for the well-being and health of the host', has been observed in research to stimulate probiotic proliferation in fermentation products, thereby improving fermentation efficiency and overall effectiveness. Numerous studies have highlighted the advantages of employing Lactobacillus plantarum in the biological processing of fruits and vegetables. For instance, in addition to improving sensory perceptions, fermentation can significantly augment aroma components in apple juice^[7], kiwi fruit^[8], and wolfberry juice^[9]. This enhances health benefits, as the hydrolase of L. plantarum releases antioxidant compounds from conjugated phytochemicals in fruits and vegetables^[10,11]. To the best of our knowledge, the current research on wolfberry mainly focuses on the fermentation of its plant components or extracts, and the fermentation of fruit pulp has not been reflected in the literature. The fermentation process of wolfberry pulp is complex and influenced by various factors such as the amount of added prebiotics, the inoculum size of lactic acid bacteria, and the fermentation time. Therefore, developing an accurate kinetic model is not only advantageous for comprehending and forecasting the dynamic alterations of several crucial parameters throughout the fermentation process, but it also aids in optimizing fermentation conditions. This, in turn, aims to achieve increased efficiency and energy savings through model optimization.

Following the above discussion, this study was conducted in three distinct parts. Firstly, the changes of substrates, products and bacterial number parameters in the process of fermentation of wolfberry pulp by Lactobacillus plantarum were recorded, and the kinetic model equation of lactic acid fermentation of wolfberry pulp was emphatically explored. In addition, the changes in phenolic compounds and antioxidant activity in unfermented goji berry pulp and fermented goji berry pulp were analyzed. In the third part, the volatile aroma components of wolfberry were detected by GC-IMS to clarify the effect of fermentation on the aroma change of wolfberry pulp.

Materials and methods

Materials

Dried wolfberry sourced from Ningxia Runxinyuan Wolfberry Development Co., Ltd. (Zhongning, China). Lactobacillus plantarum CCFM1050 obtained from the Fruit and Vegetable Storage and Processing Laboratory of the School of Food Science and Engineering, Northwest A&F University (Yangling, China). DPPH (D4313), ABTS(IA0010), Caffeic acid (SC8010), Gallic acid (SG8040), Rutin (SR8250), and other phenolic standard products were purchased from Beijing Solarbio Science & Technology Co., Ltd. (Beijing, China).

Preparation of wolfberry pulp
Dried wolfberry was thoroughly rinsed with tap water. Spoiled berries were removed, and the remaining berries were soaked in tap water at a ratio of 1:5 (w/v). After pulp beating, the mixture was homogenized under a colloid mill for 10 min. The resulting wolfberry pulp was then sterilized at 100 °C for 5 min cooled and set aside for use.

Preparation of bacterial cultures
Lactobacillus plantarum CCFM1050, stored in a glycerol solution at −80 °C was first thawed at room temperature and then activated in 20 mL MRS broth at 37 °C for 12 h. One hundred μL bacterial culture was activated twice, washed with 20 mL of physiological saline, and utilized as an inoculum for wolfberry pulp.

Prebiotic screening single factor experiment
The activated bacterial culture's viability was determined using the coating plate method. A 1.0 × 10⁸ CFU/100 g concentration served as the 1% inoculum. Firstly, inulin, lactulose, and oligosaccharides were individually added to 50 g of wolfberry pulp at 1%, 3%, 5%, 7%, and 9% concentrations. Then after 24 h of fermentation, measurements were taken for total acid content and viable bacterial count.

Construction of fermentation dynamics model
Leveraging the insights gleaned from prior response surface optimization experiments, Lactobacillus plantarum CCFM1050 was employed as the fermentation strain. Primarily, each 100 g of wolfberry pulp received supplementation of 1 × 10⁸ bacterial solution, coupled with the addition of 0.06 g of oligosaccharides for the fermentation process. Next, sampling intervals of 6 h was maintained throughout the fermentation trajectory to scrutinize the dynamics of viable bacteria, reducing sugars, and total acid content. The model's parameters were methodically computed based on the empirical data.

Dynamic model of bacterial growth

The growth of bacterial cells typically adheres to an 'S' curve, a pattern well-suited for simulation by the logistic equation^[12]. This equation effectively captures the changes in bacterial growth and the distinct expression of bacterial growth metabolism rates, as observed in the wolfberry pulp fermentation process.

The logistic equation is expressed as follows:

$ \dfrac{\text{1}}{\text{x}}\dfrac{\text{dx}}{\text{dt}}=\text{μ}\text{m}\left(\text{1}-\dfrac{\text{X}}{{\text{X}}_{\text{m}}}\right) $

(1)

At the commencement of fermentation (t = 0) and with the initial microbial population denoted as X = X_m, the integral deformation equation is substituted, yielding the following expression:

$ \text{X}=\dfrac{{\text{X}}_{\text{0}}{\text{e}}^{{\text{μ}}_{\text{m}}\text{t}}}{\text{1}-\dfrac{{\text{X}}_{\text{0}}}{{\text{X}}_{\text{m}}}\text{(}\text{1}-{\text{e}}^{{\text{μ}}_{\text{m}}\text{t}}\text{)}} $

(2)

In the formula, X₀ is the initial number of live lactic acid bacteria during growth / (10⁸ CFU/mL); X_m represents the highest viable count of lactic acid bacteria during the growth period/(10⁸ CFU/mL); μ_m is the maximum specific growth rate/h⁻¹, t denotes time in hours.

Upon converting Eqn (2) into a deformed form, simultaneous logarithmic transformation of both sides results in:

$ \text{ln}\dfrac{\text{X}}{{\text{X}}_{\text{m}}-\text{X}}={\text{μ}}_{\text{m}}\text{t}-\ln\left(\dfrac{{\text{X}}_{\text{m}}}{\text{X}}-\text{1}\right) $

(3)

Product generation kinetics model

In bacterial fermentation, the relationship between cell growth rate and product generation rate can manifest in three ways: coupled with bacterial growth, partially coupled, and non-coupled^[13]. The product generation rate does not perfectly align with any single model, introducing a degree of error. Consequently, the Leudeking-Piret equation is employed:

$ \dfrac{\text{dP}}{\text{dt}}=\text{α}\dfrac{\text{dX}}{\text{dt}}+\text{βX} $

(4)

In the formula, P represents the total acid concentration after fermentation, (g/L); X denotes the number of live bacteria, (10⁸ CFU/mL); T is the fermentation time, h; α is the product synthesis constant associated with bacterial growth; β is the product synthesis constant associated with bacterial volume.

In the context of lactic acid bacteria fermenting wolfberry pulp to produce acid, the process conforms to a partially coupled type, specifically α ≠ 0 and β ≠ 0. At this stage, the bacterial body is in a stable phase: dX/dt = 0, X = X_m, so that:

$ \text{β}=\dfrac{\text{dP}}{\text{dt}\times {\text{X}}_{\text{m}}} $

(5)

When taking t = 0 and P = 0 as the initial conditions, the integral results in:

$ \begin{split}&\rm P={\text α}A(t)+{\text β}B(t) \\&\text{A}\left(\text{t}\right)={\text{X}}_{\text{0}}\left[\dfrac{{\text{e}}^{{\text{μ}}_{\text{m}}\text{t}}}{\text{1}-\dfrac{{\text{X}}_{\text{0}}}{{\text{X}}_{\text{m}}}\left(\text{1}-{\text{e}}^{{\text{μ}}_{\text{m}}\text{t}}\right)}-\text{1}\right] \\& \text{B}\left(\text{t}\right)=\dfrac{{\text{X}}_{\text{m}}}{{\text{μ}}_{\text{m}}}\ln\left[\text{1}-\dfrac{{\text{X}}_{\text{0}}}{{\text{X}}_{\text{m}}}\left(\text{1}-{\text{e}}^{{\text{μ}}_{\text{m}}\text{t}}\right)\right] \end{split}$

(6)

Substrate consumption dynamics model

Throughout the fermentation process of lactic acid bacteria, the sustenance of normal physiological activities in cells necessitates specific substrates. The energy generated through substrate consumption serves both microbial growth and the production of new metabolites. The dynamics of substrate consumption can be effectively described using the Luedeking equation:

$ -\dfrac{\text{dS}}{\text{dt}}=\text{γ}\dfrac{\text{dX}}{\text{dt}}+\text{δX} $

(7)

In the formula, S represents the substrate concentration/(g/100 mL), X denotes the number of live bacteria/(10⁸ CFU/mL), T is time/h, γ and δ are substrate consumption parameters.

When the bacterial body is in a stable phase with dX/dt = 0 and X = X_m, the following can be derived from Eqn (7):

$ \text{δ}=-\dfrac{\text{dS}}{\text{dt}\;\text{×}\;{\text{X}}_{\text{m}}} $

(8)

After integration:

$\begin{split}& S=S_0-\gamma (t)-\delta D(t)\\&\text{C}\left(\text{t}\right)={\text{X}}_{\text{0}}\left[\dfrac{{\text{e}}^{{\text{μ}}_{\text{m}}\text{t}}}{\text{1}-\dfrac{{\text{X}}_{\text{0}}}{{\text{X}}_{\text{m}}}\left(\text{1}-{\text{e}}^{{\text{μ}}_{\text{m}}\text{t}}\right)}-\text{1}\right] \\& \text{D}\left(\text{t}\right)=\dfrac{{\text{X}}_{\text{m}}}{{\text{μ}}_{\text{m}}}\ln\left[\text{1}-\dfrac{{\text{X}}_{\text{0}}}{{\text{X}}_{\text{m}}}\left(\text{1}-{\text{e}}^{{\text{μ}}_{\text{m}}\text{t}}\right)\right] \end{split}$

(9)

Determination of chemical substances and antioxidant activity during fermentation

Determination of total phenolic and total flavonoids content

The estimation of total phenolic content was performed by slightly modifying the Folin-Ciocalteu procedure^[14]. To put it briefly, 1 mL of the sample, once diluted, was amalgamated with 2 mL of the Folin-Ciocalteu reagent (1:9, v/v). This was followed by the introduction of 2 mL of Na₂CO₃ solution (75 g/L). The blend was then left undisturbed in a dark environment at room temperature for 30 min. Post this incubation, the absorbance of the concoction was gauged at 760 nm.

The total flavonoid content (TFC) was evaluated using the AlCl₃ colorimetric method, as described by Wu et al.^[15]. Initially, 2 mL of the diluted phenolic extract was incubated with 0.25 mL of NaNO₂ solution at a concentration of 50 g/L for 5 min. Then, 0.5 mL of AlCl₃ solution, prepared at a concentration of 100 g/L, was added, followed by a further 5 min incubation. Subsequently, 1 mL of NaOH solution, with a concentration of 2 mol/L, was introduced and allowed to react for 10 min. The absorbance of the resulting solution was measured at 510 nm.

DPPH and ABTS radical scavenging rate
The DPPH radical scavenging activity was assessed using a modified protocol based on prior methods^[15]. A total of 0.4 mL of the appropriately diluted sample was combined with 9.6 mL of a methanolic DPPH solution (at a concentration of 20 mg/mL). The resulting solution was subsequently incubated at a consistent temperature of 37 °C in a light-restricted environment for exactly 30 min. Following this incubation period, the absorbance of the mixture was carefully measured at a target wavelength of 517 nm.

The ABTS radical scavenging activity was determined with slight modifications to previously described methods^[16]. The process commenced with the incubation of 2.45 mmol/L K₂S₂O₈ and 7 mmol/L ABTS in a 1:1 (v/v) ratio, maintained in a dark environment for 16 h to synthesize the ABTS radical cationic reagents. The subsequent step involved diluting the reaction mixture with 80% ethanol to obtain an absorbance of 0.70 ± 0.02 at a wavelength of 734 nm. Thereafter, a 0.6 mL sample was mixed with 5.4 mL of the ABTS radical cation solution, allowing for a 6 min reaction period. The absorbance of the mixture was then precisely measured at 734 nm. The outcome of this assay was expressed as the percentage of ABTS free radical inhibition.

Phenolic profiles
The samples were extracted three times by ethyl acetate, combined with organic phases, evaporated by a rotary evaporator, and then reconstituted with methanol for testing.

High-Performance Liquid Chromatography (HPLC) was utilized to determine the phenolic profiles, adhering to the methodology delineated in a prior study^[15]. The flow rate was set at 1 mL/min, and the detection was facilitated by a UV–visible spectrophotometer, monitoring at a wavelength of 280 nm. The quantification of the phenolic compounds was achieved by correlating the obtained peak areas with those of established external standards.

Phenolic profiles were quantified by HPLC according to previously reported method^[15]. The mobile phase, consisting of a 1% formic acid solution (referred to as solvent A) and acetonitrile (designated as solvent B), were combined according to a specific gradient elution scheme. This program was as follows: from the start to 5 min, the proportion of solvent B was maintained at 5%; from 5 to 25 min, it increased to 12%; from 25 to 40 min, the concentration rose to 30%; between 40 and 50 min, solvent B constituted 45% of the mixture; and from 50 to 60 min, the program returned to an initial 5% concentration of B. The column oven temperature was set at 30 °C and 10 μL of samples were injected into the sampler. Separation was carried out on a Symmetry C18 column (4.6 mm × 250 mm, 5 μm, Waters). The flow rate was set at 1 mL/min, and the detection was facilitated by a UV–visible spectrophotometer, monitoring at a wavelength of 280 nm. The quantification of the phenolic compounds was achieved by correlating the obtained peak areas with those of established external standards.

GC-IMS detection
The analysis of Volatile Organic Compounds (VOCs) was conducted using the FlavourSpec® analytical system (G.A.S., Dortmund, Germany)^[17]. The initial step involved the preparation of wolfberry pulp samples, where 5 g were precisely measured and deposited into a 20 mL headspace vial. This vial was then subjected to a thermal treatment at a temperature of 60 °C for 30 min to facilitate the release of VOCs. Following the incubation period, the samples were injected into the gas chromatography system using an injection needle heated to 85 °C, with a specified air volume of 500 μL at the top. The Gas Chromatography-Ion Mobility Spectrometry (GC-IMS) technique was subsequently employed to resolve the volatile components within the sample. The separation process occurred in a capillary column (MXT5, 15 m × 0.53 mm inner diameter). Nitrogen gas, with a purity level of no less than 99.999%, was chosen as the carrier gas. The flow rate of the carrier gas was programmed to initiate at 2 mL/min, which was sustained for the first 2 min. This rate was then incremented to 10 mL/min over 8 min, further increased to 100 mL/min within the subsequent 10 min, and ultimately raised to 150 mL/min in another 10 min. The ions resulting from the analytical process were directed into a drift tube, which was maintained at a temperature of 45 °C. The drift gas, set at a flow rate of 150 mL/min, facilitated the ion mobility within the drift tube, thereby completing the VOC assessment procedure.

Statistical analysis
Sample preparation and analysis were conducted in triplicate to ensure consistency. Data were displayed as Mean ± SEM and processed using Origin 2022 software (Origin Lab, China). Statistical analysis was carried out via one-way ANOVA, with a p-value less than 0.05 indicating statistical significance. HS-GC-IMS data were extracted through the GC-IMS library retrieval method, and a bi-dimensional cross-qualitative approach was employed for qualitative analysis.

Conclusions

This study demonstrated the substantial impact of lactic acid bacteria fermentation on the flavor, chemical characteristics, and antioxidant activity of wolfberry pulp. Lab fermentation significantly increased the content of total phenols and flavonoids in wolfberry pulp (p < 0.05), subsequently enhancing its antioxidant activity with a positive correlation. The alterations in volatile aroma components in wolfberry pulp before and after fermentation were scrutinized using HS-GC-IMS. The findings revealed that lab fermentation augmented various aldehydes, ketones, and esters, introducing novel flavors like sourness and fruitiness to the fermented wolfberry pulp. Concerning fermentation efficiency, the addition of galactooligosaccharides expedited the fermentation process of wolfberry pulp, elevating the production of total acids and yielding a more favorable fermentation outcome. In summary, this study unveiled the fermentation kinetic model of L. plantarum CCFM1050 on wolfberry pulp with galactooligosaccharides. It concluded that lactic acid fermentation could enhance the flavor and functional properties of wolfberry pulp, offering insights for its advanced processing and potential guidance for the future development of the wolfberry industry.

Author contributions

The authors confirm contribution to the paper as follows: conceptualization, funding acquisition: Peng Q; investigation: Liu H, Wang Y, Chen T; methodology: Liu H, Li N; data curation, formal analysis, draft manuscript preparation: Liu H; validation, software: Li N; resources, supervision, manuscript revision & editing: Yang H, Peng Q. All authors reviewed the results and approved the final version of the manuscript.

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Phytochemicals	1	2	3	4	5
Gallic acid	3.49 ± 0.74^c	4.74 ± 0.38^b	4.87 ± 0.30^b	7.76 ± 0.02^a	7.92 ± 0.28^a
Catechin	33.79 ± 4.83^b	37.70 ± 2.76^a	39.95 ± 3.87^a	42.36 ± 2.01^a	42.31 ± 2.78^a
p-Coumaric acid	5.32 ± 0.46^b	23.28 ± 0.81^a	21.09 ± 1.06^a	5.27 ± 0.55^b	5.37 ± 0.13^b
Chlorogenic acid	36.63 ± 10.11^c	109.29 ± 3.87^b	107.56 ± 3.95^b	165.56 ± 4.08^a	159.04 ± 8.58^a
Caffeic acid	2.68 ± 0.68^ab	1.39 ± 0.81^b	4.30 ± 0.79^a	4.57 ± 0.99^a	3.11 ± 0.54^ab
Ferulic acid	5.97 ± 0.25^c	8.12 ± 0.80^ab	8.37 ± 0.82^a	7.45 ± 0.41^abc	6.55 ± 0.26^bc
Rutin	208.09 ± 19.27^b	311.27 ± 41.04^ab	263.13 ± 16.56^ab	361.47 ± 23.15^a	265.70 ± 60.17^ab
Quercetin	41.60 ± 1.09^c	39.93 ± 1.76^c	38.88 ± 0.38^c	58.21 ± 1.88^a	53.29 ± 1.79^b
Values with different superscripts in the same row have significant differences (p < 0.05). Among them: without any processing (control) (1); after enzymatic hydrolysis (2); add prebiotics (3); fermentation without added prebiotics (4); adding prebiotic fermentation (5).

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Study on fermentation kinetics, antioxidant activity and flavor characteristics of Lactobacillus plantarum CCFM1050 fermented wolfberry pulp

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Study on fermentation kinetics, antioxidant activity and flavor characteristics of Lactobacillus plantarum CCFM1050 fermented wolfberry pulp