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. 2021 Feb 21;58(8):3235–3242. doi: 10.1007/s13197-021-05018-3

In-vitro biotransformation of tea using tannase produced by Enterobacter cloacae 41

Rasiravathanahalli Kaveriyappan Govindarajan 1,2,✉, Chartchai Khanongnuch 2,✉, Krishnamurthy Mathivanan 3, Douglas J H Shyu 4, Kanti Prakash Sharma 5, Surajit De Mandal 6
PMCID: PMC8249508  PMID: 34294986

Abstract

Tannase is a widely used enzyme that improves the quality of tea by facilitating the release of water-soluble polyphenolic compounds, as well as reduces the formation of tea creams. The microbial tannase enzymes are often employed for tea biotransformation by hydrolyses esters of phenolic acids, including the gallated polyphenols found in blacks teas. The study was focused to investigate the tannase enzyme mediated biotransformation of black tea such as CTC-(Crush, tear, curl) & Kangra orthodox which are commonly used by the south Indian peoples. HPLC spectral analysis revealed that tannase treatment on tea cream formation (CTC & Kangra orthodox tea) allows the hydrolysis of the EGC, GA, ECG, and EGCG. A significant reduction in the formation of tea cream and increased antioxidant activity has been observed in the CTC (1.62 fold) and Kangra orthodox (1.55 fold). The results revealed that tannase treatment helps to improve the quality of black tea infusions with respect to cream formation, the intensity of colour, and sensory characteristics of tea. The result of this study indicates that E. cloacae 41 produced tannase can be used to improve the quality of both tea samples.

Keywords: Enterobacter cloacae 41, Tannase enzyme, CTC, Kangara orthodox, HPLC, DPPH

Introduction

Over the last several decades, peoples are using various types of drinks especially black tea is one of the most famous beverages worldwide (Li et al. 2017). Tea contains several polyphenolic compounds like flavanols as well as flavonoids, and glycosides which reduce the incidence of chronic diseases in humans (Balentine et al. 1997; Yang et al. 2011). These polyphenolic compounds are also known to possess several beneficial properties such as a anti-oxidant, anti-tumor, anti-aging and anti-inflammatory and neurological protective activities (Conde et al. 2015; Xu et al. 2019). The DPPH activity of black tea depends on the redox properties of the phenolic secondary compounds, which is allow them to act as reducing complex agents, single-oxygen condensers, singlet-oxygen quenchers, and heavy elements and surfactant (Macedo et al. 2011; Roy et al. 2018; Fang et al. 2019). However, studies based on clinical reports and invivo model have shown that depsite the proven antioxidant power of secondary polyphenolics, majorly these know compounds, particularly esters, and glycosides bonds, is not absorbed by oral administration (Athar et al. 2007; Mahmoud et al. 2018).

Tannase, also known as tannin acyl-hydrolase (TAH) (E.C 3.1.1.20) is an extracellular hydrolytic enzyme that catalyzes the hydrolysis and synthesis of depside bonds of hydrolysable tannins (tannic acid substrate) and facilitating the release of gallic acid as well as glucose (Govindarajan et al. 2019; Shao et al. 2020). The importance and utility of tannase enzymes have been gaining significance since the eighteenth century, resulted in several reports and a wide range of applications. Depending on the habitat, bacteria and fungi produce a variety of tannase enzymes that have been applied in different fields, including processing tea, beer, fruit juices, and alcoholic beverages product (Unban et al. 2020). Tannase is a crucial enzyme for modifying the structure of tea catechins and thereby improving the quality and bio-activities of tea. Tea treated with tannase showed higher antioxidant properties than typical black tea due to the effective inhibition of nitrosamines, which are caused by carcinogenic and mutagenic etc., It also enhances the color durability and organoleptic properties and increases cellular uptakes of tea catechin (Sherief et al. 2011; Govindarajan et al. 2016).

Tannase hydrolyzes the Epicatechin gallate (ECG) and Epigallocatechin-3-gallate (EGCG) into Epigallocatechin (EGC), Epicatechin (EC) (Naidu et al. 2010). These hydrolyzed products have high antioxidant activity by scavenging of free radicals. Generally, the radical scavenging activity of bio-transformed tea increases with increasing concentration of water-soluble secondary metabolites such as ECG and GA (Raghuwanshi et al. 2011; Macedo et al. 2012; Ong & Mohamad Annuar, 2017; Liu et al. 2017). It has been reported that bacterial species such as Lactobacillus plantarum, L. paraplantarum, Enterobacter cloacae and Pseudomonas aeruginosa, Listeria monocytogenes can produce tannase enzyme and catalyze tea catechins (Beniwal et al. 2013; Kanpiengjai et al. 2020). In our previous study, we have isolated the strain Enterobacter cloacae 41 and evaluated their tannase producing capability. In particular, this strain produced tannase more efficiently than other tested tannase producing bacterial strain (Govindarajan et al. 2019; Kanpiengjai et al. 2019). In the present study, we explore the roles of tannase produced by strain E.cloacae 41 in the biotransformation of tea samples such as (ctc and kangra orthodox). Further, the antioxidant potential of the tannase mediated biotransformed tea was also evaluated. Tannase is a crucial enzyme for modifying the structure of tea catechins and thereby improving the quality and bio-activities of tea.

Material and methods

Tannase production

Tannase producing bacterial strain Enterobacter cloacae 41 was used in this study which was isolated from insect gut microbes in our previous study (Govindarajan et al. 2019). Tannase production was performed by inoculating the bacterial strain E. cloacae 41 in a basal media [(g/l) 0.5 g CaCl2,; 0.5 g KH2PO4,; 2.0 g NaNO3, and 2.0 g MgCl2,] containing 12 g/l tannin as a carbon source and incubated for 24 h at 37 °C at the end of incubation, the bacterial culture was centrifuged at 4 °C, and the culture supernatant through filtered an 0.22 μm membrane filter and the filtrate was assayed for the enzyme activity.

Tannase assay

The tannase activity was analyzed according to the standard spectrophotometric methods (Govindarajan et al. 2019). One unit (U) of enzyme activity is defined as the amount of the enzyme that catalyzes the reaction of 1 mM of substrate 1 min/under assay condition.

Preparation of black tea infusion and enzymatic treatment

Both black tea samples (each 1 g) were combined with the 100 ml of sterilized distilled double water and the black teas were incubated with 85 °C for 20 min (Lu and Chen, 2008). In each case, black tea infusions obtained were filtered through filter membrane and the filtrate was examined in order to know the contents of the individual catechins. The filtrate derived from the tea infusion of both tested tea samples was incubated with tannase enzyme at 30 °C, for 1 h, and the hydrolysis process was stopped by placing the reaction kept in cold conditions for 15 min.

Cream formation from ctc, kangra orthodox samples

Both treated and non-treated black tea samples were centrifuged at 10,000 rpm for 25 min at 8 °C. The precipitate was collected and dried in a hot air oven at 100 °C till standard weight is obtained. The weight obtained for tea precipitate in 100 ml of cream infusion, was expressed as g/100 ml.

Liquid colour measurement analysis

The colour measurement of tea liquid sample (L*, a*, b*) was determined using Konica Minolta CR-300 chromo meter (Bayram and Kaya, 2018). The reading was follows given below.

L*, represents the darkest black at L* = 0, and the brightest white at L* = 100.

A* value: (+ red), (–green), b* value: (+ yellow), (–blue).

Sensory evaluation of the treated tea sample (CTC and Kangra orthodox)

The organoleptic properties of the treated tea (ctc and kangra orthodox) samples were determined by a test panel consisting of 50 volunteers (25 men and 25 women) selected between the ages group of 20 to 60 years. The sensory evaluation was performed with the addition of ~ 1 g of each sample to 100 ml of boiling water in a teapot and applying different time duration (5, 10 and 15 min). The samples (treated and controlled) were evaluated for the following characteristics: overall appearance, quality, flavor, taste, after taste, and overall accepted. All these experiments were compared with the control sample.

Quantification of ctc and kangra orthodox tea by HPLC

A 20 µl tested samples (100 × dilutions) using a Millipore filter, type FH (pore size 0.5 µm) was from Millipore Pvt. Ltd. India, and were injected into an HPLC equipped with a C18 column (150 × 4.6 mm, 5 µm) and UV detector for analysis of (EGC), GA), (ECG) and (EGCG). The tested sample were eluted with a gradient system consisting of solution A [methanol/formic acid/distilled water (9:5:90.5v/v)] and solvent B [methanol/formic acid/distilled water (80:5:18v/v)] delivered at flow rate of 1 ml/min with UV detection at 270 nm. The gradient was run from 0 to 35% solvent B in 30 min, and the column temperature was maintained at 30ºC. The concentration of polyphenolic compounds was determined by using external calibration curves of the standard compounds at various concentrations.

DPPH radical scavenging effects

Using the standard procedure described by Turkmen et al. (2006), the biotransformed black tea samples obtained after enzymatic reaction were subjected to antioxidant assays with slight modification. Test samples and DPPH working solution were mixed and incubated at 25 °C. Further, the reaction mixture was incubated in a dark place for 30 min at room temperature. Distilled water used as a control for this experiment. The absorbance was determined at 520 nm by using the Shimadzu UV-2450 UV–Vis spectrophotometer. All analysis was run in triplicate and the values were averaged. DPPH was expressed as the inhibition percentage and follow the standard formula.

Antiradical activity%=Control absorbance-Sample absorbancex 100Control absorbanceControl absorbance

Data analysis

The tests were performed in three independent tests, and data were presented as mean ± standard deviation (SD). The statistical analysis was performed with SPSS-19.0 and statistical analysis was carried out using one-way ANOVA, determine the significance of difference for each test, with statistical significance at p < 0.05 are presented.

Result and discussion

Evaluation of tea cream formation

The decrease in the cream formation of tea helps to supply turbidity-free, ice water-soluble instantaneous tea that is more acceptable to the tea buyer and seller. It has been reported that addition of free enzymes was helpful to decrease the turbidity of black tea (Boadi and Neufeld, 2001). According to Table 1, the results showed the reduction of cream formation was observed in the CTC. CTC is an abbreviation of Crush, tear, and curl. Kangra orthodox is a Palampur, municipal council in Kangra district (Kangra valley) in the Indian state of Himachal Pradesh. In this study, the tea infusion was treated with various concentrations of tannase enzyme obtained from the bacterial strain Enterobacter cloacae 41. The tea cream was treated with different concentrations (0.05–0.2%) of tannase enzyme against control. The result showed that E.cloacae 41, at an optimal concentration of 0.1% tannase enzyme could carry out efficiently reduction in cream formation up to 84.25% (0.124 g) in CTC and 80.2% (0.091 g) in Kangra orthodox tea against control (tannase free tea cream), wherein 0.520 and 0.390 g of tea cream formation was observed in 100 ml of the reaction medium, respectively. However, the further increase in enzyme concentration beyond 0.1% did not support the significant decrease in tea cream formation (Table 1). Similarly, Lu et al. (2009) had also reported that a reduction in tea cream formation was observed with increasing the at similar concentration from 0.9 to 0.2 g. The obtained results were compared with the previously reported findings of Chandini et al. (2011) and where they proved that tannase enzyme from Aspergillus hetromorphous MTCC 5466 could reduce the tea cream formation by 65–72%.

Table 1.

Effect of tannase concentration on cream formation in tea (Mean ± SD)

Tannase concentration (%) CTC tea cream formation (g/100 mL) Kangra orthodox tea cream formation in (g/100 mL)
Control (without enzyme) 0.520 ± 0.013 0.390 ± 0.009
0.050 0.415 ± 0.00d 0.219 ± 0.00c
0.075 0.250 ± 0.013c 0.141 ± 0.019b
0.100 0.124 ± 0.00b 0.091 ± 0.00a
0.150 0.089 ± 0.00a,b 0.085 ± 0.00a
0.175 0.079 ± 0.00a 0.079 ± 0.001a
0.200 0.075 ± 0.00a 0.067 ± 0.00a
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Different letter denotes statistically (at p < 0.05) significance of tannase enzyme concentrated with CTC, Kangra orthodox tea samples treatment

Colour measurement analysis

The color measurements of liquid sample are shown in Table 2. L* values of tea liquid different between 2.57 ± 0.00a & 4.67 ± 0.00a. L* values of the liquid production with 6% tea concentration and 3 days extraction was more than higher the L* values of the other liquid sample. Difference in L* values of liquid produced in 2% tea sample concentrations and 3 days extraction duration were does not found to be considerable. Therefore, the difference in L* values of liquid by 4, 6% tea concentration and 3 days extraction was found to be significant. In addition, the difference in L* values of liquid with 2, 4 and 6% ratios of tea and 3 days extraction were considerable in themselves. The a* values [red ( +), green (–)] of liquid different between 12.08 ± 0.02c and 12.62 ± 0.01c. The positive ( +) a* value indicated with red colour and a negative (–) a* value indicates green colour. A difference in a* values of all liquid produced with various tea concentration and extraction duration no found to be significant. Therefore, high tea ratios and short extraction duration not have significant effects on a* values of liqueur tea samples. The b* values [yellow ( +), blue (–)] of liqueurs different between 4.18 ± 0.01b & 6.71 ± 0.01b. The b* values of the liqueur production with 2% kangra orthodox tea concentration and 3 days extraction were have higher b* value than the other tea liqueur samples. A positive ( +) b* value indicates yellow color and a negative (–) b* value indicates blue color. Therefore, the b* ( +) value indicates that there is a few yellow color presented.

Table 2.

The color measurement of liquid tea samples from CTC and Kangra orthodox (Mean ± SD)

Liquid tea concentration CTC tea Kangra orthodox tea
2% 4% 6% 2% 4% 6%
Extraction 3 days 3 days
L* 2.57 ± 0.00a 3.35 ± 0.01a 4.21 ± 0.02a 2.61 ± 0.01a 3.54 ± 0.00a 4.67 ± 0.00a
a* 12.62 ± 0.01c 12.18 ± 0.00c 11.89 ± 0.00c 13.51 ± 0.02c 13.12 ± 0.02c 12.08 ± 0.02c
b* 4.18 ± 0.01b 7.12 ± 0.01b 5.57 ± 0.10b 8.21 ± 0.02b 6.76 ± 0.03b 6.71 ± 0.01b
F values 582.23 262.15 294.64 362.26 345.54 586.32
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Different letters in the same row indicate significant differences between different tea concentrations

Sensory evaluation of ctc and kangra orthodox tea samples

The sensory quality of the tea is regarded as a vital factor since it influences the overall quality of the tea. These characteristics are also important in the product development process. in this study, a panel of 50 volunteers was participated to carry out the sensory test of the beverage, and the results were presented in Fig. 1. It indicated that both tea samples treated with tannase were higher acceptability in terms of flavor (overall), taste, after taste, overall acceptability and appearance. The finding of this study is comparable with results from published studies by Ivanisova et al. (2020) where they were reported that the enzyme-treated kangra orthodox tea beverages have an acidic and satisfying taste. Similarly, Neffe-Skocinska et al. (2017) indicated the higher acceptability of treated tea in terms of the sensory characteristics. These results indicated that the quality of both tea samples was improved after treatment with tannase enzyme.

Fig.1.

Fig.1

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Sensory evaluation of CTC and Kangra orthodox tea sample (sum of all evaluators) the significant variance (one-way ANOVA, p < 0.05) is designated by various letter and Error bars suggest ± SE”

HPLC analysis of tea compounds

Tannase are inducible enzymes involved in the biotransformation of polyphenolic compounds. HPLC analysis indicated that polyphenolic compounds, namely EGCG, and ECG, were thought to be hydrolyzed to de-gallated catechins (EGC or EC), and such as alteration was maximized in 2 h. This changes in the composition of the black tea extraction is due to the enzymatic action, which cleave the ester, depside bonds (EGCG/ECG) and Gallic acid (GA). In this study, both the treated (bio-transformed) and untreated both tea sample was analyzed for catechins molecules using HPLC chromatogram. In tannase treated with tea sample cream formation, a higher concentration of EGC and ECG along with an increasing GA concentration was compared with a tannase free infusion tea samples. Figure 2, 3 indicates the rising in the peak of the EGC, GA, ECG, and EGCG in the treated tea samples. A part of the residual (EGCG) forms complex with caffeine. Hence, the supply of the free morpheme of caffeine is decreased within the tea samples. Garcia-Conesa et al. (2001) showed that tannase present in Aspergillus oryzae could hydrolyze the ester bonds of the natural substrates (Garcia-Conesa et al. 2001). Traditionally tea usually contains four major types of catechins, EC, (–)-ECG, (–)-EGC, and (–)-EGCG. The EGCG constitutes 70% of the catechins (Perva-Uzunalic et al. 2006). The enzymatic reaction improved the contents of non-ester catechin like EGC and EC and decreased the content of ester molecules (EGCG and ECG). Ester catechins are the source of the bitter taste in tea infusion (Li et al. 2017).

Fig. 2.

Fig. 2

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HPLC spectra shows the changes in the content of individual catechins before and after enzymatic hydrolysis of CTC tea infusion a CTC tea (control, b Bio-transformed CTC tea shows peaks of EGC Epigallocatechin, GA Gallic acid, ECG Epicatechin gallate, EGCG Epigallocatechin-3-gallate

Fig. 3.

Fig. 3

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HPLC spectra shows the changes in the content of individual catechins before and after enzymatic hydrolysis of black tea infusion a Kangra orthodox tea (control), b Biotransformed Kangra orthodox tea shows peaks of EGC Epigallocatechin, GA Gallic acid, ECG Epicatechin gallate, EGCG Epigallocatechin-3-gallate

DPPH analysis of the biotransformed tea samples extract

Tea is considered a good source of antioxidant compounds and protects against different chronic diseases, including cancer (Forester et al. 2011). It has been reported that the biotransformed tea extract mediated by various micro-organisms acquire high antioxidant activity than non-treated catechins or tea extracts molecules (Chaiwut et al. 2019). Therefore, the tea catechins were treated with E. cloacae 41 to evaluate the antioxidant potential of the biotransformed tea extracts. The biotransformed black tea samples are obtained after tannase enzymatic reactions were subjected to the antioxidant activity assay and was determined based on the percentage of inhibition of the DPPH radical as depicted in Fig. 4. Results showed that the tea samples incubated with crude enzyme exhibited higher radical-scavenging activity compared to the non-treated tea samples. The biotransformed both tea infusion has 57.8% and 69.5% free radicals-scavenging activity which was greater than the enzyme-free tea infusion samples, which show 35.6% (ctc tea), 44.8% (kangra orthodox tea) scavenging activity. Antioxidant activity increased by 1.622- and 1.55-fold for ctc and kangra tea samples, respectively. This indicated the significance of the tannase enzyme present in E. cloacae 41 towards the improvements of the antioxidant potential of the tested tea (ctc and kangra orthodox) samples. This could be due to the hydrolyzed product of the substrate presents in the tested tea samples that contribute to the increase of the antioxidant properties of tea. The results of this study is similar to those reported by Pure and pure, (2016), who found the high scavenging activity (15.65%) in the fermented tea samples than the non-fermented black tea (26.16%). According, to Battestin et al. (2008), tannase can completely hydrolyze the epigallocatechin gallate (ECG) in black tea to epigallocatechin (EGC), gallic acid (GA), epicatechin gallate and epigallocatechin-3-gallate (EGCG) by increasing the scavenging activity of tea samples. Hence, the present study suggested that the Enterobacter cloacae 41 tannase was able to hydrolyze the natural tannic acid substrate ester bonds and release byproduct gallic acid and glucose. The degalloylation of the gallate (Epi-gallocatechin gallate) present in the ctc and kangara orthodox tea samples can form epigallocatechin and gallic acid.

Fig. 4.

Fig. 4

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Antioxidant activity of control and biotransformed black by DPPH assay. The significant variance (one-way ANOVA, p < 0.05) is designated by various letter and Error bars denotes SE

Conclusion

In this study, the biotransformation of tea infusion using tannase produced by E. cloacae 41 was studied. The colour and sensory evaluation showed that the prepared beverages were fresh sour fruity taste. In addition, our findings could also valuable for the extension of the existing application of bacterial enzymes about improving the tea colour to better quality, and flavor strength. Furthermore, HPLC analysis of treated and non-treated tea polyphenolic compounds showed that different compounds (EGC, GA, ECG and EGCG) were found and both tea leaves had higher polyphenolic contents which improved higher the quality of tea. Tea concentration of the stronger antioxidant activity and reducing power assay. Therefore, it appears reasonable to conclude that our reports may be useful in extending the existing tannase application in relation to the improvement of black tea.

Acknowledgement

The authors would like to thank Division of Biotechnology, School of Agro-Industry, Faculty of Agro-Industry, Chiang Mai University, for their facilities. We also acknowledge to Science and Technology Park, Chiang Mai University, Thailand.

Author contributions

RKG: Supervision, Resources, Investigation, Formal analysis, Methodology, Writing–original draft. CK: Supervision, Resources, Investigation, Formal analysis, Methodology, Writing–original draft. KM: Writing–review & editing, Data curation, Writing–original draft. DJHS: Methodology, Software, Validation. Formal analysis. KPS and SM: Data curation, Methodology, Validation.

Funding

No funds, grants, or other support was received.

Code availability

Not applicable.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Ethics approval

Author does not use any ethics approval.

Consent to participate

All authors of the manuscript have consented to submission.

Consent for publication

The author has consented to the submission of the research report to the journal.

Availability of data and material

The data that support the findings of this study are available from the corresponding author upon reasonable request.

Footnotes

Publisher's Note

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Contributor Information

Rasiravathanahalli Kaveriyappan Govindarajan, Email: biogovindarajan@gmail.com.

Chartchai Khanongnuch, Email: chartchai.k@cmu.ac.th.

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