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Kombucha Tea: Metabolites

  • Rasu JayabalanEmail author
  • Radomir V. Malbaša
  • Muthuswamy Sathishkumar
Living reference work entry
Part of the Reference Series in Phytochemistry book series (RSP)

Abstract

Kombucha, fermented black tea with symbiotic association of bacteria and yeast, has been claimed by its drinkers for several health benefits. Health benefits of kombucha tea are directly associated with the composition and the concentration of the biomolecules present in it. Being a product fermented by bacteria and yeast association, kombucha has very complex composition which has a range of components from tea plant, bacteria, yeast, and compounds produced during fermentation process. The compounds responsible for the claimed benefits of kombucha have not been explored due to its complexity. This chapter focuses on the metabolites of kombucha which have been reported.

Keywords

Acetic acid bacteria Cellulose pellicle Fermentation Fermented tea Kombucha Kombucha tea Medusomyces gisevii Symbiotic culture Tea beverage Tea fungus Tea fermentation Yeast 

1 Introduction

Kombucha tea is a slightly sweet, slightly acidic refreshing beverage consumed worldwide, obtained by the fermentation of sugared tea by a symbiotic association of bacteria and yeasts, forming “tea fungus” [1]. The tea fungus broth is composed of two portions, a floating cellulosic pellicle layer and the sour liquid broth (Fig. 1). This refreshing beverage tasting like sparkling apple cider is often produced in the home by fermentation using a tea fungus passed from home to home. Black tea and white sugar are the best substrates for the preparation of kombucha, although green tea can also be used. Tea fungus is a best example of biofilm made by symbiotic association of acetic acid bacteria and yeasts. The association of Kombucha with human was reported to be since BC, but the exact details about the origin are unclear. Details about the invention of tea fungus are also missing in the history. Kombucha tea is prepared by inoculating the tea fungus culture into cooled sugared tea decoction along with some amount of previous batch of fermented tea and allowing fermenting in dark for 7–14 days. During fermentation, the pH reduces drastically due to production of organic acids from added sugar due to yeast and bacterial metabolism. Tea polyphenols undergo degradation or transformation by the enzymes of bacteria and yeast which was evident by changes in color of the black tea during the course of fermentation. Various enzymes have been reported to be active in kombucha tea. Tea fungus is basically cellulose network where bacteria and yeast cells are attached which finally appears as a jelly membrane. The thickness of this biofilm is due to the deposition of cellulose as layer by layer during fermentation time. Reports about the first use of tea fungus, its formation for the first time, and inventor details are missing in the history. Kombucha has been reported continuously by scientific community and users for its health benefits. Composition and the concentration of the metabolites available in kombucha after the required time of fermentation would be the sole reason for the health benefits claimed. Kombucha has a range of metabolites originated from tea plant, bacterial metabolism, yeast metabolism, sugar, and the biotransformed compounds produced during fermentation which makes it very complex to study even by the state-of-the-art instruments [2]. It is surprised to see in the literature that there were very less attempts taken to reveal the complex composition of kombucha tea. As an initiative to achieve this, the present chapter focussed to review the metabolites already reported in the literature.
Fig. 1

Kombucha black tea having fermented broth and tea fungus (Reproduced with prior permission, Jayabalan et al. [2])

2 Kombucha Tea Preparation

Kombucha tea is traditionally prepared by freshly making sugared tea decoction and inoculating the portion of tea fungus and previously fermented kombucha. The preparation will be covered with paper towel or cheese cloth and will be kept for fermentation in dark at room temperature for 7–14 days. After fermentation, the fermented beverage will be separated from the newly formed tea fungus and filtered through cheese cloth. The filtered beverage will be refrigerated and consumed whenever required. The traditional preparation was subjected to different modifications based on the taste of kombucha drinkers. The modification lies in the amount of sugar , amount and types of tea substrate , time taken for preparing the tea decoction , period of fermentation, amount of inoculum, and fermentation temperature [2].

3 Beneficial Effects of Kombucha Tea

Kombucha tea has been claimed to have several beneficial effects on human health by the kombucha drinkers from all over the world. Except few, reported effects on human health are yet to be studied scientifically. Reported effects of kombucha from tea drinkers’ testimony and Russian researchers are to [3]:
  • Detoxify the blood

  • Reduce cholesterol level

  • Reduce atherosclerosis by regeneration of cell walls

  • Reduce blood pressure

  • Reduce inflammatory problems

  • Alleviate arthritis, rheumatism, and gout symptoms

  • Promote liver functions

  • Normalize intestinal activity, balance intestinal flora, and cure hemorrhoids

  • Reduce obesity and regulate appetite

  • Prevent/heal bladder infection and reduce kidney calcification

  • Stimulate glandular systems

  • Protect against diabetes

  • Increase body resistance to cancer

  • Have an antibiotic effect against bacteria, viruses, and yeasts

  • Enhance the immune system and stimulate interferon production

  • Relieve bronchitis and asthma

  • Reduce menstrual disorders and menopausal hot flashes

  • Improve hair, skin, and nail health

  • Reduce an alcoholic’s craving for alcohol

  • Reduce stress and nervous disturbances and insomnia

  • Relieve headaches

  • Improve eyesight

  • Counteract aging

  • Enhance general metabolism

4 Biochemical Composition of Kombucha Tea

Several scientific investigations published in the last 15 years have reported the presence of several metabolites in kombucha tea. The composition of kombucha tea, what is known today, is given in Fig. 2. All the analysis carried out to explore the biochemical composition was done in static mode. The biochemical composition of tea fungus and kombucha tea was not similar in all the reports. This might be due to the fact that the microbial composition of tea fungus varies with region and country. Hence, the metabolites produced by the bacteria and yeasts also vary which reflects in the chemical composition of kombucha tea. The difference in composition may also be due to the differences in amount of sugar and tea substrate, differences in the amount of tea fungus and kombucha tea used as inoculum, and difference in fermentation time. However, uniform trends of change in some property have been discussed by most of the researchers. For example, reduction in pH, increase in content of organic acids , and initial increase and intermittent decrease in concentration of bacteria and yeast cells in tea broth were observed by many researchers around world irrespective of the above mentioned differences. Few reports have also revealed the trend of increase in antioxidant activity throughout the fermentation time. Considering the contents of the biomolecules present in kombucha, an intermittent increase and decrease during fermentation time was observed for most of the compounds studied. Table 1 lists out the concentration of metabolites measured in kombucha tea [2].
Fig. 2

Biochemical composition of kombucha tea

Table 1

Predominant components in kombucha tea at the end of the fermentation on sugared black tea infusion (Reproduced with prior permission, Jayabalan et al. [2])

Component

Component content (g/L)

Initial sucrose (%)

Black tea

Fermentation temperature (°C)

Fermentation time (days)

Acetic acid

8

10

2 bags

24 ± 3

60

 

4.69

10

12 g/L

24 ± 3

18

Glucuronic acid

0.0031

5

1.5 g/L

28

21

 

0.0026

7

1.5 g/L

28

21

 

0.0034

10

1.5 g/L

28

21

 

1.71

10

12 g/L

24 ± 3

18

Gluconic acid

39

10

2 bags

24 ± 3

60

Glucose

179.5

7

1.5 g/L

28

21

 

24.59

7

1.5 g/L

28

21

 

12

10

2 bags

24 ± 3

60

Fructose

76.9

7

1.5 g/L

28

21

 

5.40

7

1.5 g/L

28

21

 

55

10

2 bags

24 ± 3

60

Remaining sucrose

192.8

7

1.5 g/L

28

21

 

11

10

2 bags

24 ± 3

60

 

2.09

7

1.5 g/L

28

21

5 Sugar

Kombucha drinkers use only table sugar (sucrose ) for the preparation and hence the scientific analysis. One molecule of alpha-d-glucose and beta-d-fructose linked by an alpha-1,4-glycosidic bond make one molecule of a disaccharide, sucrose. Hydrolysis of alpha-1,4-glycosidic bond releases equimolar mixture of glucose and fructose. During kombucha fermentation, the yeast cells from the initial inoculum hydrolyse sucrose to glucose and fructose by producing invertase or sucrase enzyme (beta-fructofuranosidase, EC 3.2.1.26). Due to its broad range in acidic pH (3.5–5.5), invertase activity is not inhibited by acids produced during kombucha fermentation, and hence the added sucrose is continuously hydrolysed to glucose and fructose.
$$ \mathrm{Sucrose}\ \left({\mathrm{C}}_{22}{\mathrm{H}}_{12}{\mathrm{O}}_{11}\right)\overset{\mathrm{Yeast}\ \mathrm{Invertase}}{\to}\mathrm{Glucose}\ \left({\mathrm{C}}_6{\mathrm{H}}_{12}{\mathrm{O}}_6\right)+\mathrm{Fructose}\ \left({\mathrm{C}}_6{\mathrm{H}}_{12}{\mathrm{O}}_6\right) $$
Yeast cells consume most of the fructose released by invertase action through glycolysis and convert them to ethanol and carbondioxide. The produced ethanol is rapidly oxidized to acetic acid by acetic acid bacteria present in the consortium. Acetic acid is the predominant organic acid produced during fermentation and the main reason for the pH decrease. Acetic acid bacteria also oxidizes glucose to gluconic acid [2].
$$ \mathrm{Fructose}\ \left({\mathrm{C}}_6{\mathrm{H}}_{12}{\mathrm{O}}_6\right)\overset{\mathrm{Yeast}\ \mathrm{Glycolysis}}{\to}\mathrm{Ethanol}\ \left({\mathrm{C}\mathrm{H}}_3{\mathrm{C}\mathrm{H}}_2\mathrm{O}\mathrm{H}\right)+\mathrm{Caron}\ \mathrm{dioxide}\ \left({\mathrm{C}\mathrm{O}}_2\right) $$

6 Cellulose

Cellulose is a homopolysaccharide composed of beta-d-glucose monomers linked by beta 1,4-glycosidic bond. Cellulose is the predominant material found in tea fungus and is produced by aerobic acetic acid bacteria found in its consortium. Acetic acid bacteria found in the air–liquid interface of the vessel used to produce kombucha produces cellulose biofilm in direct contact with oxygen to protect themselves from the high stressful growth conditions due to the presence of high concentration of acetic acid or ethanol [4]. Biofilm production by acetic acid bacteria is reported to be through cell–cell communication via quorum-sensing signaling [5]. Synthesis of cellulose involves the synthesis of uridine diphosphoglucose (UDPGlc) by UDPGlc pyrophosphorylase which were later polymerized into long and unbranched chains through beta-1,4-glycosidic bond by cellulose synthase enzyme. However, the conversion of glucose to UDPGlc requires two more additional steps which converts initial glucose molecules to glucose-6-phosphate by glucose kinase and then to glucose-1-phosphate by phosphoglucomutase (Scheme 1). It is also possible to produce cellulose through fructose by its conversion to glucose-6-phosphate through successive actions of fructose kinase and phosphoglucose isomerase enzymes. But fructose may not be available to acetic acid bacteria due to the action of yeast cells. Only part of the cellulose would be available for cellulose synthesis since glucose is also oxidized to gluconic acid by acetic acid bacteria. Both gluconic acid production and cellulose synthesis requires the presence of oxygen and this is the reason why cellulose layer formation occurs only at the air–liquid interface of the kombucha fermentation vessel [2].
Scheme 1

Formation of gluconic acid and cellulose from cellulose

Bacterial cellulose prepared from pellicles of A. xylinum (Gluconacetobacter xylinus) is a unique biopolymer in terms of its molecular structure, mechanical strength, and chemical stability [11]. A similar cellulose network floating on the surface of various fruit juices fermented by a symbiotic culture composed of A. xylinum and yeasts and named “nata” is consumed in Philippines as a delicacy. In Brazil, this cellulose network is used for the treatment of skin burns and other dermal injuries and is produced by a pure culture of A. xylinum grown on a medium composed mainly of sucrose and tea xanthines [6]. Caffeine and related compounds (theophylline and theobromine ) are identified as activators for cellulose production in A. xylinum [7]. In ancient days, this cellulose biofilm has been used for the treatment of wounds. Microbial cellulose synthesized in abundance by Acetobacter xylinum shows vast potential as a novel wound healing system. The high mechanical strength and remarkable physical properties result from the unique nanostructure of the never-dried membrane [8].

7 Organic Acids

Kombucha was reported to have several acetic, gluconic, glucuronic, citric, l-lactic, malic, tartaric, malonic, oxalic, succinic, pyruvic, and usnic acids. Most of these acids are having origin of the tea substrate used to prepare kombucha tea. About 0.5–0.6 % of dry weight of fresh tea shoot consists of organic acids. Among the organic acids present in kombucha tea citric, malic, tartaric, oxalic, and succinic acids are reported to be present in fresh tea shoots [9]. Acetic, gluconic, glucuronic, l-lactic, malonic, pyruvic, and usnic acids present in kombucha tea are produced by the action of microbes on sugar during fermentation time. Acetic acid is the predominant organic acid and is produced by acetic acid bacteria through oxidation of ethanol. It is the main reason for the decrease in pH. Due to increased concentration of organic acids produced during the fermentation process by bacteria and yeasts in the tea fungus consortium , the pH value decreased from 5.0 to 3.0. Apparently the fermentation broth possessed some buffer capacity. During the fermentation process, carbon dioxide is released at first slowly and much faster after 2–3 days. The obtained water solution of carbon dioxide dissociates and produces the amphiprotic hydrocarbonate anion (HCO3 _), which easily reacts with hydrogen ions (H+) from organic acids, preventing further changes in the H+ concentration and contributing to a buffer character of the system. This will be the valid reason for slight decrease in pH after 3 days [2].

Acetic acid was reported even when the sugar source was molasses. l-lactic and citric acid is not characteristic compound for traditional kombucha beverage. l-lactic acid was detected in traditional kombucha beverage and even when molasses and green tea was used as sugar source and tea substrate, respectively. Citric acid was detected in very small amount when black tea and green tea was used as tea substrate [2]. Oxidation of first carbon of glucose gives gluconic acid and at sixth carbon gives glucuronic acid (Fig. 3). Glucuronic acid is therapeutically important due to the detoxification action inside human body. Conjugation of glucuronic acid with undesirable compounds results in decreased toxicity due to the increased solubility of them that further facilitates transport and elimination from the body. Glucuronidation is aided by UDP glucuronosyltransferases enzyme [10]. Acetic acid bacteria convert glucose to gluconic acid and ethanol to acetic acid by oxidation.
Fig. 3

Structure of d-gluconic and d-glucuronic acid

8 Total Phenolic Compounds

Total phenolic compounds were progressively increased with fermentation time. Phenolic compounds are considered as high-level antioxidants because of their ability to scavenge free radical and active oxygen species such as singlet oxygen, superoxide free radicals, and hydroxyl radicals. Complex phenolic compounds in green tea, black tea, and waste tea might be subjected to degradation in acidic environment of kombucha and by the enzymes liberated by bacteria and yeast in tea fungus consortium. So, there are many chances for the enzymes liberated by bacteria and yeast during kombucha fermentation which be the reason for the degradation of complex polyphenols to small molecules which in turn results in the increase of total phenolic compounds [2].

9 Tea Polyphenols

Source of polyphenols in kombucha tea is the tea substrate, black tea, or green tea. The amount of polyphenols present depends on the variety or the grade of tea substrate, the amount used, brewing time given to prepare decoction, and time of fermentation. Total phenol content of tea decoction increases with time during kombucha fermentation. Gallic acid, epicatechin isomers (-)-epigallocatechin-3-gallate , (-)-epigallocatechin , (-)-epicatechin-3-gallate , (-)-epicatechin , theaflavin isomers, and thearubigins were detected and quantified during fermentation period (Fig. 4a, 4b, 4c). Theaflavin isomers (theaflavin-3-gallate, theaflavin 3′-gallate, and theaflavin 3,3′-digallate) were not detected in kombucha tea. Highly complexed polyphenols like EGCG and ECG undergo degradation and get converted to EGC and EC, respectively, which was evident through the quantification of polyphenols. The color of finally fermented kombucha tea is lighter than the initial tea decoction. This suggests that the compounds responsible for color, thearubigins undergo degradation in acidic environment of kombucha or by the enzymes liberated by bacteria and yeasts. Loss in initial color might be also due to the microbial or enzymatic transformation of thearubigins to less colored compounds [2].
Fig. 4

Structure of epicatechin isomers (a), theaflavin isomers (b), and thearubigins (c)

10 Microbial Composition of Kombucha

The name “Kombucha” usually denotes the beverage prepared through fermentation or the inoculum (tea fungus) used to ferment. Tea fungus or Medusomyces gisevii is a symbiotic association of bacteria and yeast in cellulose biofilm (Fig. 5a, 5b). The name “tea fungus ” is wrongly given to this association by local people due to its resemblance with the statically grown fungus mat or with the upper portion of the mushroom. Bacteria belong to acetic acid producers and yeasts belong to osmophilic group. Cellulose is the metabolite produced by acetic acid bacteria when it is aerobically grown and microbial cells present near the cellulose fibers are trapped inside it. Composition of microbes present in tea fungus is not similar throughout the world. The composition of metabolites of kombucha tea is depending on the metabolism of the microbes present in this symbiotic association. Hence, the composition of metabolites of kombucha is not same everywhere. Bacteria belong to the genus Acetobacter and Gluconobacter . Among Acetobacter, A. xylinum, A. pasteurianus, A. aceti, A. intermedium sp. nov., and Acetobacter nitrogenifigens sp. nov are reported. Gluconobacter oxydans, Gluconoacetobacter sp. A4, and Gluconoacetobacter kombuchae sp. nov. are found to be present among Gluconobacter genus. Presence of Lactobacillus species were reported very recently. Yeasts in tea fungus includes the genus Brettanomyces/Dekkera, Candida, Kloeckera, Mycotorula, Mycoderma, Pichia, Saccharomyces, Schizosaccharomyces, Torulospora, and Zygosaccharomyces. Genus Brettanomyces includes Brettanomyces intermedius, B. bruxellensis, and B. claussenii. The reported species in the genus Candida includes Candida famata, C. guilliermondii, C. obutsa, C. famata, C. stellate, C. guilliermondi, C. colleculosa, C. kefyr, and C. krusei. Saccharomyces genus includes Saccharomyces cerevisiae and Saccharomyces bisporus. Schizosacchromyces genus was found to have Schizosaccharomyces pombe and Zygosaccharomyces was identified as Zygosaccharomyces rouxii, Zygosaccharomyces bailii, and Zygosaccharomyces kombuchaensis sp. n. Apart from these yeast species, Sacchromyccoides ludwigii and Schizosaccharomyces pombe were also reported. The following yeast species were also reported: Torula, Torulopsis, Torulaspora delbrueckii, Mycoderma, Pichia, Pichia membranefaciens, Kloeckera apiculata, and Kluyveromyces africanus. It is reported that viable count of acetic acid bacteria and yeast reached maximum after 6 days of fermentation and continued to decrease in latter period of fermentation. The decreased number of bacteria and yeast during latter period of fermentation was likely caused by acid shock (low pH), which influenced the multiplication of bacteria and yeast [2]. Chen and Liu [1] reported that anaerobic and starved environment created could also be the reason for the decrease in microbial content during the fermentation period. Carbon dioxide generated as a result of alcohol fermentation by yeasts accumulated in the interface between the pellicle and broth. This separates the pellicle from the broth and creates an anaerobic and starved environment due to block of transfer of nutrients from broth to pellicle and transfer of oxygen from the surface of the pellicle to broth. There are controversial statements existing in literature about the concentration of viable microbial cells in tea broth and cellulose pellicle.
Fig. 5

Scanning electron microscope image of the consortia of yeasts and bacteria in a portion of tea fungus (magnification 4A = 3500× and 4B = 3700×) (Reproduced with prior permission, Jayabalan et al. [2])

11 Other Minor Metabolites

Yeast cells produce ethanol as a fermentative product from fructose through glycolysis and by the action of pyruvate dehydrogenase and alcohol dehydrogenase during kombucha fermentation. Ethanol was detected only in very less concentrations (0.55 %) due to its oxidation to acetic acid by acetic acid bacteria. Water soluble vitamins B1, B6, B12, and C are reported to be present in kombucha prepared with traditional substrates, sugar, and black tea. Yeasts are responsible for the biosynthesis of B vitamins. Presence of manganese, iron, nickel, copper, zinc, lead, cobalt, and chromium was determined in kombucha beverage. Essential minerals like copper, iron, manganese, nickel, and zinc were increased during fermentation period. Due to the inclusion of cobalt in vitamin B12, it is not increased. Presence of anionic minerals like fluoride, chloride, bromide, iodide, nitrate, phosphate, and sulphate is also proved. The content of d-saccharic acid 1,4 lactone (DSL) increases during fermentation period up to 8th day and found to be decreased after that. Likewise, the protein content of kombucha beverage also increases up to 12th day of fermentation and started to decrease after that. It may be due to the decrease in content of extracellular proteins secreted by the bacteria and yeasts [2].

12 Factors Influencing the Presence and Concentration of Kombucha Metabolites

Presence of different metabolites and their concentration in Kombucha from different regions cannot be similar due to the following reasons:
  1. i.

    Changes in the microbial composition of tea fungus consortium

     
  2. ii.

    Changes in the variety of tea substrates

     
  3. iii.

    Changes in the amount of sugar, tea, inoculum, and temperature

     
  4. iv.

    Changes in the fermentation time

     

13 Conclusion

Beneficial effects reported for kombucha drinking are based on the presence and concentration of polyphenols, organic acids, and other micronutrients produced during fermentation. Tea polyphenols are important in cancer prevention and other metabolites are essential for the beneficial effects of kombucha tea. It is expected that there will be an influence of microorganisms present in kombucha on the concentration of kombucha metabolites. Changes in the concentration of metabolites during fermentation period and the detailed composition of kombucha tea have not been studied well. Studies on biotransformation of components by acidic environment and enzymes of microbes during kombucha fermentation will be interesting and provide details of therapeutic benefits of kombucha tea.

Notes

Acknowledgement

Author Rasu Jayabalan acknowledges the support given by the National Institute of Technology (Rourkela, Odisha, India), Prof. K. Swaminathan (Dept. of Microbial Biotechnology, Bharathiar University, Coimbatore, Tamil Nadu, India), Prof. Sei Eok Yun (Department of Food Science and Technology, Institute of Agricultural Science and Technology, Chonbuk National University, Jeonju, Republic of Korea), Dr. S. Marimuthu (R & D Centre, Parry Agro Industries Ltd., Valparai, Tamil Nadu, India), Department of Science and Technology (DST grant No. SERC/LS-156/2012), and Department of Biotechnology (DBT grant No. 102/IFD/SAN/2770/2013–2014), Ministry of Science and Technology, Government of India. Author Radomir Malbaša thanks the Ministry of Education, Science and Technological Development, Republic of Serbia (Grant III-46009).

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Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • Rasu Jayabalan
    • 1
    Email author
  • Radomir V. Malbaša
    • 2
  • Muthuswamy Sathishkumar
    • 3
  1. 1.Food Microbiology and Bioprocess Laboratory, Department of Life ScienceNational Institute of TechnologyRourkelaIndia
  2. 2.Faculty of TechnologyUniversity of Novi SadNovi SadSerbia
  3. 3.R&D Division, Eureka Forbes LtdHaralukunte, Kudlu, BangaloreIndia

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