Kombucha tea fermentation: Microbial and biochemical dynamics

International Journal of Food Microbiology

Volumn 220, Issue , 2016, Pages 63-72

  Chakravorty, Somnath ^a   Bhattacharya, Semantee ^a   Chatzinotas, Antonis ^b   Chakraborty, Writachit ^a   Bhattacharya, Debanjana ^a   Gachhui, Ratan ^a  

^a JADAVPUR UNIVERSITY   (India)

^b HELMHOLTZ CENTRE FOR ENVIRONMENTAL RESEARCH UFZ   (Germany)

Author keywords

Change in fermentation; High throughput sequencing; Kombucha tea; Microbial community structure and dynamics; Radical scavenging; T RFLP

Indexed keywords

ALCOHOL; CAFFEINE; FLAVONOID; FUNGAL RNA; POLYPHENOL; RNA 16S; SACCHAROLACTONE; SUGAR; KOMBUCHA; LACTONE; SACCHARIC ACID; SACCHARIC ACID-1,4-LACTONE;

ACIDITY; ARTICLE; BACTERIUM; BIOCHEMICAL ANALYSIS; BIOFILM; CANDIDA; COMMUNITY DYNAMICS; CONTROLLED STUDY; DEGRADATION KINETICS; FERMENTATION; FUNGAL COMMUNITY; HIGH THROUGHPUT SEQUENCING; KOMAGATEIBACTER; KOMBUCHA; LACHANCEA; MICROBIAL COMMUNITY; NONHUMAN; PH; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; YEAST; BIODIVERSITY; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; MICROFLORA; PHYSIOLOGY; SACCHAROMYCETALES;

BACTERIA; BIODIVERSITY; BIOFILMS; CANDIDA; FERMENTATION; GLUCARIC ACID; KOMBUCHA TEA; LACTONES; MICROBIOTA; SACCHAROMYCETALES;

EID: 84954348723     PISSN: 01681605     EISSN: 18793460     Source Type: Journal    
DOI: 10.1016/j.ijfoodmicro.2015.12.015     Document Type: Article

References (78)

1. Abdo Z., Schuette U.M.E., Bent J.S., Williams C.J., Forney L.J., Joyce P. Statistical methods for characterizing diversity of microbial communities by analysis of terminal restriction fragment length polymorphisms of 16S rRNA genes. Environ. Microbiol. 2006, 8:929-938.
2. Ahmed N. Advanced glycosylation end products-role in pathology of diabetic complications. Diabetes Res. Clin. Pract. 2005, 67:3-21.
3. Aloulou A., Hamden K., Elloumi D., Ali M.B., Hargafi K., Jaouadi B., Ayadi F., Elfeki A., Ammar E. Hypoglycemic and antilipidemic properties of Kombucha tea in alloxan-induced diabetic rats. BMC Complement. Altern. Med. 2012, 12:63-71.
4. Bancirova M. Comparison of the anti-oxidant capacity and the anti-microbial activity of black and green tea. Food Res. Int. 2010, 43:1379-1382.
5. Banerjee D., Hassarajani S.A., Maity B., Narayan G., Bandyopadhya S.K., Chattopadhyay S. Comparative healing property of Kombucha tea and black tea against indomethacin induced gastric ulceration in mice: possible mechanism of action. Food Funct. 2010, 1:284-293.
6. Bhattacharya S., Gachhui R., Sil P.C. Effect of Kombucha, a fermented black tea in attenuating oxidative stress mediated tissue damage in alloxan induced diabetic rats. Food Chem. Toxicol. 2013, 60:328-340.
7. Bhusari S.I., Desai V.D., Nalavade M.L., Wadkar S.S., Ghosh J.S. Fermentation and characterization of wine from fruits of Phoenix dactylifera, using Saccharomyces cerevisae NCIM 3495. Int. Food Res. J. 2013, 20:3411-3415.
8. Blois M.S. Antioxidant determination by use of a stable free radical. Nature 1958, 181:1199-1200.
9. Camarinha-Silva A., Wos-Oxley M.L., Jáuregui R., Becker K., Pieper D.H. Validating T-RFLP as a sensitive and high-throughput approach to assess bacterial diversity patterns in human anterior nares. FEMS Microbiol. Ecol. 2012, 79:98-108.
10. Caporaso J.G., Kuczynski J., Stombaugh J., Bittinger K., Bushman F.D., Costello E.K., Fierer N., Pena A.G., Goodrich J.K., Gordon J.I., Huttley G.A., et al. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 2010, 7:335-336.
11. Caporaso J.G., Lauber C.L., Walters W.A., Berg Lyons D., Huntley J., Fierer N., Owens S.M., Betley J., Fraser L., Bauer M., Gormley N., Gilbert J.A., Smith G., Knight R. Ultra high throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J. 2012, 6:1621-1624.
12. Chakravorty S., Sarkar S., Gachhui R. Identification of new conserved and variable regions in the 16S rRNA gene of acetic acid bacteria and Acetobacteraceae family. Mol. Biol. 2015, 49:668-677. 10.1134/S0026893315050052.
13. Chan E.W.C., Soh E.Y., Tie P.P., Law Y.P. Antioxidant and antibacterial properties of green, black, and herbal teas of Camellia sinensis. Pharmacogn. Res. 2011, 3:266-272.
14. Chang C.C., Yang M.H., Wen H.M., Chern J.C. Estimation of total flavonoid content in propolis by two complementary colorimetric Methods. J. Food Drug Anal. 2002, 10:178-182.
15. Chen C., Liu B.Y. Changes in major components of tea fungus metabolites during prolonged fermentation. J. Appl. Microbiol. 2000, 89:834-839.
16. Chen D., Milacic V., Chen M.S., Wan S.B., Lam W.H., Huo C., et al. Tea polyphenols, their biological effects and potential molecular targets. Histol. Histopathol. 2008, 23:487-496.
17. Chu S.C., Chen C. Effects of origins and fermentation time on the antioxidant activities of Kombucha. Food Chem. 2006, 98:502-507.
18. Cole J.R., Wang Q., Fish J.A., Chai B., McGarrell D.M., Sun Y., Brown C.T., Porras-Alfaro A., Kuske C.R., Tiedje J.M. Ribosomal database project: data and tools for high throughput rRNA analysis. Nucleic Acids Res. 2013, 1-10.
19. Dufresne C., Farnworth E. Tea, Kombucha, and health: a review. Food Res. Int. 2000, 33:409-421.
20. Dutta D., Gachhui R. Novel nitrogen-fixing Acetobacter nitrogenifigens sp. nov., isolated from Kombucha tea. Int. J. Syst. Evol. Microbiol. 2006, 56:1899-1903.
21. Dutta D., Gachhui R. Nitrogen-fixing and cellulose-producing Gluconacetobacter kombuchae sp. nov., isolated from Kombucha tea. Int. J. Syst. Evol. Microbiol. 2007, 57:353-357.
22. Edgar R.C. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 2013, 10:996-998.
23. El-Salam S.S.A. 16S rRNA gene sequence detection of acetic acid bacteria isolated from tea Kombucha. N. Y. Sci. J. 2012, 5:55-61.
24. Ettayebi K., Errachidi F., Jamai L., Tahri-Jouti M.A., Sendide K., Ettayebi M. Biodegradation of polyphenols with immobilized Candida tropicalis under metabolic induction. FEMS Microbiol. Lett. 2003, 223:215-219.
25. Ferreira I.C.F.R., Baptista P., Vilas-Boas M., Barros L. Free-radical scavenging capacity and reducing power of wild edible mushrooms from northeast Portugal: individual cap and stipe activity. Food Chem. 2007, 100:1511-1516.
26. Giebler J., Wick L.Y., Chatzinotas A., Harms H. Alkane-degrading bacteria at the soil-litter interface: comparing isolates with T-RFLP-based community profiles. FEMS Microbiol. Ecol. 2013, 86:45-58.
27. Giebler J., Wick L.Y., Harms H., Chatzinotas A. Evaluating T-RFLP protocols to sensitively analyze the genetic diversity and community changes of soil alkane degrading bacteria. Eur. J. Soil Microbiol. 2014, 65:107-113.
28. Greenwalt C.J., Steinkraus K.H., Ledford R.A. Kombucha, the fermented tea: microbiology, composition, and claimed health effects. J. Food Prot. 2000, 63:976-981.
29. Harris C.S., Beaulieu L.P., Fraser M.H., McIntyre K.L., Owen P.L., Martineau L.C., Cuerrier A., Johns T., Haddad P.S., Bennett S.A.L., Arnason J.T. Inhibition of advanced glycation end product formation by medicinal plant extracts correlates with phenolic metabolites and antioxidant activity. Planta Med. 2011, 77:196-204.
30. Hesseltine C.W. A millenium of fungi. Food and fermentation. Mycologia 1965, 57:148-167.
31. Hugenholtz P., Goebel B.M., Pace N.R. Impact of culture independent studies on the emerging phylogenetic view of bacterial diversity. J. Bacteriol. 1998, 180:4765-4774.
32. Hur S.J., Lee S.Y., Kim Y.C., Choi I., Kim G.B. Effect of fermentation on the antioxidant activity in plant-based foods. Food Chem. 2014, 160:346-356.
33. Jankovic I., Stojanovic M. Microbial and chemical composition, growth, therapeutical and antimicrobial characteristics of tea fungus. Mikrobiologija 1994, 31.
34. Jarrell J., Cal T., Bennett J.W. The Kombucha consortia of yeasts and bacteria. Mycologist 2000, 14:166-170.
35. Jayabalan R., Marimuthu S., Swaminathan K. Changes in content of organic acids and tea polyphenols during Kombucha tea fermentation. Food Chem. 2007, 102:392-398.
36. Jayabalan R., Marimuthu S., Sathishkumar M., Swaminathan K. Changes in free-radical scavenging ability of Kombucha tea during fermentation. Food Chem. 2008, 109:227-234.
37. Jayabalan R., Marimuthu S., Thangaraj P., Sathishkumar M., Binupriya A.R., Swaminathan K., Sei E.Y. Preservation of Kombucha tea: effect of temperature on tea components and free radical scavenging properties. J. Agric. Food Chem. 2008, 56:9064-9071.
38. Jayabalan R., Baskaran S., Marimuthu S., Swaminathan K., Yun S.E. Effect of Kombucha tea on aflatoxin B1-induced acute hepatotoxicity in albino rats-prophylactic and curative studies. J. Appl. Biol. Chem. 2010, 53:407-416.
39. Jayabalan R., Chen P.N., Hsieh Y.S., Prabhakaran K., Pitchai P., Marimuthu S., Thangaraj P., Swaminathan K., Yun S.E. Effect of solvent fractions of Kombucha tea on viability and invasiveness of cancer cells-characterization of dimethyl 2-(2-hydroxy-2-methoxypropylidine) malonate and vitexin. Indian J. Biotechnol. 2011, 10:75-82.
40. Jayabalan R., Malbaša R.V., Lončar E.S., Vitas J.S., Sathishkumar M. A review on Kombucha tea-microbiology, composition, fermentation, beneficial effects, toxicity, and tea fungus. Compr. Rev. Food Sci. Food Saf. 2014, 13:538-550.
41. Kallel L., Desseaux V., Hamdi M., Stocker P., Ajandouz E.H. Insights into the fermentation biochemistry of Kombucha teas and potential impacts of Kombucha drinking on starch digestion. Food Res. Int. 2012, 49:226-232.
42. Konovalov I.N., Semenova M.N. K Fiziologii "Cajnogo Griba". Bot Žurnal (Moscow) 1955, 40:567-570.
43. Kumari R., Meyyappan A., Nandi D., Agrawalla B.K., Chowdhury A.A., Selvamani P., Latha S., Giri V.S., Mukherjee J., Bandyopadhyay S., Jaisankar P. Antioxidant and antibacterial activities of bark extracts from Commiphora berryi and Commiphora caudate. Nat. Prod. Res. 2011, 25:1454-1462.
44. Lane D.J., Goodfellow M. 16S/23S rRNA Sequencing. Nucleic Acid Techniques in Bacterial Systematics 1991, 115-175. John Wiley and Sons, New York, NY. E. Stackebrandt (Ed.).
45. Lee K.W., Lee H.J. Anti-oxidant activity of black tea vs. green tea. J. Nutr. 2002, 132:785.
46. Liu C.H., Hsu W.H., Lee F.L., Liao C.C. The isolation and identification of microbes from a fermented tea beverage, Haipao, and their interactions during Haipao fermentation. Food Microbiol. 1996, 13:407-415.
47. Loncar E.S., Petrovic S.E., Malbasa R.V., Verac R.M. Biosynthesis of glucuronic acid by means of tea fungus. Food Nahrung 2000, 44:138e139.
48. Malbaša R.V., Lončar E.S., Vitas J.S., Čanadanović-Brunet J.M. Influence of starter cultures on the anti-oxidant activity of Kombucha beverage. Food Chem. 2011, 127:1727-1731.
49. Marsh A.J., Sullivan O.O., Hill C., Ross R.P., Cotter P.D. Sequence-based analysis of the bacterial and fungal compositions of multiple Kombucha (tea fungus) samples. Food Microbiol. 2014, 38:171-178.
50. Mayo B., Rachid C.T.C.C., Alegría A., Leite A.M.O., Peixoto R.S., Delgado S. Impact of next generation sequencing techniques in food microbiology. Curr. Genet. 2014, 15:293-309.
51. Mayser P., Fromme S., Leitzmann C., Grunder K. The yeast spectrum of the 'tea fungus Kombucha'. Mycoses 1995, 38:289-295.
52. Moyer C.L., Dobbs F.C., Karl D.M. Estimation of diversity and community structure through restriction fragment length polymorphism distribution analysis of bacterial 16S rRNA genes from a microbial mat at an active, hydrothermal vent system, Loihi seamount, Hawaii. Appl. Environ. Microbiol. 1994, 60:871-879.
53. Mühling M., Woolven-Allen J., Colin Murrel l.J., Joint I. Improved group-specific PCR primers for denaturing gradient gel electrophoresis analysis of the genetic diversity of complex microbial communities. ISME J. 2008, 2:379-392.
54. Nash T. The colorimetric estimation of formaldehyde by means of the Hantzsch reaction. Biochem. J. 1953, 55:416-421.
55. Nikolaev Y.A., Plakunov V.K. Biofilm-"City of Microbes" or an analogue of multicellular organisms. Microbiology 2007, 76:125-138.
56. Pilloni G., Granitsiotis M.S., Engel M., Lueders T. Testing the limits of 454 pyrotag sequencing: reproducibility, quantitative assessment and comparison to t-RFLP fingerprinting of aquifer microbes. Plos One 2012, 7.
57. Pruesse E., Peplies J., Glöckner F.O. SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 2012, 28:1823-1829.
58. Quast C., Pruesse E., Yilmaz P., Gerken J., Schweer T., Yarza P., Peplies J., Glöckner F.O. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2013, 41:D590-D596.
59. R Core Team R: A language and environment for statistical computing 2014, R Foundation for Statistical Computing, Vienna, Austria, URL, http://www.R-project.org/.
60. Ram M.S., Anju B., Pauline T., Prasad D., Kain A.K., Mongia S.S., Sharma S.K., Singh B., Singh R., Ilavazhagan G., Kumar D., Selvamurthy W. Effect of Kombucha tea on chromate(VI)-induced oxidative stress in albino rats. J. Ethnopharmacol. 2000, 71:e235-e240.
61. Ramaswamy S. Report of Tea Technologist. UPASI Scientific Department of Annual Report 1978, 126-148.
62. Roy S., Hazra B., Mandal N., Chaudhuri T.K. Assessment of the antioxidant and free radical scavenging activities of methanolic extract of Diplazium esculentum. Int. J. Food Prop. 2013, 16:1351-1370.
63. Sengupta S., Jana M.L., Sengupta D., Naskar A.K. A note on the estimation of microbial glycosidase activities by dinitrosalicylic acid reagent. Appl. Microbiol. Biotechnol. 2000, 53:732-735.
64. Shannon C.E., Weaver W. A mathematical theory of communication. Bell Syst. Tech. J. 1948, 27. (379-423 and 623-656).
65. Sievers M., Lanini C., Weber A., Schuler-Schmid U., Teuber M. Microbiology and fermentation balance in a Kombucha beverage obtained from a tea fungus fermentation. Syst. Appl. Microbiol. 1995, 18:590-594.
66. Simpson E.H. Measurement of diversity. Nature 1949, 163:688.
67. Singleton V.L., Orthofer R., Lamuela-Raventos R.M. Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin-Ciocalteu reagent. Methods Enzymol. 1999, 299:152-178.
68. Skoog D.A., Holler F.J., Crouch S.R. Principles of Instrumental Analysis 2007, Harcourt Brace College Publishers, (Chapters 26 and 28). sixth ed.
69. Takeo T., Oosawa K. Photometric analysis of black tea infusion. Bull. Natl. Res. Inst. Tea (Jpn.) 1976, 12:125-181.
70. Teoh A.L., Heard G., Cox J. Yeast ecology of Kombucha fermentation. Int. J. Food Microbiol. 2004, 95:119-126.
71. Thanaraj S.N.S., Seshadri R. Influence of polyphenol oxidase activity and polyphenol content of tea shoot as quality of black teas. J. Sci. Food Agric. 1990, 35:57-69.
72. Tonge D.P., Pashley C.H., Gant T.W. Amplicon-based metagenomic analysis of mixed fungal samples using proton release amplicon sequencing. PLOS One 2014, 9.
73. Wang K., Gan X., Tang X., Wang S., Tan H. Determination of d-saccharic acid-1,4-lactone from brewed Kombucha broth by high-performance capillary electrophoresis. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 2010, 878:371-374.
74. Wang Y., Ji B., Wu W., Wang R., Yang Z., Zhang D., Tian W. Hepatoprotective effects of Kombucha tea: identification of functional strains and quantification of functional components. J. Sci. Food Agric. 2014, 94:265-272.
75. Weisburg W.G., Barns S.M., Pelletier D.A., Lane D.J. 16S ribosomal DNA amplification for phylogenetic study. J. Bacteriol. 1991, 173:697-703.
76. Whittaker R.H. Evolution and measurement of species diversity. Taxon 1972, 21:213-251. 10.2307/1218190.
77. Yamada Y., Yukphan P., Vu H.T.L., Muramatsu Y., Ochaikul D., Tanasupawat S., Nakagawa Y. Description of Komagataeibacter gen. nov., with proposals of new combinations (Acetobacteraceae). J. Gen. Appl. Microbiol. 2012, 58:397-404.
78. Yang Z.W., Ji B.P., Zhou F., Li B., Luo Y., Yang L., Li T. Hypocholesterolaemic and antioxidant effects of kombucha tea in high-cholesterol fed mice. J. Sci. Food Agric. 2009, 89:150-156.