Kombucha beverage from green, black and rooibos teas: A comparative study looking at microbiology, chemistry and antioxidant activity

Nutrients

Volumn 11, Issue 1, 2019, Pages

  Gaggìa, Francesca ^a   Baffoni, Loredana ^a   Galiano, Michele ^a   Nielsen, Dennis Sandris ^b   Jakobsen, Rasmus Riemer ^b   Castro Mejía, Josue Leonardo ^b   Bosi, Sara ^a   Truzzi, Francesca ^a   Musumeci, Federica ^a   Dinelli, Giovanni ^a   Di Gioia, Diana ^a  

^a UNIVERSITY OF BOLOGNA   (Italy)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Fermentation; Kombucha; Oxidative stress; Rooibos

Indexed keywords

ALCOHOL; FLAVONOID; GENOMIC DNA; GLUCOSE; GLUCURONIC ACID; POLYPHENOL; RNA 16S; ANTIOXIDANT;

ANIMAL CELL; ANTIMICROBIAL ACTIVITY; ANTIOXIDANT ACTIVITY; ARTICLE; BEVERAGE; BIOFILM; BIOINFORMATICS; CELL VIABILITY; COMPARATIVE STUDY; CONTROLLED STUDY; CYTOTOXICITY; DNA EXTRACTION; DNA SEQUENCE; DPPH RADICAL SCAVENGING ASSAY; FERMENTATION; FIBROBLAST; GENOTYPE; HERBAL TEA; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HIGH THROUGHPUT SEQUENCING; KOMBUCHA; LIQUID CHROMATOGRAPHY-MASS SPECTROMETRY; MICROBIAL DIVERSITY; MOUSE; MTT ASSAY; NONHUMAN; OXIDATIVE STRESS; POLYMERASE CHAIN REACTION; TEA; ANALYSIS; ANIMAL; ASPALATHUS; CELL LINE; CHEMISTRY; METABOLISM; MICROBIOLOGY; YEAST;

ANIMALS; ANTIOXIDANTS; ASPALATHUS; BEVERAGES; CELL LINE; ETHANOL; FERMENTATION; FIBROBLASTS; FLAVONOIDS; KOMBUCHA TEA; MICE; OXIDATIVE STRESS; POLYPHENOLS; TEA; YEASTS;

EID: 85058915194     PISSN: None     EISSN: 20726643     Source Type: Journal    
DOI: 10.3390/nu11010001     Document Type: Article

References (74)

1. Jarrell, J.; Cal, T.; Bennett, J.W. The Kombucha consortia of yeasts and bacteria. Mycologist 2000, 14, 166–170. [CrossRef]
2. Marsh, A.J.; O’Sullivan, 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, 8, 171–178. [CrossRef] [PubMed]
3. De Filippis, F.; Troise, A.D.; Vitaglione, P.; Ercolini, D. Different temperatures select distinctive acetic acid bacteria species and promotes organic acids production during Kombucha tea fermentation. Food Microbiol. 2018, 73, 11–16. [CrossRef] [PubMed]
4. Dufresne, C.; Farnworth, E. Tea, kombucha, and health: A review. Food Res. Intern. 2000, 33, 409–421. [CrossRef]
5. Kapp, J.M.; Sumner, W. Kombucha: A systematic review of the empirical evidence of human health benefit.. Ann. Epidemiol. 2018, in press. [CrossRef] [PubMed]
6. 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. [CrossRef]
7. Malbaša, R.V.; Lončar, E.S.; Kolarov, L.J.A. Sucrose and inulin balance during tea fungus fermentation. Roum. Biotechnol. Lett. 2002, 7, 573–576.
8. Malbaša, R.V.; Lončar, E.S.; Kolarov, L.J.A. L-lactic, L-ascorbic, total and volatile acids contents in dietetic kombucha beverage. Roum. Biotechnol. Lett. 2002, 7, 891–896.
9. Vitas, J.S.; Malbaša, R.V.; Grahovac, J.A.; Lončar, E.S. The antioxidant activity of kombucha fermented milk products with stinging nettle and winter savory. CI CEQ 2013, 19, 129–139. [CrossRef]
10. 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. [CrossRef] [PubMed]
11. Valduga, A.T.; Gonçalves, I.L.; Magri, E.; Delalibera Finzer, J.R. Chemistry, pharmacology and new trends in traditional functional and medicinal beverages. Food Res. Int. 2018. [CrossRef]
12. Chu, S.C.; Chen, C. Effects of origins and fermentation time on the antioxidant activities of kombucha. Food Chem. 2006, 98, 502–507. [CrossRef]
13. 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. [CrossRef]
14. Jayabalan, R.; Subathradevi, P.; Marimuthu, S.; Sathishkumar, M.; Swaminathan, K. Changes in free radical scavenging ability of kombucha tea during fermentation. Food Chem. 2008, 109, 227–234. [CrossRef]
15. Lin, Y.L.; Juan, I.M.; Chen, Y.L.; Liang, Y.C.; Lin, J.K. Composition of polyphenols in fresh tea leaves and associations of their oxygen-radical absorbing capacity with antiproliferative actions in fibroblast cells. J. Agric. Food Chem. 1996, 44, 1387–1394. [CrossRef]
16. Lin, J.K.; Lin, C.L.; Liang, Y.C.; Lin-Shiau, S.Y.; Juan, I.M. Survey of catechins, gallic acid, and methylxanthines in green, oolong, puerh, and black teas. J. Agric. Food Chem. 1998, 46, 3635–3642. [CrossRef]
17. Villarreal-Soto, S.A.; Beaufort, S.; Bouajila, J.; Souchard, J.P.; Tailandier, P. Understanding kombucha tea fermentation: A review. J. Food Sci. 2018, 83, 580–588. [CrossRef]
18. Hiremath, U.S.; Vaidehi, M.P.; Mushtari, B.J. Effect of Fermented tea on the blood sugar levels of NIDDM Subjects. Indian Pract. 2002, 55, 423–425.
19. Joubert, E.; Gelderblom, W.C.A.; Louw, A.; De Beer, D. South African herbal teas: Aspalathus linearis, Cycilopia spp. and Athrixia phylicoides—A review. J. Ethnopharmacol. 2008, 119, 376–412. [CrossRef]
20. McKay, D.L.; Blumberg, J.B. A review of the bioactivity of South African herbal teas: Rooibos (Aspalathus linearis) and honeybush (Cyclopia intermedia). Phytoth. Res. 2007, 21, 1–16. [CrossRef]
21. 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. [CrossRef] [PubMed]
22. Mamlouk, D.; Gullo, M. Acetic acid bacteria: Physiology and carbon sources oxidation. Indian J. Microbiol. 2013, 53, 377–384. [CrossRef]
23. Yamada, Y.; Hosono, R.; Lisdyanti, P.; Widyastuti, Y.; Saono, S.; Uchimura, T.; Komagata, K. Identification of acetic acid bacteria isolated from Indonesian sources, especially of isolates classified in the genus Gluconobacter. J. Gen. Appl. Microbiol. 1999, 45, 23–28. [CrossRef] [PubMed]
24. Di Gioia, D.; Mazzola, G.; Nikodinoska, I.; Aloisio, I.; Langerholc, T.; Rossi, M.; Raimondi, S.; Melero, B.; Rovira, J. Lactic acid bacteria as protective cultures in fermented pork meat to prevent Clostridium spp. growth. Int. J. Food Microbiol. 2016, 235, 53–59. [CrossRef] [PubMed]
25. Gaggìa, F.; Baffoni, L.; Stenico, V.; Alberoni, D.; Buglione, E.; Lilli, A.; Di Gioia, D.; Porrini, C. Microbial investigation on honey bee larvae showing atypical symptoms of European foulbrood. Bull. Insectol. 2015, 68, 321–327.
26. Jeyarama, K.; Mohendro Singha, W.; Capece, A.; Romano, P. Molecular identification of yeast species associated with ‘Hamei’-A traditional starter used for rice wine production in Manipur, India. Int. J. Food Microbiol. 2008, 124, 115–125. [CrossRef]
27. Jespersen, L.; Nielsen, D.S.; Hønholt, S.; Jakobsen, M. Occurrence and diversity of yeasts involved in fermentation of West African cocoa beans. FEMS Yeast Res. 2005, 5, 441–453. [CrossRef]
28. Basic Local Alignment Search Tool. Available online: http://www.ncbi.nlm.nih.gov/BLAST/(accessed on 6 June 2018).
29. GenBank, NCBI Submission Portal. Available online: https://submit.ncbi.nlm.nih.gov/subs/genbank (accessed on 3 September 2018).
30. Krych, L.; Kot, W.; Bendtsen, K.M.B.; Hansen, A.K.; Vogensen, F.K.; Nielsen, D.S. Have you tried spermine? A rapid and cost-effective method to eliminate dextran sodium sulfate inhibition of PCR and RT-PCR. J. Microbiol. Methods 2018, 144, 1–7. [CrossRef]
31. Haastrup, M.K.; Johansen, P.; Malskær, A.H.; Castro-Mejía, J.L.; Kot, W.; Krych, L.; Arneborg, N.; Jespersen, L. Cheese brines from Danish dairies reveal a complex microbiota comprising several halotolerant bacteria and yeasts. Int. J. Food Microbiol. 2018, 285, 173–187. [CrossRef]
32. Edgar, R.C. Updating the 97% identity threshold for 16S ribosomal RNA OTUs. Bioinformatics 2018, 34, 2371–2375. [CrossRef]
33. Edgar, R. SINTAX: A simple non-Bayesian taxonomy classifier for 16S and ITS sequences. bioRxiv 2016. [CrossRef]
34. Kim, O.S.; Cho, Y.J.; Lee, K.; Yoon, S.H.; Kim, M.; Na, H.; Park, S.C.; Jeon, Y.S.; Lee, J.H.; Yi, H.; Won, S.; Chun, J. Introducing EzTaxon-e: A prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int. J. Syst. Evol. Microbiol. 2012, 62, 716–721. [CrossRef] [PubMed]
35. Kõljalg, U.; Nilsson, R.H.; Abarenkov, K.; Tedersoo, L.; Taylor, A.F.; Bahram, M.; Bates, S.T.; Bruns, T.D.; Bengtsson-Palme, J.; Callaghan, T.M.; et al. Towards a unified paradigm for sequence-based identification of fungi. Mol. Ecol. 2013, 22, 5271–5277.
36. Paulson, J.N.; Stine, O.C.; Bravo, H.C.; Pop, M. Differential abundance analysis for microbial marker-gene surveys. Nat. Methods 2013, 10, 1200–1202. [CrossRef] [PubMed]
37. Weiss, S.; Xu, Z.Z.; Peddada, S.; Amir, A.; Bittinger, K.; Gonzalez, A.; Lozupone, C.; Jesse, R.; Zaneveld, J.R.; Vázquez-Baeza, Y.; et al. Normalization and microbial differential abundance strategies depend upon data characteristics. Microbiome 2017, 5, 1–27. [CrossRef] [PubMed]
38. Caporaso, J.G.; Kuczynski, J.; Stombaugh, J.; Bittinger, K.; Bushman, F.D.; Costello, E.K.; Fierer, N.; Peña, A.G.; Goodrich, J.K.; Gordon, J.I.; et al. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 2010, 7, 335–336. [CrossRef] [PubMed]
39. McMurdie, P.J.; Holmes, S. Waste not, want not: WHY rarefying microbiome data is inadmissible. PLoS Comput. Biol. 2014, 10, E1003531. [CrossRef]
40. Crafack, M.; Mikkelsen, M.B.; Saerens, S.; Knudsen, M.; Blennow, A.; Lowor, S.; Takrama, J.; Swiegers, J.H.; Petersen, G.B.; Heimdal, H.; et al. Influencing cocoa flavour using Pichia kluyveri and Kluyveromyces marxianus in a defined mixed starter culture for cocoa fermentation. Int. J. Food Microbiol. 2013, 167, 103–116. [CrossRef] [PubMed]
41. Singleton, V.L.; Orthofer, R.; Lamuela-Raventós, R.M.; Lester, P. Analysis of total phenols and other oxidation substrates and antioxidants by means of folin-ciocalteu reagent. Meth. Enzimol. 1999, 299, 152–178.
42. Adom, K.K.; Liu, R.H. Antioxidant activity of grains. J. Agric. Food. Chem. 2002, 50, 6182–6187. [CrossRef] [PubMed]
43. Benzie, I.F.; Strain, J.J. The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: THE FRAP assay. Anal. Biochem. 1996, 239, 70–76. [CrossRef] [PubMed]
44. Floegel, A.; Kim, D.O.; Chung, S.J.; Koo, S.I.; Chun, O.K. Comparison of ABTS/DPPH assays to measure antioxidant capacity in popular antioxidant-rich US foods. J. Food Compos. Anal. 2011, 24, 1043–1048. [CrossRef]
45. Naldi, M.; Fiori, J.; Gotti, R.; Périat, A.; Veuthey, J.L.; Guillarme, D.; Andrisano, V. UHPLC determination of catechins for the quality control of green tea. J. Pharm. Biomed. Anal. 2014, 88, 307–314. [CrossRef] [PubMed]
46. Leoncini, E.; Prata, C.; Malaguti, M.; Marotti, I.; Segura-Carretero, A.; Catizone, P.; Dinelli, G.; Hrelia, S. Phytochemical profile and nutraceutical value of old and modern common wheat cultivars. PLoS ONE 2012, 7, e45997. [CrossRef]
47. International Organization for Standardization. Biological Evaluation of Medical Devices—Part 5: Tests for In Vitro Cytotoxicity. In ISO 10993-5. International Standard, 3rd ed.; International Organization for Standardization: Geneva, Switzerland, 2009; Available online: https://www.iso.org/standard/36406.html (accessed on 17 February 2018).
48. R Core Team. A Language and Environment for Statistical Computing; R Foundation for Statistical Computing: Vienna, Austria, 2016; Available online: http://www.R-project.org(accessed on 16 April 2018).
49. Smith, C.; Swart, A. Aspalathus linearis (Rooibos)—A functional food targeting cardiovascular disease. Food Funct. 2018, 17, 5041–5058. [CrossRef] [PubMed]
50. Ku, S.K.; Kwak, S.; Kim, Y.; Bae, J.S. Aspalathin and Nothofagin from Rooibos (Aspalathus linearis) inhibits high glucose-induced inflammation in vitro and in vivo. Inflammation 2015, 38, 445–455. [CrossRef]
51. Chakravorty, S.; Bhattacharya, S.; Chatzinotas, A.; Chakraborty, W.; Bhattacharya, D.; Gachhui, R. Kombucha tea fermentation: Microbial and biochemical dynamics. Int. J. Food Microbial. 2016, 220, 63–72. [CrossRef]
52. Ramana, K.V.; Batra, H.V. Occurrence of Cellulose-Producing Gluconacetobacter spp. in fruit samples and Kombucha tea, and production of the biopolymer. Appl. Biochem. Biotechnol. 2015, 176, 1162–1173.
53. Nguyen, N.K.; Nguyen, P.B.; Nguyen, H.T.; Le, P.H. Screening the optimal ratio of symbiosis between isolated yeast and acetic acid bacteria strain from traditional kombucha for high-level production of glucuronic acid. LWT Food Sci. Technol. 2015, 64, 1149–1155. [CrossRef]
54. Semjonovs, P.; Ruklisha, M.; Paegle, L.; Saka, M.; Treimane, R.; Skute, M.; Cleenwerck, I. Cellulose synthesis by Komagataeibacter rhaeticus strain P 1463 isolated from Kombucha. Appl. Microbiol. Biotechnol. 2017, 101, 1003–1012. [CrossRef]
55. Kose, R.; Sunagawa, N.; Yoshida, M.; Tajima, K. One-step production of nanofibrillated bacterial cellulose (NFBC) from waste glycerol using Gluconacetobacter intermedius NEDO-01. Cellulose 2013, 20, 2971–2979. [CrossRef]
56. Schüller, G.; Hertel, C.; Hammes, W.P. Gluconacetobacter entanii sp. nov., isolated from submerged high-acid industrial vinegar fermentations. Int. J. Syst. Evol. Microbiol. 2000, 50, 2013–2020. [CrossRef] [PubMed]
57. Reva, O.N.; Zaets, I.E.; Ovcharenko, L.P.; Kukharenko, O.E.; Shpylova, S.P.; Podolich, O.V.; Kozyrovska, N.O. Metabarcoding of the kombucha microbial community grown in different microenvironments. AMB Express 2015, 5, 35. [CrossRef] [PubMed]
58. Rozpedowska, E.; Hellborg, L.; Ishchuk, O.P.; Orhan, F.; Galafassi, S.; Merico, A.; Woolfit, M.; Compagno, C.; Piškur, J. Parallel evolution of the make–accumulate–consume strategy in Saccharomyces and Dekkera yeasts. Nat. Commun. 2011, 2, 302. [CrossRef] [PubMed]
59. Schifferdecker, A.J.; Dashko, S.; Ishchuk, O.P.; Piškur, J. The wine and beer yeast Dekkera bruxellensis. Yeast 2014, 31, 323–332. [CrossRef] [PubMed]
60. De Souza Liberal, A.T.; Basílio, A.C.M.; do Monte Resende, A.; Brasileiro, B.T.V.; Da Silva-Filho, E.A.; De Morais, J.O.F.; de Morais, M.A., Jr. Identification of Dekkera bruxellensis as a major contaminant yeast in continuous fuel ethanol fermentation. J. Appl. Microbiol. 2007, 102, 538–547. [CrossRef] [PubMed]
61. Passoth, V.; Blomqvist, J.; Schnürer, J. Dekkera bruxellensis and Lactobacillus vini form a stable ethanol-producing consortium in a commercial alcohol production process. Appl. Environ. Microbiol. 2007, 73, 4354–4356. [CrossRef] [PubMed]
62. Shahbazi, H.; Hashemi Gahruie, H.; Golmakani, M.T.; Eskandari, M.H.; Movahedi, M. Effect of medicinal plant type and concentration on physicochemical, antioxidant, antimicrobial, and sensorial properties of kombucha. Food Sci. Nutr. 2018, 6, 2568–2577. [CrossRef] [PubMed]
63. Vīna, I.; Linde, R.; Patetko, A.; Semjonovs, P. Glucuronic acid from fermented beverages: Biochemical functions in humans and its role in health protection. IJRRAS 2013, 14, 217–230.
64. Vina, I.; Semjonovs, P.; Linde, R.; Patetko, A. Glucuronic acid containing fermented functional beverages produced by natural yeasts and bacteria associations. Int. J. Res. Rev. Appl. 2013, 14, 17–25.
65. Martinez Leal, J.; Valenzuela Suárez, L.; Jayabalan, R.; Huerta Oros, J.; Escalante-Aburto, A. A review on health benefits of kombucha nutritional compounds and metabolites. CyTA J. Food 2018, 16, 390–399. [CrossRef]
66. 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. [CrossRef]
67. Tanaka, T.; Matsuo, Y.; Kouno, I. Chemistry of secondary polyphenols produced during processing of tea and selected foods. Int. J. Mol. Sci. 2010, 11, 14–40. [CrossRef]
68. Dipti, P.; Yogesh, B.; Kain, A.K.; Pauline, T.; Anju, B.; Sairam, M.; Singh, B.; Mongia, S.S.; Kumar, G.I.; Selvamurthy, W. Lead induced oxidative stress: BENEFICIAL effects of Kombucha tea. Biomed. Environ. Sci. 2003, 16, 276–282. [PubMed]
69. Gharib, O.A. Effects of Kombucha on oxidative stress induced nephrotoxicity in rats. Chin. Med. 2009, 27, 4–23. [CrossRef] [PubMed]
70. Bhattacharya, S.; Manna, P.; Gachhui, R.; Sil, P.C. Protective effect of kombucha tea against tertiary butyl hydroperoxide induced cytotoxicity and cell death in murine hepatocytes. Indian J. Exp. Biol. 2011, 49, 511–524.
71. Almajano, M.P.; Carbo, R.; Jiménez, J.A.L.; Gordon, M.H. Antioxidant and antimicrobial activities of tea infusions. Food Chem. 2008, 108, 55–63. [CrossRef]
72. Lee, W.; Kim, K.M.; Bae, J.S. Ameliorative effect of aspalathin and nothofagin from Rooibos (Aspalathus linearis) on HMGB1-Induced septic responses in vitro and in vivo. Am. J. Chin. Med. 2015, 43, 991–1012. [CrossRef]
73. Sanderson, M.; Mazibuko, S.E.; Joubert, E.; de Beer, D.; Johnson, R.; Pheiffer, C.; Louw, J.; Muller, C.J. Effects of fermented rooibos (Aspalathus linearis) on adipocyte differentiation. Phytomedicine 2014, 15, 109–117. [CrossRef]
74. Pringle, N.A.; Koekemoer, T.C.; Holzer, A.; Young, C.; Venables, L.; van de Venter, M. Potential therapeutic benefits of green and fermented Rooibos (Aspalathus linearis) in dermal wound healing. Planta Med. 2018, 84, 645–652. [CrossRef]