Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
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Bidirectional Interactions between Green Tea (GT) Polyphenols and Human Gut Bacteria

  • Se Rin Choi (Department of Bioscience and Biotechnology, Konkuk University) ;
  • Hyunji Lee (Department of Bioscience and Biotechnology, Konkuk University) ;
  • Digar Singh (Department of Bioscience and Biotechnology, Konkuk University) ;
  • Donghyun Cho (Amorepacific R&I Center) ;
  • Jin-Oh Chung (Amorepacific R&I Center) ;
  • Jong-Hwa Roh (Amorepacific R&I Center) ;
  • Wan-Gi Kim (Amorepacific R&I Center) ;
  • Choong Hwan Lee (Department of Bioscience and Biotechnology, Konkuk University)
  • Received : 2023.06.08
  • Accepted : 2023.06.26
  • Published : 2023.10.28
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Abstract

Green tea (GT) polyphenols undergo extensive metabolism within gastrointestinal tract (GIT), where their derivatives compounds potentially modulate the gut microbiome. This biotransformation process involves a cascade of exclusive gut microbial enzymes which chemically modify the GT polyphenols influencing both their bioactivity and bioavailability in host. Herein, we examined the in vitro interactions between 37 different human gut microbiota and the GT polyphenols. UHPLC-LTQ-Orbitrap-MS/MS analysis of the culture broth extracts unravel that genera Adlercreutzia, Eggerthella and Lactiplantibacillus plantarum KACC11451 promoted C-ring opening reaction in GT catechins. In addition, L. plantarum also hydrolyzed catechin galloyl esters to produce gallic acid and pyrogallol, and also converted flavonoid glycosides to their aglycone derivatives. Biotransformation of GT polyphenols into derivative compounds enhanced their antioxidant bioactivities in culture broth extracts. Considering the effects of GT polyphenols on specific growth rates of gut bacteria, we noted that GT polyphenols and their derivate compounds inhibited most species in phylum Actinobacteria, Bacteroides, and Firmicutes except genus Lactobacillus. The present study delineates the likely mechanisms involved in the metabolism and bioavailability of GT polyphenols upon exposure to gut microbiota. Further, widening this workflow to understand the metabolism of various other dietary polyphenols can unravel their biotransformation mechanisms and associated functions in human GIT.

Keywords

Acknowledgement

This paper was supported by Konkuk University Researcher Fund in 2021. This work was supported by the National Research Foundation of Korea(NRF) grant funded by the Korea government. (MSIT) (NRF-2023R1A2C1004930).

References

  1. Arumugam M, Raes J, Pelletier E, Paslier D le, Yamada T, Mende DR, et al. 2011. Enterotypes of the human gut microbiome. Nature 473: 174-180.  https://doi.org/10.1038/nature09944
  2. Ley RE, Hamady M, Lozupone C, Turnbaugh, PJ, Ramey RR, Bircher JS, et al. 2008. Evolution of mammals and their gut microbes. Science 320: 1647-1651.  https://doi.org/10.1126/science.1155725
  3. Bull MJ, Plummer NT, Part 1: The Human Gut Microbiome in Health and Disease. 2014. Integrative Medicine: Clin. J. 13: 17. 
  4. Shreiner AB, Kao JY, Young VB. The gut microbiome in health and in disease. 2015. Curr. Opin. Gastroenterol. 31: 69. 
  5. Kasprzak-Drozd K, Oniszczuk T, Stasiak M, Oniszczuk A. 2021. Beneficial effects of phenolic compounds on gut microbiota and metabolic syndrome. Int. J. Mol. Sci. 22: 3715. 
  6. Alves-Santos AM, Sugizaki CSA, Lima GC, Naves MMV. 2020. Prebiotic effect of dietary polyphenols: A systematic review. J. Funct. Foods 74: 104169. 
  7. Sun H, Chen Y, Cheng M, Zhang X, Zheng X, Zhang Z. 2018. The modulatory effect of polyphenols from green tea, oolong tea and black tea on human intestinal microbiota in vitro. J. Food Sci. Technol. 55: 399-407.  https://doi.org/10.1007/s13197-017-2951-7
  8. Da Silva Pinto M. Tea: a new perspective on health benefits. 2013. Food Res. Int. 53: 558-567.  https://doi.org/10.1016/j.foodres.2013.01.038
  9. Balentine DA, Wiseman SA, Bouwens LCM. 1997. The chemistry of tea flavonoids. Crit. Rev. Food Sci. Nutr. 37: 693-704.  https://doi.org/10.1080/10408399709527797
  10. Stalmach A, Mullen W, Steiling H, Williamson G, Lean MEJ, Crozier A. 2010. Absorption, metabolism, and excretion of green tea flavan-3-Ols in humans with an ileostomy. Mol. Nutr. Food Res. 54: 323-334.  https://doi.org/10.1002/mnfr.200900194
  11. Chen W, Zhu X, Lu Q, Zhang L, Wang X, Liu R. 2020. C-Ring cleavage metabolites of catechin and epicatechin enhanced antioxidant activities through intestinal microbiota. Food Res. Int. 135: 109271. 
  12. Liu Z, de Bruijn WJC, Bruins ME, Vincken JP. 2020. Reciprocal interactions between Epigallocatechin-3-Gallate (EGCG) and human gut microbiota in vitro. J. Agric. Food Chem. 68: 9804-9815.  https://doi.org/10.1021/acs.jafc.0c03587
  13. Rha CS, Jeong HW, Park S, Lee S, Jung YS, Kim DO. 2019. Antioxidative, anti-inflammatory, and anticancer effects of purified flavonol glycosides and aglycones in green tea. Antioxidants (Basel) 8: 278. 
  14. Dey P, Sasaki GY, Wei P, Li J, Wang L, Zhu J, et al. 2019. Green tea extract prevents obesity in male mice by alleviating gut dysbiosis in association with improved intestinal barrier function that limits endotoxin translocation and adipose inflammation. J. Nutr. Biochem. 67: 78-89.  https://doi.org/10.1016/j.jnutbio.2019.01.017
  15. Li Y, Rahman SU, Huang Y, Zhang Y, Ming P, Zhu L, et al. 2020. Green tea polyphenols decrease weight gain, ameliorate alteration of gut microbiota, and mitigate intestinal inflammation in canines with high-fat-diet-induced obesity. J. Nutr. Biochem. 78: 108324. 
  16. Liu YC, Li XY, Shen L. 2019. Modulation effect of tea consumption on gut microbiota. Appl. Microbiol. Biotechnol. 104: 981-987.  https://doi.org/10.1007/s00253-019-10306-2
  17. Braune A, Blaut M. 2016. Bacterial species involved in the conversion of dietary flavonoids in the human gut. Gut Microbes 7: 216-234.  https://doi.org/10.1080/19490976.2016.1158395
  18. Cueva C, Silva M, Pinillos I, Bartolome B, Moreno-Arribas MV. 2020. Interplay between dietary polyphenols and oral and gut microbiota in the development of colorectal cancer. Nutrients 12: 625. 
  19. Kwon MC, Kim YX, Lee S, Jung ES, Singh D, Sung J, et al. 2019. Comparative metabolomics unravel the effect of magnesium oversupply on tomato fruit quality and associated plant metabolism. Metabolites 9: 231. 
  20. Baranyi J, Roberts TA. 1994. A dynamic approach to predicting bacterial growth in food. Int. J. Food. Microbiol. 23: 277-294.  https://doi.org/10.1016/0168-1605(94)90157-0
  21. Cueva C, Gil-Sanchez I, Moreno-Arribas MV, Bartolome B. 2016. Interactions between wine polyphenols and gut microbiota. Wine Safety, Consumer Preference, and Human Health. pp. 259-278. 
  22. Rowland I, Gibson G, Heinken A, Scott K, Swann J, Thiele I, et al. 2018. Gut microbiota functions: Metabolism of nutrients and other food components. Eur. J. Nutr. 57: 1-24.  https://doi.org/10.1007/s00394-017-1445-8
  23. Takagaki A, Nanjo F. 2015. Bioconversion of (-)-Epicatechin, (+)-Epicatechin, (-)-Catechin, and (+)-Catechin by (-)-Epigallocatechin-metabolizing bacteria. Biol. Pharm. Bull. 38: 789-794.  https://doi.org/10.1248/bpb.b14-00813
  24. Sanchez-Patan F, Tabasco R, Monagas M, Requena T, Pelaez C, Moreno-Arribas, et al. 2012. Capability of Lactobacillus Plantarum IFPL935 to catabolize flavan-3-Ol compounds and complex phenolic extracts. J. Agric. Food Chem. 60: 7142-7151.  https://doi.org/10.1021/jf3006867
  25. Chen H, Hayek S, Rivera Guzman J, Gillitt ND, Ibrahim SA, Jobin C, et al. 2012. The microbiota is essential for the generation of black tea theaflavins-derived metabolites. PLoS One 7: e51001. 
  26. Santangelo R, Silvestrini A, Mancuso C. 2019. Ginsenosides, catechins, quercetin and gut microbiota: Current evidence of challenging interactions. Food Chem. Toxicol. 123: 42-49.  https://doi.org/10.1016/j.fct.2018.10.042
  27. Zhu MZ, Li N, Zhou F, Ouyang J, Lu D, Xu W, et al. 2019. Microbial bio-conversion of the chemical components in dark tea. Food Chem. 312: 126043-126043.  https://doi.org/10.1016/j.foodchem.2019.126043
  28. Kosuru RY, Roy A, Das SK, Bera S. 2018. Gallic acid and gallates in human health and disease: Do mitochondria hold the key to success? Mol. Nutr. Food Res. 62: 1700699. 
  29. Shin M, Park E, Lee H. 2019. Plant-inspired pyrogallol-containing functional materials. Adv. Funct. Mater. 29: 1903022. 
  30. Liu M, Xie H, Ma Y, Li H, Li C, Chen L, Jiang B, et al. 2020. High-performance liquid chromatography and metabolomics analysis of tannase metabolism of gallic acid and gallates in tea leaves. J. Agric. Food. Chem. 68: 4946-4954,  https://doi.org/10.1021/acs.jafc.0c00513
  31. Seifried HE, Anderson DE, Fisher EI, Milner JA. 2007. A review of the interaction among dietary antioxidants and reactive oxygen species. J. Nutr. Biochem. 18: 567-579  https://doi.org/10.1016/j.jnutbio.2006.10.007
  32. Duda-Chodak A, Tarko T, Satora P, Sroka P. 2015. Interaction of dietary compounds, especially polyphenols, with the intestinal microbiota: A review. Eur. J. Nutr. 54: 325-341.  https://doi.org/10.1007/s00394-015-0852-y
  33. Ozdal T, Sela DA, Xiao J, Boyacioglu D, Chen F, Capanoglu E. 2016. The reciprocal interactions between polyphenols and gut microbiota and effects on bio-accessibility. Nutrients 8: 78. 
  34. Xu J, Chen HB, Li SL. 2017. Understanding the molecular mechanisms of the interplay between herbal medicines and gut microbiota. Med. Res. Rev. 37: 1140-1185.  https://doi.org/10.1002/med.21431
  35. Zhang Z, Lv J, Pan L, Zhang Y. 2018. Roles and applications of probiotic Lactobacillus strains. Appl. Microbiol. Biotechnol. 102: 8135-8143.  https://doi.org/10.1007/s00253-018-9217-9
  36. Liu YW, Liong MT, Tsai YC. 2018. New perspectives of Lactobacillus Plantarum as a probiotic: The gut-heart-brain axis. J. Microbiol. 56: 601-613.  https://doi.org/10.1007/s12275-018-8079-2
  37. Zhang F, Li Y, Wang X, Wang S, Bi D. 2019. The impact of Lactobacillus Plantarum on the gut microbiota of mice with DSS-induced colitis. Biomed. Res. Int. 2019: 3921315. 
  38. Mu Q, Tavella VJ, Luo XM. 2018. Role of Lactobacillus Reuteri in human health and diseases. Front. Microbiol. 9: 757. 
  39. Ahn YJ, Kawamura T, Kim M, Yamamoto T, Mitsuoka T. 1991. Tea polyphenols: Selective growth inhibitors of Clostridium spp. Agric. Biol. Chem. 55: 1425-1426.  https://doi.org/10.1080/00021369.1991.10870770
  40. Guo P, Zhang K, Ma X, He P. 2020. Clostridium species as probiotics: Potentials and challenges. J. Anim. Sci. Biotechnol. 11: 24. 
  41. Zafar H, Saier MH. 2021. Gut Bacteroides species in health and disease. Gut Microbes 13: 1-20.  https://doi.org/10.1080/19490976.2020.1848158
  42. Gauffin CP, Santacruz A, Moya A, Sanz Y. 2012. Bacteroides Uniformis CECT 7771 ameliorates metabolic and immuno-logical dysfunction in mice with high-fat-diet induced obesity. PLoS One 7: e41079. 
  43. Fernandez-Murga ML, Yolanda S. 2016. Safety assessment of Bacteroides uniformis CECT 7771 isolated from stools of healthy breastfed infants. PLoS One 11: e0145503. 
  44. Zhou C, Zhao H, Xiao X, Chen B, Guo R, Wang Q, et al. 2020. Metagenomic profiling of the pro-inflammatory gut microbiota in ankylosing spondylitis. J. Autoimmun. 107: 102360. 
  45. Ezeji JC, Sarikonda DK, Hopperton A, Erkkila HL, Cohen DE, Martinez SP, et al. 2021. Parabacteroides Distasonis: Intriguing aerotolerant gut anaerobe with emerging antimicrobial resistance and pathogenic and probiotic roles in human health. Gut Microbes 13: 192241. 
  46. Reygaert WC. 2014. The antimicrobial possibilities of green tea. Front. Microbiol. 5: 434. 
  47. Michlmayr H, Kneifel W. 2014. β-glucosidase activities of lactic acid bacteria: Mechanisms, impact on fermented food and human health. FEMS Microbiol. Lett. 352: 1-10.  https://doi.org/10.1111/1574-6968.12348
  48. de Moraes Barros HR, Garcia-Villalba R, Tomas-Barberan FA, Genovese MI. 2016. Evaluation of the distribution and metabolism of polyphenols derived from cupuassu (Theobroma grandiflorum) in mice gastrointestinal tract by UPLC-ESI-QTOF. J. Funct. Foods 22: 477-489. https://doi.org/10.1016/j.jff.2016.02.009