Abstract
Glycosidic bond of C-glycosides is difficult to be broken due to its chemical stability. Screening specific microbe from microbiota is a practical way to deglycosylate these compounds. In this study, a new strain W974-1 which is capable of cleaving C-glycosidic bonds was isolated from human gut microbiota by spread plate method. It deglycosylates flavonoid 8-C-glycosides such as orientin and vitexin to their aglycones with the enzymes secreted outside the bacterial cells. This strain was identified as Enterococcus avium by 16S rDNA sequencing, physiological and biochemical characterization.
Similar content being viewed by others
Data availability
The datasets generated during the current study are available from the corresponding author on reasonable request.
References
Blaut M, Schoefer L, Braune A (2003) Transformation of flavonoids by intestinal microorganisms. Int J Vitam Nutr Res 73:79–87. https://doi.org/10.1024/0300-9831.73.2.79
Braune A, Blaut M (2011) Deglycosylation of puerarin and other aromatic C-glucosides by a newly isolated human intestinal bacterium. Environ Microbiol 13:482–494. https://doi.org/10.1111/j.1462-2920.2010.02352.x
Braune A, Blaut M (2012) Intestinal bacterium Eubacterium cellulosolvens deglycosylates flavonoid C- and O-glucosides. Appl Environ Microbiol 78:8151–8153. https://doi.org/10.1128/AEM.02115-12
Braune A, Engst W, Blaut M (2016) Identification and functional expression of genes encoding flavonoid O- and C-glycosidases in intestinal bacteria. Environ Microbiol 18:2117–2129. https://doi.org/10.1111/1462-2920.12864
Brazier-Hicks M, Evans KM, Gershater MC, Puschmann H, Steel PG, Edwards R (2009) The C-glycosylation of flavonoids in cereals. J Biol Chem 284:17926–17934. https://doi.org/10.1074/jbc.M109.009258
Chen Y, Wang J, Jia XB, Tan XB, Hu M (2011) Role of intestinal hydrolase in the absorption of prenylated flavonoids present in Yinyanghuo. Molecules 16:1336–1348. https://doi.org/10.3390/molecules16021336
Courts FL, Williamson G (2015) The occurrence, fate and biological activities of C-glycosyl flavonoids in the human diet. Crit Rev Food Sci Nutr 55:1352–1367. https://doi.org/10.1080/10408398.2012.694497
Dong XZ, Cai MY (2001) Manual on the identification of common bacterial systems, 1st edn. Science Press, Beijing, pp 310–313
Garrity G, Brenner DJ, Krieg NR, Staley JR (2003) Bergey’s manual of systematic bacteriology, 2nd edn. Springer, New York, pp 197–198
Gechev TS, Hille J, Woerdenbag HJ, Benina M, Mehterov N, Toneva V, Fernie AR, Mueller-Roeber B (2014) Natural products from resurrection plants: potential for medical applications. Biotechnol Adv 32:1091–1101. https://doi.org/10.1016/j.biotechadv.2014.03.005
Guo LN, Qiao SS, Hu JH, Li DL, Zheng SQ, Shi DZ, Liu J, Wang RF (2017) Investigation of the effective components of the flowers of Trollius chinensis from the perspectives of intestinal bacterial transformation and intestinal absorption. Pharm Biol 55:1747–1758. https://doi.org/10.1080/13880209.2017.1321023
Hattori M, Akao T, Kobashi K, Namba T (1993) Cleavages of the O- and C-glucosyl bonds of anthrone and 10, 10’-bianthrone derivatives by human intestinal bacteria. Pharmacology 47:125–133. https://doi.org/10.1080/13880209.2017.1321023
Salem-Bekhit MM, Moussa IMI, Ahmed MMM, Elsherbini M, Alrejaie S (2011) Increasing prevalence of high-level gentamicin resistant enterococci: An emerging clinical problem. Afr J Microbiol Res 5:5713–5720. https://doi.org/10.5897/AJMR11.1124
Jin JS, Nishihata T, Kakiuchi N, Hattori M (2008) Biotransformation of C-glucosylisoflavone puerarin to estrogenic (3S)-equol in co-culture of two human intestinal bacteria. Biol Pharm Bull 31:1621–1625. https://doi.org/10.1248/bpb.31.1621
Kim DH, Jung EA, Sohng IS, Han JA, Kim TH, Han MJ (1998) Intestinal bacterial metabolism of flavonoids and its relation to some biological activities. Arch Pharm Res 21:17–23. https://doi.org/10.1007/BF03216747
Kim MH, Lee JK, Han JH (2015) Deglycosylation of isoflavone C-glycosides by newly isolated human intestinal bacteria. J Sci Food Agric 95:1925–1931. https://doi.org/10.1002/jsfa.6900
Liu Y, Liu Y, Dai Y, Xun LY, Hu M (2003) Enteric disposition and recycling of flavonoids and ginkgo flavonoids. J Altern Complement Med 9:631–640. https://doi.org/10.1089/107555303322524481
Liu LJ, Guo LN, Zhao C, Wu XW, Wang RF, Liu C (2015) Characterization of the intestinal absorption of seven flavonoids from the flowers of Trollius chinensis using the Caco-2 cell monolayer model. PLoS ONE 10:e0119263. https://doi.org/10.1371/journal.pone.0119263
Mori T, Kumano T, He H, Watanabe S, Senda M, Moriya T, Adachi N, Hori S, Terashita Y, Kawasaki M, Hashimoto Y, Awakawa T, Senda T, Abe I, Kobayashi M (2021) C-glycoside metabolism in the gut and in nature: Identification, characterization, structural analyses and distribution of C-C bond-cleaving enzymes. Nat Commun 12:6294. https://doi.org/10.1038/s41467-021-26585-1
Nakamura K, Komatsu K, Hattori M, Iwashima M (2013) Enzymatic cleavage of the C-glucosidic bond of puerarin by three proteins, Mn (2+), and oxidized form of nicotinamide adenine dinucleotide. Biol Pharm Bull 36:635–640. https://doi.org/10.1248/bpb.b12-01011
Nakamura K, Zhu S, Komatsu K, Hattori M, Iwashima M (2019) Expression and characterization of the human intestinal bacterial enzyme which cleaves the C-glycosidic bond in 3ʺ-oxo-puerarin. Biol Pharm Bull 42:417–423. https://doi.org/10.1248/bpb.b18-00729
Nakamura K, Zhu S, Komatsu K, Hattori M, Iwashima M (2020) Deglycosylation of the isoflavone C-glucoside puerarin by a combination of two recombinant bacterial enzymes and 3-oxo-glucose. Appl Environ Microbiol 86:e00607-00620. https://doi.org/10.1128/AEM.00607-20
Rechner AR, Kuhnle G, Bremner P, Hubbard GP, Moore KP, Rice-Evans CA (2002) The metabolic fate of dietary polyphenols in humans. Free Radic Biol Med 33:220–235. https://doi.org/10.1016/s0891-5849(02)00877-8
Sanugul K, Akao T, Nakamura N, Hattori M (2005) Two proteins, Mn2+, and low molecular cofactor are required for C-glucosyl-cleavage of mangiferin. Biol Pharm Bull 28:2035–2039. https://doi.org/10.1248/bpb.28.2035
Shin NR, Moon JS, Shin SY, Li L, Lee YB, Kim TJ, Han NS (2016) Isolation and characterization of human intestinal Enterococcus avium EFEL009 converting rutin to quercetin. Lett Appl Microbiol 62:68–74. https://doi.org/10.1111/lam.12512
Talhi O, Silva AMS (2012) Advances in C-glycosylflavonoid research. Curr Org Chem 16:859–896. https://doi.org/10.2174/138527212800194791
van Harten RM, Willems RJL, Martin NI, Hendrickx APA (2017) Multidrug-resistant Enterococcal infections: new compounds, novel antimicrobial therapies? Trends Microbiol 25:467–479. https://doi.org/10.1016/j.tim.2017.01.004
Wei B, Wang YK, Qiu WH, Wang SJ, Wu YH, Xu XW, Wang H (2020) Discovery and mechanism of intestinal bacteria in enzymatic cleavage of C-C glycosidic bonds. Appl Microbiol Biotechnol 104:1883–1890. https://doi.org/10.1007/s00253-019-10333-z
Wei B, Wang YK, Yu JB, Wang SJ, Yu YL, Xu XW, Wang H (2021) Discovery of novel glycoside hydrolases from C-glycoside-degrading bacteria using sequence similarity network analysis. J Microbiol 59:931–940. https://doi.org/10.1007/s12275-021-1292-4
Xiao J (2017) Dietary flavonoid aglycones and their glycosides: which show better biological significance? Crit Rev Food Sci Nutr 57:1874–1905. https://doi.org/10.1080/10408398.2015.1032400
Xiao J, Capanoglu E, Jassbi AR, Miron A (2016) Advance on the flavonoid C-glycosides and health benefits. Crit Rev Food Sci Nutr 56(Suppl 1):S29-45. https://doi.org/10.1080/10408398.2015.1067595
Xu J, Qian D, Jiang S, Guo J, Shang EX, Duan J, Yang J (2014) Application of ultra-performance liquid chromatography coupled with quadrupole time-of-flight mass spectrometry to determine the metabolites of orientin produced by human intestinal bacteria. J Chromatogr B Analyt Technol Biomed Life Sci 944:123–127. https://doi.org/10.1016/j.jchromb.2013.11.002
Zheng SQ, Geng D, Liu SY, Wang QQ, Liu SQ, Wang RF (2019) A newly isolated human intestinal bacterium strain capable of deglycosylating flavone C-glycosides and its functional properties. Microb Cell Fact 18:94. https://doi.org/10.1186/s12934-019-1144-7
Zhou Y, Zhang H, Peng C (2014) Puerarin: a review of pharmacological effects. Phytother Res 28:961–975. https://doi.org/10.1002/ptr.5083
Acknowledgements
This work was supported by the National Key R&D Program of China 2018YFC1704506.
Funding
Funding was provided by National Key R&D Program of China (2018YFC1704506).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
We declare that the research was conducted in the absence of any commercial or financial relationship that could be construed as a potential conflict of interest.
Additional information
Communicated by Erko Stackebrandt.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Wang, S., Liu, S., Wang, J. et al. A newly isolated human intestinal strain deglycosylating flavonoid C-glycosides. Arch Microbiol 204, 310 (2022). https://doi.org/10.1007/s00203-022-02881-2
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00203-022-02881-2