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Polysaccharides from Fuzhuan brick tea (FBTPS), one of most important bioactive components in tea, showed various health-promoting functions. Our previous work demonstrated that the crude FBTPS (CFBTPS) could modulate the gut microbiota. However, which purified fraction in CFBTPS contributing to the modulation of gut microbiota remains unclear. Thus, the fermentation characteristics and probiotic activity of a purified fraction (FBTPS-2-1) of CFBTPS were evaluated in this work. The results showed that gut microbiota could utilize FBTPS-2-1 to produce short-chain fatty acids including acetic, propionic, n-butyric and n-valeric acids. FBTPS-2-1 could modulate the structure and metabolic pathways of gut microbiota. FBTPS-2-1 could increase the health-promoting gut microbiota such as Prevotellaceae and Bifidobacteriaceae, and decreased the harmful bacteria such as Enterobacteriaceae and Fusobacteriaceae. The results of metagenomics showed that Prevotella copri and Megamonas funiformis were the dominant bacteria after fermentation of FBTPS-2-1. Furthermore, FBTPS-2-1 could regulate the biosynthesis and metabolism pathways of gut microbiota. Thus, the enrichment of food with FBTPS-2-1 is expected as a potential strategy for promoting human health due to modulation of gut microbiota.


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Fermentation characteristics and probiotic activity of a purified fraction of polysaccharides from Fuzhuan brick tea

Show Author's information Guijie ChenaZiqi ZengaMinhao XiebYujia PengaWangting ZhouaWeiqi XuaYi SunaXiaoxiong Zenga( )Zhonghua Liuc,d( )
College of Food Science and Technology, Nanjing Agricultural University, Nanjing 210095, China
Collaborative Innovation Center for Modern Grain Circulation and Safety, College of Food Science and Engineering, Nanjing University of Finance and Economics, Nanjing 210023, China
Key Laboratory of Ministry of Education for Tea Science, Hunan Agricultural University, Changsha 410128, China
National Research Center of Engineering Technology for Utilization of Botanical Functional Ingredients, Changsha 410128, China

Peer review under responsibility of KeAi Communications Co., Ltd.

Abstract

Polysaccharides from Fuzhuan brick tea (FBTPS), one of most important bioactive components in tea, showed various health-promoting functions. Our previous work demonstrated that the crude FBTPS (CFBTPS) could modulate the gut microbiota. However, which purified fraction in CFBTPS contributing to the modulation of gut microbiota remains unclear. Thus, the fermentation characteristics and probiotic activity of a purified fraction (FBTPS-2-1) of CFBTPS were evaluated in this work. The results showed that gut microbiota could utilize FBTPS-2-1 to produce short-chain fatty acids including acetic, propionic, n-butyric and n-valeric acids. FBTPS-2-1 could modulate the structure and metabolic pathways of gut microbiota. FBTPS-2-1 could increase the health-promoting gut microbiota such as Prevotellaceae and Bifidobacteriaceae, and decreased the harmful bacteria such as Enterobacteriaceae and Fusobacteriaceae. The results of metagenomics showed that Prevotella copri and Megamonas funiformis were the dominant bacteria after fermentation of FBTPS-2-1. Furthermore, FBTPS-2-1 could regulate the biosynthesis and metabolism pathways of gut microbiota. Thus, the enrichment of food with FBTPS-2-1 is expected as a potential strategy for promoting human health due to modulation of gut microbiota.

Keywords: Gut microbiota, Polysaccharide, Fuzhuan brick tea, Fermentation characteristics

References(62)

[1]

A.M. Valdes, J. Walter, E. Segal, et al., Role of the gut microbiota in nutrition and health, Br. Med. J. 361 (2018) k2179. https://doi.org/10.1136/bmj.k2179

[2]

A. Lavelle, H. Sokol, Gut microbiota-derived metabolites as key actors in inflammatory bowel disease, Nat. Rev. Gastroenterol. Hepatol. 17 (2020) 223-237. https://doi.org/10.1038/s41575-019-0258-z

[3]

S.V. Lynch, O. Pedersen, The human intestinal microbiome in health and disease, New Engl. J. Med., 375 (2016) 2369-2379. https://doi.org/10.1056/NEJMra1600266

[4]

L.H. Morais, H.L. Schreiber, S.K. Mazmanian, The gut microbiota-brain axis in behaviour and brain disorders, Nat. Rev. Microbiol. 19 (2021) 241-255. https://doi.org/10.1038/s41579-020-00460-0

[5]

E.E. Canfora, R.C.R. Meex, K. Venema, et al., Gut microbial metabolites in obesity, NAFLD and T2DM, Nat. Rev. Endocrinol. 15 (2019) 261-273. https://doi.org/10.1038/s41574-019-0156-z

[6]

I. Nemet, P.P. Saha, N. Gupta, et al., A cardiovascular disease-linked gut microbial metabolite acts via adrenergic receptors, Cell 180 (2020) 862-877. https://doi.org/10.1016/j.cell.2020.02.016

[7]

Y. Peng, Y. Yan, P. Wan, et al., Gut microbiota modulation and anti-inflammatory properties of anthocyanins from the fruits of Lycium ruthenicum Murray in dextran sodium sulfate-induced colitis in mice, Free Radical Bio. Med. 136 (2019) 96-108. https://doi.org/10.1016/j.freeradbiomed.2019.04.005

[8]

K.D. LaCourse, C.D. Johnston, S. Bullman, The relationship between gastrointestinal cancers and the microbiota, Lancet Gastroenterol. Hepatol. 6 (2021) 498-509. https://doi.org/10.1016/S2468-1253(20)30362-9

[9]

Y. Fan, O. Pedersen, Gut microbiota in human metabolic health and disease, Nat. Rev. Microbiol. 19 (2020) 55-71. https://doi.org/10.1038/s41579-020-0433-9

[10]

Y. Han, H. Xiao, Whole food–based approaches to modulating gut microbiota and associated diseases, Annu. Rev. Food Sci. Technol. 11 (2020) 119-143. https://doi.org/10.1146/annurev-food-111519-014337

[11]

F.A. Tomás-Barberán, J.C. Espín, Effect of food structure and processing on (poly)phenol-gut microbiota interactions and the effects on human health, Annu. Rev. Food Sci. Technol. 10 (2019) 221-238. https://doi.org/10.1146/annurev-food-032818-121615

[12]

J. Doré, H. Blottière, The influence of diet on the gut microbiota and its consequences for health, Curr. Opin. Biotechnol. 32 (2015) 195-199. https://doi.org/10.1016/j.copbio.2015.01.002

[13]

C.L. Gentile, T.L. Weir, The gut microbiota at the intersection of diet and human health, Science 362 (2018) 776-780. https://doi.org/10.1126/science.aau5812

[14]

G. Roeselers, J. Bouwman, E. Levin, The human gut microbiome, diet, and health: "post hoc non ergo propter hoc", Trends Food Sci. Technol. 57 (2016) 302-305. https://doi.org/10.1016/j.tifs.2016.08.010

[15]

J. Verspreet, B. Damen, W.F. Broekaert, et al., A critical look at prebiotics within the dietary fiber concept, Annu. Rev. Food Sci. Technol. 7 (2016) 167-190. https://doi.org/10.1146/annurev-food-081315-032749

[16]

M.L. Patnode, Z.W. Beller, N.D. Han, et al., Interspecies competition impacts targeted manipulation of human gut bacteria by fiber-derived glycans, Cell 179 (2019) 59-73. https://doi.org/10.1016/j.cell.2019.08.011

[17]

Y.E. Tuncil, R.D. Thakkar, S. Arioglu-Tuncil, et al., Subtle variations in dietary-fiber fine structure differentially influence the composition and metabolic function of gut microbiota, mSphere 5 (2020) e00180-20. https://doi.org/10.1128/mSphere.00180-20

[18]

G.R. Gibson, R. Hutkins, M.E. Sanders, et al., The International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics, Nat. Rev. Gastroenterol. Hepatol. 14 (2017) 491-502. https://doi.org/10.1038/nrgastro.2017.75

[19]

B. Chassaing, T. van de Wiele, J. de Bodt, et al., Dietary emulsifiers directly alter human microbiota composition and gene expression ex vivo potentiating intestinal inflammation, Gut 66 (2017) 1414-1427. https://doi.org/10.1136/gutjnl-2016-313099

[20]

B. Chassaing, O. Koren, J.K. Goodrich, et al., Dietary emulsifiers impact the mouse gut microbiota promoting colitis and metabolic syndrome, Nature 519 (2015) 92-96. https://doi.org/10.1038/nature14232

[21]

V. Singh, B.S. Yeoh, R.E. Walker, et al., Microbiota fermentation-NLRP3 axis shapes the impact of dietary fibres on intestinal inflammation, Gut 68 (2019) 1801-1812. http://doi.org/10.1136/gutjnl-2018-316250

[22]

G. Chen, M. Xie, Z. Dai, et al., Kudingcha and Fuzhuan brick tea prevent obesity and modulate gut microbiota in high-fat diet fed mice, Mol. Nutr. Food Res. 62 (2018) 1700485. https://doi.org/10.1002/mnfr.201700485

[23]

G. Chen, M. Xie, P. Wan, et al., Digestion under saliva, simulated gastric and small intestinal conditions and fermentation in vitro by human intestinal microbiota of polysaccharides from Fuzhuan brick tea, Food Chem. 244 (2018) 331-339. https://doi.org/10.1016/j.foodchem.2017.10.074

[24]

G. Chen, M. Xie, P. Wan, et al., Fuzhuan brick tea polysaccharides attenuate metabolic syndrome in high-fat diet induced mice in association with modulation in the gut microbiota, J. Agric. Food Chem., 66 (2018) 2783-2795. https://doi.org/10.1021/acs.jafc.8b00296

[25]

A.C. Keller, T.L. Weir, C.D. Broeckling, et al., Antibacterial activity and phytochemical profile of fermented Camellia sinensis (Fuzhuan tea), Food Res. Int. 53 (2013) 945-949. https://doi.org/10.1016/j.foodres.2013.04.023

[26]

Y. Wang, A. Xu, P. Liu, et al., Effects of Fuzhuan brick-tea water extract on mice infected with E. coli O157:H7, Nutrients 7 (2015) 5309-5326. https://doi.org/10.3390/nu7075218

[27]

G. Chen, M. Wang, M. Xie, et al., Evaluation of chemical property, cytotoxicity and antioxidant activity in vitro and in vivo of polysaccharides from Fuzhuan brick teas, Int. J. Biol. Macromol. 116 (2018) 120-127. https://doi.org/10.1016/j.ijbiomac.2018.04.184

[28]

B. Liu, T. Yang, L. Zeng, et al., Crude extract of Fuzhuan brick tea ameliorates DSS-induced colitis in mice, Int. J. Food Sci. Technol. 51 (2016) 2574-2582. https://doi.org/10.1111/ijfs.13241

[29]

M.T. Foster, C.L. Gentile, K. Cox-York, et al., Fuzhuan tea consumption imparts hepatoprotective effects and alters intestinal microbiota in high saturated fat diet-fed rats, Mol. Nutr. Food Res. 60 (2016) 1213-1220. https://doi.org/10.1002/mnfr.201500654

[30]

M. Wang, G. Chen, D. Chen, et al., Purified fraction of polysaccharides from Fuzhuan brick tea modulates the composition and metabolism of gut microbiota in anaerobic fermentation in vitro, Int. J. Biol. Macromol. 140 (2019) 858-870. https://doi.org/10.1016/j.ijbiomac.2019.08.187

[31]

G. Chen, Y. Bai, Z. Zeng, et al., Structural characterization and immunostimulatory activity of heteropolysaccharides from Fuzhuan brick tea, J. Agric. Food Chem. 69 (2021) 1368-1378. https://doi.org/10.1021/acs.jafc.0c06913

[32]

D. Chen, G. Chen, P. Wan, et al., Digestion under saliva, simulated gastric and small intestinal conditions and fermentationin in vitro of polysaccharides from the flowers of Camellia sinensis induced by human gut microbiota, Food Funct. 8 (2017) 4619-4629. https://doi.org/10.1039/c7fo01024a

[33]

A. Koh, F. De Vadder, P. Kovatcheva-Datchary, et al., From dietary fiber to host physiology: short-chain fatty acids as key bacterial metabolites, Cell 165 (2016) 1332-1345. https://doi.org/10.1016/j.cell.2016.05.041

[34]

H. Wang, G. Chen, X. Li, et al., Yeast β-glucan, a potential prebiotic, showed a similar probiotic activity to inulin, Food Funct. 11 (2020) 10386-10396. https://doi.org/10.1039/d0fo02224a

[35]

J. Hu, S. Nie, C. Li, et al., In vitro fermentation of polysaccharide from the seeds of Plantago asiatica L. by human fecal microbiota, Food Hydrocoll. 33 (2013) 384-392. https://doi.org/10.1016/j.foodhyd.2013.04.006

[36]

J. Fernández, S. Redondo-Blanco, I. Gutiérrez-del-Río, et al., Colon microbiota fermentation of dietary prebiotics towards short-chain fatty acids and their roles as anti-inflammatory and antitumour agents: a review, J. Funct. Foods 25 (2016) 511-522. https://doi.org/10.1016/j.jff.2016.06.032

[37]

K. Makki, E.C. Deehan, J. Walter, et al., The impact of dietary fiber on gut microbiota in host health and disease, Cell Host Microbe. 23 (2018) 705-715. https://doi.org/10.1016/j.chom.2018.05.012

[38]

B. Dalile, L. Van Oudenhove, B. Vervliet, et al., The role of short-chain fatty acids in microbiota-gut-brain communication, Nat. Rev. Gastroenterol. Hepatol. 16 (2019) 461-478. https://doi.org/10.1038/s41575-019-0157-3

[39]

B. van der Hee, J.M. Wells, Microbial regulation of host physiology by short-chain fatty acids, Trends Microbiol. (2021) https://doi.org/10.1016/j.tim.2021.02.001

[40]

E.E. Canfora, J.W. Jocken, E.E. Blaak, Short-chain fatty acids in control of body weight and insulin sensitivity, Nat. Rev. Endocrinol. 11 (2015) 577-591. https://doi.org/10.1038/nrendo.2015.128

[41]

T. Di, G. Chen, Y. Sun, et al., In vitro digestion by saliva, simulated gastric and small intestinal juices and fermentation by human fecal microbiota of sulfated polysaccharides from Gracilaria rubra, J. Funct. Foods 40 (2018) 18-27. https://doi.org/10.1016/j.jff.2017.10.040

[42]

Y. Rui, P. Wan, G. Chen, et al., Simulated digestion and fermentation in vitro by human gut microbiota of intra- and extra-cellular polysaccharides from Aspergillus cristatus, LWT-Food Sci. Technol. 116 (2019) 108508. https://doi.org/10.1016/j.lwt.2019.108508

[43]

M. Xie, G. Chen, P. Wan, et al., Modulating effects of dicaffeoylquinic acids from Ilex kudingcha on intestinal microecology in vitro, J. Agric. Food Chem. 65 (2017) 10185-10196. https://doi.org/10.1021/acs.jafc.7b03992

[44]

P.J. Turnbaugh, R.E. Ley, M.A. Mahowald, et al., An obesity-associated gut microbiome with increased capacity for energy harvest, Nature 444 (2006) 1027-1031. https://doi.org/10.1038/nature05414

[45]

P.J. Turnbaugh, M. Hamady, T. Yatsunenko, et al., A core gut microbiome in obese and lean twins, Nature 457 (2009) 480-484. https://doi.org/10.1038/nature07540

[46]

R.E. Ley, Prevotella in the gut: choose carefully, Nat. Rev. Gastroenterol. Hepatol. 13 (2016) 69-70. https://doi.org/10.1038/nrgastro.2016.4

[47]

A. Tett, K.D. Huang, F. Asnicar, et al., The Prevotella copri complex comprises four distinct clades underrepresented in westernized populations, Cell Host Microbe. 26 (2019) 666-679. https://doi.org/10.1016/j.chom.2019.08.018

[48]

T. Yu, Y. Wang, S. Chen, et al., Low-molecular-weight chitosan supplementation increases the population of Prevotella in the cecal contents of weanling pigs, Front. Microbiol. 8 (2017) 2182. https://doi.org/10.3389/fmicb.2017.02182

[49]

G.D. Wu, J. Chen, C. Hoffmann, et al., Linking long-term dietary patterns with gut microbial enterotypes, Science 334 (2011) 105-108. https://doi.org/10.1126/science.1208344

[50]

E.J.C. Gálvez, A. Iljazovic, L. Amend, et al., Distinct polysaccharide utilization determines interspecies competition between intestinal Prevotella spp., Cell Host Microbe. 28 (2020) 838-852. https://doi.org/10.1016/j.chom.2020.09.012

[51]

H. Fehlner-Peach, C. Magnabosco, V. Raghavan, et al., Distinct polysaccharide utilization profiles of human intestinal Prevotella copri isolates, Cell Host Microbe. 26 (2019) 680-690. https://doi.org/10.1016/j.chom.2019.10.013

[52]

N. Péan, A. Le Lay, F. Brial, et al., Dominant gut Prevotella copri in gastrectomised non-obese diabetic Goto–Kakizaki rats improves glucose homeostasis through enhanced FXR signalling, Diabetologia 63 (2020) 1223-1235. https://doi.org/10.1007/s00125-020-05122-7

[53]

P.J. Vuillermin, M.O. Hely, F. Collier, et al., Maternal carriage of Prevotella during pregnancy associates with protection against food allergy in the offspring, Nat. Commun. 11 (2020) 1452. https://doi.org/10.1038/s41467-020-14552-1

[54]

G. Precup, D. Vodnar, Gut Prevotella as a possible biomarker of diet and its eubiotic versus dysbiotic roles: a comprehensive literature review, Br. J. Nutr. 122 (2019) 131-140. https://doi.org/10.1017/S0007114519000680

[55]

P. Qin, Y. Zou, Y. Dai, et al., Characterization a novel butyric acid-producing bacterium Collinsella aerofaciens subsp. Shenzhenensis subsp. Nov., Microorganisms 7 (2019) 78. https://doi.org/10.3390/microorganisms7030078

[56]

A.P. Allen, W. Hutch, Y.E. Borre, et al., Bifidobacterium longum 1714 as a translational psychobiotic: modulation of stress, electrophysiology and neurocognition in healthy volunteers, Transl. Psychiatry 6 (2016) 939. https://doi.org/10.1038/tp.2016.191

[57]

C.B. Wong, T. Odamaki, J. Xiao, Beneficial effects of Bifidobacterium longum subsp. longum BB536 on human health: modulation of gut microbiome as the principal action, J. Funct. Foods 54 (2019) 506-519. https://doi.org/10.1016/j.jff.2019.02.002

[58]

Z. Fan, B. Yang, R.P. Ross, et al., Protective effects of Bifidobacterium adolescentis on collagen-induced arthritis in rats depend on timing of administration, Food Funct. 11 (2020) 4499-4511. https://doi.org/10.1039/D0FO00077A

[59]

G. Wang, T. Jiao, Y. Xu, et al., Bifidobacterium adolescentis and Lactobacillus rhamnosus alleviate non-alcoholic fatty liver disease induced by a high-fat, high-cholesterol diet through modulation of different gut microbiota-dependent pathways, Food Funct. 11 (2020) 6115-6127. https://doi.org/10.1039/c9fo02905b

[60]

S. Zeng, S. Li, P. Xiao, et al., Citrus polymethoxyflavones attenuate metabolic syndrome by regulating gut microbiome and amino acid metabolism, Sci. Adv. 6 (2020) eaax6208. https://doi.org/10.1126/sciadv.aax6208

[61]

J.M. Green, M.J. Barratt, M. Kinch, et al., Food and microbiota in the FDA regulatory framework, Science 357 (2017) 39-40. https://doi.org/10.1126/science.aan0836

[62]

R.Y. Chen, I. Mostafa, M.C. Hibberd, et al., A Microbiota-directed food intervention for undernourished children, New Engl. J. Med. 384 (2021) 1517-1528. https://doi.org/10.1056/NEJMoa2023294

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Publication history

Received: 30 June 2021
Revised: 03 September 2021
Accepted: 05 September 2021
Published: 04 February 2022
Issue date: May 2022

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© 2022 Beijing Academy of Food Sciences.

Acknowledgements

The study was supported by the National Natural Science Foundation of China (No.32001645 and No.31972025), the National Key Research and Development Program of China (2018YFC1604404), and the Fundamental Research Funds for the Central Universities (KJQN202154).

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This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

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