Aqueous raw and ripe Pu-erh tea extracts alleviate obesity and alter cecal microbiota composition and function in diet-induced obese rats
Pu-erh tea is attracting increased attention worldwide because of its unique flavor and health effects, but its impact on the composition and function of the gut microbiota remains unclear. The aim of this study was to investigate the effects of aqueous extracts of fermented (ripe) and non-fermented (raw) Pu-erh teas on the composition and function of the intestinal microbiota of rats with diet-induced obesity. We conducted a comparative metagenomic and meta-proteomic investigation of the microbial communities in cecal samples taken from obese rats treated with or without extracts of raw or ripe Pu-erh teas. By analyzing the composition and diversity of 16S rRNA amplicons and expression profiles of 814 distinct proteins, we found that despite differences in the chemical compositions of raw and ripe Pu-erh teas, administration of either tea at two doses (0.15- and 0.40-g/kg body weight) significantly (P < 0.05) increased microbial diversity and changed the composition of cecal microbiota by increasing the relative abundances of Firmicutes and decreasing those of Bacteroidetes. Community metabolic processes, including sucrose metabolism, glycolysis, and syntheses of proteins, rRNAs, and antibiotics were significantly (P < 0.05) promoted or had a tendency (0.10 < P < 0.05) to be promoted due to the enrichment of relevant enzymes. Furthermore, evidence at population, molecular, and metabolic levels indicated that polyphenols of raw Pu-erh tea and their metabolites potentially promote Akkermansia muciniphila growth by stimulating a type II and III secretion system protein, the elongation factor Tu, and a glyceraldehyde-3-phosphate dehydrogenase. This study provides new evidence for the prebiotic effects of Pu-erh tea.
KeywordsPu-erh tea Obese rats 16S rRNA sequencing Meta-proteomics Composition and function Cecal microbiota
Y Xia and Y Kong wrote the manuscript. TDH designed and carried out the animal experiments. J Kong and R Akerbary carried out data collection and analyses. R Seviour contributed to discussion and reviewed/edited the manuscript. All authors read and approved the final manuscript.
This work was funded by the Major Project of Yunnan Provincial Education Department (research grant ZD2015015), Key Project of Yunnan Science and Technology Department (research grant 2016FA052), Kunming, China, and National Natural Science Foundation of China (31860029).
Compliance with ethical standards
The study was performed in accordance with the Helsinki Declaration and was approved by the Ethics Committee of the Animal Care and Use Committee of Institute of Medical Biology, Chinese Academy of Medical Sciences.
Conflict of interest
The authors declare that they have no competing interests.
- Anhê FF, Roy D, Pilon G, Dudonné S, Matamoros S, Varin TV, Garofalo C, Moine Q, Desjardins Y, Levy E, Marette A (2014) A polyphenol-rich cranberry extract protects from diet-induced obesity, insulin resistance and intestinal inflammation in association with increased Akkermansia spp. population in the gut microbiota of mice. Gut 64(6):872–883. https://doi.org/10.1136/gutjnl-2014-307142 CrossRefGoogle Scholar
- Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costelio EK, Fierer N, Pène AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. https://doi.org/10.1038/nmeth.f.303 CrossRefGoogle Scholar
- Everard A, Belzer C, Geurts L, Quwerkerk JP, Druart D, Bindels LB, Guiot Y, Derrien M, Muccioli GG, Delzenne NM, de Vos WM, Cani PD (2013) Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet- induced obesity. Proc Natl Acad Sci U S A 110(22):9066–9071. https://doi.org/10.1073/pnas.1219451110 CrossRefGoogle Scholar
- Pinto AJ, Raskin L (2012) PCR biases distort bacterial and archaeal community structure in pyrosequencing datasets. PLoS One 7.8:pe43093. https://doi.org/10.1371/journal.pone.0043093
- Roopchand DE, Carmody RN, Kuhn P, Moskal K, Rojas-Silva P, Turnbaugh PJ, Raskin I (2015) Dietary polyphenols promote growth of the gut bacterium Akkermansia muciniphila and attenuate high fat diet-induced metabolic syndrome. Diabetes 64(8):2847–2858. https://doi.org/10.2337/db14-1916 CrossRefGoogle Scholar
- Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing Mothur: an open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541. https://doi.org/10.1128/AEM.01541-09 CrossRefGoogle Scholar
- Seo DB, Jeong HW, Kim YJ, Kim S, Kim J, Lee JH, Joo K, Choi JK, Shin SS, Lee S (2017) Fermented green tea extract exhibits hypolipidaemic effects through the inhibition of pancreatic lipase and promotion of energy expenditure. British J Nutrition 117:177–186. https://doi.org/10.1017/S0007114516004621 CrossRefGoogle Scholar
- Wang D, Luo X, Zhong Y, Yang W, Xu MJ, Liu Y, Meng J, Yao P, Yan H, Liu L (2012) Pu-erh black tea extract supplementation attenuates the oxidative DNA damage and oxidative stress in Sprague–Dawley rats with renal dysfunction induced by subchronic 3-methyl-2-quinoxalin benzenevinylketo-1,4-dioxide exposure. Food Chem Toxicol 50:147–154. https://doi.org/10.1016/j.fct.2011.10.069 CrossRefGoogle Scholar
- Xu X, Wang P, Luo S, Luo Y, Jiang X, Hou Y, Shao W, Yang J (2011) Effects of Puer tea on hyperlipidemia prevention, antioxidation and vascular endothelium protection in SD rats. J Yunnan Agricultural University 26(2):260–264Google Scholar