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Research Article | Open Access

Amelioration of metabolic disorders by a mushroom-derived polyphenols correlates with the reduction of Ruminococcaceae in gut of DIO mice

Li Suna,b,#Li Baoc,#Dorji Phurbud,#Shanshan Qiaoa,bShanshan Suna,eYangzom PermadHongwei Liua,b( )
State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100864, China
Savaid Medicine School, University of Chinese Academy of Sciences, Beijing 100864, China
Beijing Shijitan Hospital, Capital Medicinal University, Beijing 100864, China
Tibet Plateau Institute of Biology, Lhasa 850000, China
School of Life Sciences, University of Science and Technology of China, Hefei 230026, China

# These authors contributed equally.

Peer review under responsibility of KeAi Communications Co., Ltd

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Abstract

A polyphenolic alkaloid-enriched extract (PAE) was prepared from the fruiting bodies of a wild edible mushroom Sarcodon leucopus. Oral administration of PAE reduced hyperglycemia, hyperlipidemia, hepatic steatosis, and LPS-related inflammation in high fat diet-induced obese (DIO) mice. Furthermore, we show that PAE produces taxonomic and predicted functional changes in the gut microbiome of DIO mice. A significant decrease in the family of Ruminococcaceae, especially the secondary bile acid-producing bacteria of Intestinimonas and Anaerotruncus, is detected in the gut microbiome of PAE-treate mice. Accordingly, reductions of deoxycholic acid and lithocholic acid are found in the feces of PAE-treated DIO mice, which benefits for the intestinal integrity and the reduction of inflammation. A gut microbiota related mechanism for the anti-metabolic syndrome effects of the PAE is proposed. We suppose the polyphenolic alkaloid extract from S. leucopus be a new and beneficial prebiotic regulating glucose and lipid metabolisms.

References

[1]

G.S. Hotamisligil, Inflammation and metabolic disorders, Nature 444(7121) (2006) 860-867. https://doi.org/10.1038/nature05485.

[2]

K.M. Flegal, B.I. Graubard, D.F. Williamson, et al., Cause-specific excess deaths associated with underweight, overweight, and obesity, JAMA 298(17) (2007) 2028-2037. https://doi.org/10.1001/jama.298.17.2028.

[3]

N. Mendez-Sanchez, V.C. Cruz-Ramon, O.L. Ramirez-Perez, et al., New aspects of lipotoxicity in nonalcoholic steatohepatitis, Int. J. Mol. Sci. 19(7) (2018) 2034. https://doi.org/10.3390/ijms19072034.

[4]

K. Bhaskaran, I. Douglas, H. Forbes, et al., Body-mass index and risk of 22 specific cancers: a population-based cohort study of 5.24 million UK adults, Lancet 384(9945) (2014) 755-765. https://doi.org/10.1016/S0140-6736(14)60892-8.

[5]

M. Arnold, N. Pandeya, G. Byrnes, et al., Global burden of cancer attributable to high body-mass index in 2012: a population-based study, Lancet Oncol. 16(1) (2015) 36-46. https://doi.org/10.1016/S1470-2045(14)71123-4.

[6]

F. D'Aversa, A. Tortora, G, Laniro, et al., Gut microbiota and metabolic syndrome. Intern. Emerg. Med. 8 (1) (2013) 11-15. https://doi.org/10.1007/s11739-013-0916-z.

[7]

G. Muscogiuri, E. Cantone, S. Cassarano, et al., Gut microbiota: a new path to treat obesity, Int. J. Obesity 9(1) (2019) 10-19. https://doi.org/10.1038/s41367-019-0011-7.

[8]

L.P. Zhao, The gut microbiota and obesity: from correlation to causality, Nat. Rev. Microbiol. 11(9) (2013) 639-647. https://doi.org/10.1038/nrmicro3089.

[9]

S. Eaimworawuthikul, P. Thiennimitr, N. Chattipakorn, et al., Diet-induced obesity, gut microbiota and bone, including alveolar bone loss, Arch. Oral Biol. 78 (2017) 65-81. https://doi.org/10.1016/j.archoralbio.2017.02.009.

[10]

D.K. Dahiya, Renuka, M. Puniya, et al., Gut microbiota modulation and its relationship with obesity using prebiotic fibers and probiotics: a review, Front. Microbiol. 8(563) (2017) 563. https://doi.org/10.3389/fmicb.2017.00563.

[11]

P.J. Curtis, V. van der Velpen, L. Berends, et al., Blueberries improve biomarkers of cardiometabolic function in participants with metabolic syndrome-results from a 6-month, double-blind, randomized controlled trial, Am. J. Clin. Nutr. 109(6) (2019) 1535-1545. https://doi.org/10.1093/ajcn/nqy380.

[12]

S. Rabiei, M. Hedayati, B. Rashidkhani, et al., The effects of synbiotic supplementation on body mass index, metabolic and inflammatory biomarkers, and appetite in patients with metabolic syndrome: a tripleblind randomized controlled trial, J. Dietary Suppl. 16(3) (2019) 294-306. https://doi.org/10.1080/19390211.2018.1455788.

[13]

J. Zhu, H. Chen, Z.X. Song, et al., Effects of ginger (Zingiber officinale Roscoe) on type 2 diabetes mellitus and components of the metabolic syndrome: a systematic review and meta-analysis of randomized controlled trials, Evid. -Based Compl. Alt. 2018(1) (2018) 5692962. https://doi.org/10.1155/2018/5692962.

[14]

L.J. Bernini, S.A.N. Colado, A.H.B. de Souza, et al., Effect of Bifidobacterium lactis HN019 on inflammatory markers and oxidative stress in subjects with and without the metabolic syndrome, Brit. J. Nutr. 120(6) (2018) 645-652. https://doi.org/10.1017/S0007114518001861.

[15]
L.H. Quan, C.H. Zhang, M. Dong, et al., Myristoleic acid produced by enterococci reduces obesity through brown adipose tissue activation, Gut (2019). https://doi.org/10.1136/gutjnl-2019-319114.
[16]

Y. Luo, J.L. Fang, K. Yuan, et al., Ameliorative effect of purified anthocyanin from Lycium ruthenicum on atherosclerosis in rats through synergistic modulation of the gut microbiota and NF-κB/SREBP-2 pathways, J. Funct. Foods 59 (2019) 223-233. https://doi.org/10.1016/j.jff.2019.05.038.

[17]

K. Wang, L. Bao, N. Zhou, et al., Structural modification of natural product ganomycin I leading to discovery of a α-glucosidase and HMG-CoA reductase dual inhibitor improving obesity and metabolic dysfunction in vivo, J. Med. Chem. 61(8) (2018) 3609-3625. https://doi.org/10.1021/acs.jmedchem.8b00107.

[18]

C.J. Chang, C.S. Lin, C.C. Lu, et al., Ganoderma lucidum reduces obesity in mice by modulating the composition of the gut microbiota, Nat. Commun. 6 (2015) 7489. https://doi.org/10.1038/ncomms8489.

[19]

Y.Y. Pan, F. Zeng, W.L. Guo, et al., Effect of Grifola frondosa 95% ethanol extract on lipid metabolism and gut microbiota composition in high-fat diet-fed rats, Food Funct. 9(12) (2018) 6269-6279. https://doi.org/10.1039/C8FO01116H.

[20]

O.O. Ogbole, A.O. Nkumah, A.U. Linus, et al., Molecular identification, in vivo and in vitro activities of Calvatia gigantea (macro-fungus) as an antidiabetic agent, Mycology 10(3) (2019) 166-173. https://doi.org/10.1080/21501203.2019.1595204.

[21]

K.M. Ukwatta, J.L. Lawrence, C.D. Wijayarathna, The study of antimicrobial, anti-cancer, anti-inflammatory and α-glucosidase inhibitory activities of Nigronapthaphenyl, isolated from an extract of Nigrospora sphaerica, Mycology 10(4) (2019) 222-228. https://doi.org/10.1080/2150120 3.2019.1620892.

[22]

Q.M. Wang, K. Lu, F.H. Li, et al., Polyphenols from Morchella angusticepes peck attenuate d-galactosamine/lipopolysaccharide-induced acute hepatic failture in mice, J. Funct. Foods 58 (2019) 248-254. https://doi.org/10.1016/j.jff.2019.04.064.

[23]

M. Jayachandran, J.B. Xiao, B.J. Xu, A critical review on health promoting benefits of edible mushrooms through gut microbiota, Int. J. Mol. Sci. 18(9) (2017) 1934. https://doi.org/10.3390/ijms18091934.

[24]

N. Talhaoui, T. Vezza, A.M. Gómez-Caravaca, et al., Phenolic compounds and in vitro immunomodulatory properties of three Andalusian olive leaf extracts, J. Funct. Foods 22 (2016) 270-277. https://doi.org/10.1016/j.jff.2016.01.037.

[25]

H. Ma, B. Zhang, Y. Hu, et al., Correlation analysis of intestinal redox state with the gut microbiota reveals the positive intervention of tea polyphenols on hyperlipidemia in high fat diet fed mice, J. Agr. Food Chem. 67(26) (2019) 7325-7335. https://doi.org/10.1021/acs.jafc.9b02211.

[26]

M.K. Kemelo, A. Horinek, N.K. Canová, et al., Comparative effects of quercetin and SRT1720 against D-galactosamine/lipopolysaccharide-induced hepatotoxicity in rats: biochemical and molecular biological investigations, Eur. Rev. Med. Pharmaco. 20(2) (2016) 363.

[27]

M. Quiñones, L. Guerrero, S. Fernández-Vallinas, et al., Involvement of nitric oxide and prostacyclin in the antihypertensive effect of lowmolecular-weight procyanidin rich grape seed extract in male spontaneously hypertensive rats, J. Funct. Foods 6(1) (2014) 419-427. https://doi.org/10.1016/j.jff.2013.11.008.

[28]

M. Pinent, M. Blay, M.C. Bladé, et al., Grape seed-derived procyanidins have an antihyperglycemic effect in streptozotocin-induced diabetic rats and insulinomimetic activity in insulin-sensitive cell lines, Endocrinology 145(11) (2004) 4985-4990. https://doi.org/10.1210/en.2004-0764.

[29]

T.T. Chen, A.B. Liu, S. Sun, et al., Green tea polyphenols modify the gut microbiome in db/db mice as co-abundance groups correlating with the blood glucose lowering effect, Mol. Nutr. Food Res. 63(8) (2019). https://doi.org/10.1002/mnfr.201801064.

[30]

J.H. Liu, Z. He, N. Ma, et al., Beneficial effects of dietary polyphenols on highfat diet-induced obesity linking with modulation of gut microbiota, J. Agr. Food Chem. 68(1) (2020) 33-47. https://doi.org/10.1021/acs.jafc.9b06817.

[31]

K. Ma, J.J. Han, L. Bao, et al., Two sarcoviolins with antioxidative and α-glucosidase inhibitory activity from the edible mushroom Sarcodon leucopus collected in Tibet, J. Nat. Prod. 77(4) (2014) 942-947. https://doi.org/10.1021/np401026b.

[32]

M.X. Byndloss, E.E. Olsan, F. Rivera-Chávez, et al., Microbiota-activated PPAR-γ signaling inhibits dysbiotic Enterobacteriaceae expansion, Science 357(6351) (2017) 570. https://doi.org/10.1126/science.aam9949.

[33]

J. Yang, K.X. Liu, J.M. Qu, et al., The changes induced by cyclophosphamide in intestinal barrier and microflora in mice, Eur. J. Pharmacol. 714(1-3) (2013) 120-124. https://doi.org/10.1016/j.ejphar.2013.06.006.

[34]

Q. Christian, P. Elmar, Y. Pelin, et al., The SILVA ribosomal RNA gene database project: improved data processing and web-based tools, Nucleic Acids Res. 41 (D1) (2012). https://doi.org/10.1093/nar/gks1219.

[35]

R.C. Edgar, MUSCLE: multiple sequence alignment with high accuracy and high throughput, Nucleic Acids Res. 32(5) (2004) 1792-1797. https://doi.org/10.1093/nar/gkh340.

[36]

Q. Wang, G.M. Garrity, J.M. Tiedje, et al., Naive bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy, Appl. Environ. Microb. 73(16) (2007) 5261-5267.

[37]

W.Y.Shi, H.Y.Qi, Q.L.Sun, et al., gcMeta: a global catalogue of metagenomics platform to support the archiving, standardization and analysis of microbiome data, Nucleic Acids Res.47(D1) (2019) D637-D648.https://doi.org/10.1093/nar/gky1008.

[38]

J.Henao-Mejia, E.Elinav, C.C.Jin, et al., Inflammasome-mediated dysbiosis regulates progression of NAFLD and obesity, Nature 482(7384) (2012) 179-185.https://doi.org/10.1038/nature10809.

[39]

M.Manco, L.Putignani, G.F.Bottazzo, Gut microbiota, lipopolysaccharides, and innate immunity in the pathogenesis of obesity and cardiovascular risk, Endocr.Rev.31(6) (2010) 817-844.https://doi.org/10.1210/er.2009-0030.

[40]

P.D.Cani, R.Bibiloni, C.Knauf, et al., Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice, Diabetes 57(6) (2008) 1470-1481.https://doi.org/10.2337/db07-1403.

[41]

T.Pelaseyed, J.H.Bergstrom, J.K.Gustafsson, et al., The mucus and mucins of the goblet cells and enterocytes provide the first defense line of the gastrointestinal tract and interact with the immune system, Immun.Rev.260(1) (2014) 8-20.https://doi.org/10.1111/imr.12182.

[42]

N.O.Kaakoush, M.J.Morris, More flavor for flavonoid-based interventions? Trends Mol.Med.23(4) (2017) 293-295.https://doi.org/10.1016/j.molmed.2017.02.008.

[43]

M.Rajilić-Stojanović, D.M.Jonkers, A.Salonen, et al., Intestinal microbiota and diet in IBS: causes, consequences, or epiphenomena, Am.J.Gastroenterol.110(2) (2015) 278-287.https://doi.org/10.1038/ajg.2014.427.

[44]

N.R.Shin, J.C.Lee, H.Y.Lee, et al., An increase in the Akkermansia spp.population induced by metformin treatment improves glucose homeostasis in diet-induced obese mice, Gut 63(5) (2014) 727-735.https://doi.org/10.1136/gutjnl-2012-303839.

[45]

P.F.Xu, J.L.Wang, F.Hong, et al., Melatonin prevents obesity through modulation of gut microbiota in mice, J.Pineal.Res.62(4) (2017) e12399.https://doi.org/10.1111/jpi.12399.

[46]

R.A.Haeusler, B.Astiarraga, S.Camastra, et al., Human insulin resistance is associated with increased plasma levels of 12α-hydroxylated bile acids, Diabetes 62(12) (2013) 4184-4191.https://doi.org/10.2337/db13-0639.

[47]

B.Cariou, M.Chetiveaux, Y.Zaïr, et al., Fasting plasma chenodeoxycholic acid and cholic acid concentrations are inversely correlated with insulin sensitivity in adults, Nutr.Metab. 8(1) (2011) 48.https://doi.org/10.1186/1743-7075-8-48.

[48]

S.Yoshimoto, T.M.Loo, K.Atarashi, et al., Obesity-induced gut microbial metabolite promotes liver cancer through senescence secretome, Nature 499(7456) (2014) 97-101.https://doi.org/10.1038/nature12347.

[49]

H.Lin, Y.An, H.Tang, et al., Alterations of bile acids and gut microbiota in obesity induced by high fat diet in rat model, J.Agr.Food Chem. 67(13) (2019) 3624-3632.https://doi.org/10.1021/acs.jafc.9b00249.

[50]

J.E.Wells, P.B.Hylemon, Identification and characterization of a bile acid 7α-dehydroxylation operon in Clostridium sp.Strain TO-931, a highly active 7α-dehydroxylating strain isolated from human feces, Appl.Environ.Microbiol.66(3) (2000) 1107-1113.https://doi.org/10.1128/AEM.66.3.1107-1113.2000.

[51]
M. Vital, T. Rud, S. Rath, et al., Diversity of bacteria exhibiting bile acidinducible 7α-dehydroxylation genes in the human gut, Comput. Struct. Biotec. (2019). Available at: https://doi.org/10.1016/j.csbj.2019.07.012.
[52]

F.Berr, G.A.Kullak-Ublick, G.Paumgartner, et al., 7α-hydroxylating bacteria enhance deoxycholic acid input and cholesterol saturation of bile in patients with gallstones, Gastroenterology 111(6) (1986) 1611-1620.https://doi.org/10.1016/S0016-5085(96)70024-0.

Food Science and Human Wellness
Pages 442-451
Cite this article:
Sun L, Bao L, Phurbu D, et al. Amelioration of metabolic disorders by a mushroom-derived polyphenols correlates with the reduction of Ruminococcaceae in gut of DIO mice. Food Science and Human Wellness, 2021, 10(4): 442-451. https://doi.org/10.1016/j.fshw.2021.04.006

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Received: 14 April 2020
Revised: 20 May 2020
Accepted: 12 July 2020
Published: 04 June 2021
© 2021 Beijing Academy of Food Sciences. Production and hosting by Elsevier B.V. on behalf of KeAi Communications Co., Ltd.

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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