AI Chat Paper
Note: Please note that the following content is generated by AMiner AI. SciOpen does not take any responsibility related to this content.
{{lang === 'zh_CN' ? '文章概述' : 'Summary'}}
{{lang === 'en_US' ? '中' : 'Eng'}}
Chat more with AI
PDF (9.3 MB)
Collect
Submit Manuscript AI Chat Paper
Show Outline
Outline
Show full outline
Hide outline
Outline
Show full outline
Hide outline
Open Access

Structural elucidation of mulberry leaf oligosaccharide and its selective promotion of gut microbiota to alleviate type 2 diabetes mellitus

Tenggen Hua,b,cYuanshan Yua,bJijun WuaYujuan XuaGengsheng XiaodKejing AnaErna LiaSentai LiaoaYuxiao Zoua,( )
Sericultural & Agri-Food Research Institute, Guangdong Academy of Agricultural Sciences/Key Laboratory of Functional Foods, Ministry of Agriculture and Rural Affairs/Guangdong Key Laboratory of Agricultural Products Processing, Guangzhou 510610, China
Huagongliya (Foshan) Technology Industry Co., Ltd., Foshan 528313, China
Heyuan Branch, Guangdong Laboratory for Lingnan Modern Agriculture, Heyuan 517001, China
Zhongkai University of Agriculture and Engineering, Guangzhou 510225, China

Peer review under responsibility of Tsinghua University Press.

Show Author Information

Highlights

• A non-digestible oligosaccharide (MLO 2-1) was obtained.

• The proposed sugar chain structure of MLO 2-1 was determined.

• MLO 2-1 could tolerate simulated saliva, gastric and intestinal digestion.

• MLO 2-1 displayed the regulatory activity on the gut microbiota, especially Lactobacillus murinus.

• MLO 2-1 showed hypoglycemic activity by selectively accelerating the proliferation of L. murinus.

Graphical Abstract

Abstract

Two oligosaccharide fractions (MLO 2-1 and 2-2) were purified from enzymatic hydrolysate of mulberry leaf polysaccharide. The results of simulated digestion showed that MLO 2-2 was a digestible oligosaccharide, which could be degraded by human digestive juice; while MLO 2-1 possessed the non-digestible property in the upper gastrointestinal tract and performed the function by regulating the gut microbiota. Hence, MLO 2-1 was selected for the further analysis. The structure of MLO 2-1 was elucidated as follow: α-T-Glcp-(1→3)-β-Glcp-(1→5)-α-Araf-(1→5)-α-Araf-1→5)-α-Araf-(1→3)-α-(2-OAc)-Glcp-1. The in vitro fecal fermentation results showed that MLO 2-1 could modulate the composition of gut microbiota. Meanwhile, MLO 2-1 was effectively metabolized by fecal bacteria to produce lactate and short chain fatty acids, especially acetate and butyrate. The specific metabolic pathways of MLO 2-1 by gut microbiota were further illuminated. Gut microbiota analysis revealed that MLO 2-1 selectively promoted the growth of Ligilactobacillus murinus, a commensal bacterium presented a reduced level in T2DM mice. Animal experiments indicated that MLO 2-1 and L. murinus exhibited hypoglycemic activities. These results demonstrated that MLO 2-1 might alleviate T2DM by selectively accelerating the proliferation of L. murinus.

Electronic Supplementary Material

Download File(s)
fshw-13-4-2161_ESM.docx (714.7 KB)

References

[1]

Ö. Aydin, M. Nieuwdorp, V. Gerdes, The gut microbiome as a target for the treatment of type 2 diabetes, Curr. Diab. Rep. 18 (2018) 55. https://doi.org/10.1007/s11892-018-1020-6.

[2]

L.P. Zhao, F. Zhang, X.Y. Ding, et al. Gut bacteria selectively promoted by dietary fibers alleviate type 2 diabetes, Science 359 (2018) 1151-1156. https://doi.org/10.1126/science.aao5774.

[3]

J. Aron-Wisnewsky, C. Vigliotti, J. Witjes, et al., Gut microbiota and human NAFLD: disentangling microbial signatures from metabolic disorders, Nat. Rev. Gastro. Hepat. 17 (2020) 279-297. https://doi.org/10.1038/s41575-020-0269-9.

[4]

B.L. Zhu, X. Wang, L.J. Li, Human gut microbiome: the second genome of human body, Protein Cell. 1 (2010) 718-725. https://doi.org/10.1007/s13238-010-0093-z.

[5]

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.

[6]

C. Manichanh, L. Rigottier-Gois, E. Bonnaud, et al., Reduced diversity of faecal microbiota in Crohn's disease revealed by a metagenomic approach, Gut 55 (2006) 205. https://doi.org/10.1136/gut.2005.073817.

[7]

E. Le Chatelier, T. Nielsen, J. Qin, et al. Richness of human gut microbiome correlates with metabolic markers, Nature 500 (2013) 541-546. https://doi.org/10.1038/nature12506.

[8]

A. Cotillard, S. P. Kennedy, L. C. Kong, et al., Dietary intervention impact on gut microbial gene richness, Nature 500 (2013) 585-588. https://doi.org/10.1038/nature12480.

[9]

J. Qin, Y. Li, Z. Cai, et al., A metagenome-wide association study of gut microbiota in type 2 diabetes, Nature 490 (2012) 55-60. https://doi.org/10.1038/nature11450.

[10]

X.Y. Zhang, D.Q. Shen, Z.W. Fang, et al., Human gut microbiota changes reveal the progression of glucose intolerance, PLoS ONE 8 (2013) 71108. https://doi.org/10.1371/journal.pone.0071108.

[11]

H. Plovier, A. Everard, C. Druart, et al., A purified membrane protein from Akkermansia muciniphila or the pasteurized bacterium improves metabolism in obese and diabetic mice, Nat. Med. 23 (2017) 107-113. https://doi.org/10.1038/nm.4236.

[12]

H.F. Liu, X.Y. Zeng, J.Y. Huang, et al., Dietary fiber extracted from pomelo fruitlets promotes intestinal functions, both in vitro and in vivo, Carbohydr. Polym. 252 (2021) 117186. https://doi.org/10.1016/j.carbpol.2020.117186.

[13]

T.M. Yuan, Z.J. Yin, Z.X. Yan, et al., Tetrahydrocurcumin ameliorates diabetes profiles of db/db mice by altering the composition of gut microbiota and up-regulating the expression of GLP-1 in the pancreas, Fitoterapia 146 (2020) 104665. https://doi.org/10.1016/j.fitote.2020.104665.

[14]

M. Conlon, A. Bird, The impact of diet and lifestyle on gut microbiota and human health, Nutrients 7 (2014) 17-44. https://doi.org/10.3390/nu7010017.

[15]

Q.X. Nie, H.H. Chen, J.L. Hu, et al., Effects of nondigestible oligosaccharides on obesity, Annu. Rev. Food Sci. T. 11 (2020) 205-233. https://doi.org/10.1146/annurev-food-032519-051743.

[16]

P. Wen, T.G. Hu, R. J. Linhardt, et al., Mulberry: a review of bioactive compounds and advanced processing technology, Trends Food Sci. Tech. 83 (2019) 138-158. https://doi.org/10.1016/j.tifs.2018.11.017.

[17]

M.J. Yebra, V. Monedero, M. Zuniga, et al., Molecular analysis of the glucose-specific phosphoenolpyruvate: sugar phosphotransferase system from Lactobacillus casei and its links with the control of sugar metabolism, Microbiology 152 (2006) 95-104. https://doi.org/10.1099/mic.0.28293-0.

[18]

T.G. Hu, H. Wu, Y.S. Yu, et al. Preparation, structural characterization and prebiotic potential of mulberry leaf oligosaccharides, Food Funct. 13 (2022) 5287-5298. https://doi.org/10.1039/d1fo04048k.

[19]

Q.X. Yuan, Y.F. Xie, W. Wang, et al., Extraction optimization, characterization and antioxidant activity in vitro of polysaccharides from mulberry (Morus alba L. ) leaves, Carbohydr. Polym. 128 (2015) 52-62. https://doi.org/10.1016/j.carbpol.2015.04.028.

[20]

M. Sun, C. Sun, H.G. Xie, et al., A simple method to calculate the degree of polymerization of alginate oligosaccharides and low molecular weight alginates, Carbohydr. Res. 486 (2019) 107856. https://doi.org/10.1016/j.carres.2019.107856.

[21]

J.L. Hu, S.P. Nie, F.F. Min, et al., Artificial simulated saliva, gastric and intestinal digestion of polysaccharide from the seeds of Plantago asiatica L, Carbohydr. Polym. 92 (2013) 1143-1450. https://doi.org/10.1016/j.carbpol.2012.10.072.

[22]

C. Tedeschi, V. Clement, M. Rouvet, et al., Dissolution tests as a tool for predicting bioaccessibility of nutrients during digestion, Food Hydrocoll. 23 (2009) 1228-1235. https://doi.org/10.1016/j.foodhyd.2008.09.012.

[23]

T.G. Hu, P. Wen, W.Z. Shen, et al., Effect of 1-deoxynojirimycin isolated from mulberry leaves on glucose metabolism and gut microbiota in a streptozotocin-induced diabetic mouse model, J. Nat. Prod. 82 (2019) 2189-2200. https://doi.org/10.1021/acs.jnatprod.9b00205.

[24]

T.G. Hu, P. Wen, H.Z. Fu, et al., Protective effect of mulberry (Morus atropurpurea) fruit against diphenoxylate-induced constipation in mice through the modulation of gut microbiota, Food Funct. 10 (2019) 1513-1528. https://doi.org/10.1039/c9fo00132h.

[25]

Y.J. Bai, F. Huang, R.F. Zhang, et al. Longan pulp polysaccharides relieve intestinal injury in vivo and in vitro by promoting tight junction expression, Carbohydr. Polym. 229 (2020) 115475. https://doi.org/10.1016/j.carbpol.2019.115475.

[26]

J.W. Li, L.Z. Ai, Q. Yang, et al., Isolation and structural characterization of a polysaccharide from fruits of Zizyphus jujuba cv. Junzao, Int. J. Biol. Macromol. 55 (2013) 83-87. https://doi.org/10.1016/j.ijbiomac.2012.12.017.

[27]

Y.L. Fan, W.H. Wang, W. Song, et al., Partial characterization and anti-tumor activity of an acidic polysaccharide from Gracilaria lemaneiformis, Carbohydr. Polym. 88 (2012) 1313-1318. https://doi.org/10.1016/j.carbpol.2012.02.014.

[28]

L.L. Cai, S.S. Zou, D.P. Liang, et al., Structural characterization, antioxidant and hepatoprotective activities of polysaccharides from Sophorae tonkinensis Radix, Carbohydr. Polym. 184 (2018) 354-365. https://doi.org/10.1016/j.carbpol.2017.12.083.

[29]

M.K. Patel, B. Tanna, A. Mishra, et al., Physicochemical characterization, antioxidant and anti-proliferative activities of a polysaccharide extracted from psyllium (P. ovata) leaves, Int. J. Biol. Macromol. 118 (2018) 976-987. https://doi.org/10.1016/j.ijbiomac.2018.06.139.

[30]

N. Yang, N.N. Zhang, Y.M. Jin, et al., Development of a fluidic system for efficient extraction of mulberry leaves polysaccharide using induced electric fields, Sep. Purif. Technol. 172 (2017) 318-325. https://doi.org/10.1016/j.seppur.2016.08.025.

[31]

A. Klaus, M. Kozarski, J. Vunduk, et al., Biological potential of extracts of the wild edible Basidiomycete mushroom Grifola frondosa, Food Res. Int. 67 (2015) 272-283. https://doi.org/10.1016/j.foodres.2014.11.035.

[32]

B. Gullon, G. Eibes, I. Davila, et al., Hydrothermal treatment of chestnut shells (Castanea sativa) to produce oligosaccharides and antioxidant compounds, Carbohydr. Polym. 192 (2018) 75-83. https://doi.org/10.1016/j.carbpol.2018.03.051.

[33]

S.M. Van Ruth, J. P Roozen, Influence of mastication and saliva on aroma release in a model mouth system, Food Chem. 71 (2000) 339-345. https://doi.org/10.1016/S0308-8146(00)00186-2.

[34]

L.G. Chen, W. Xu, D. Chen, et al. Digestibility of sulfated polysaccharide from the brown seaweed Ascophyllum nodosum and its effect on the human gut microbiota in vitro, Int. J. Biol. Macromol. 112 (2018) 1055-1061. https://doi.org/10.1016/j.ijbiomac.2018.01.183.

[35]

C. Chen, B. Zhang, X. Fu, et al., The digestibility of mulberry fruit polysaccharides and its impact on lipolysis under simulated saliva, gastric and intestinal conditions, Food Hydrocoll. 58 (2016) 171-178. https://doi.org/10.1016/j.foodhyd.2016.02.033.

[36]

I.F. Olawuyi, W.Y. Lee, Structural characterization, functional properties and antioxidant activities of polysaccharide extract obtained from okra leaves (Abelmoschus esculentus), Food Chem. 354 (2021) 129437. https://doi.org/10.1016/j.foodchem.2021.129437.

[37]

P.E. Jansson, L. Kenne, G. Widmalm, Computer-assisted structural analysis of polysaccharides with an extended version of CASPER using 1H- and 13C-NMR data, Carbohydr. Res. 188 (1989) 169-191. https://doi.org/10.1016/0008-6215(89)84069-8.

[38]

H. Kono, S. Kawano, T. Erata, et al., Regioselective syntheses of new tri-and tetrasaccharides by transglycosylation of trichoderma viride β-glucosidase, J. Carbohydr. Chem. 19 (2000) 127-140. https://doi.org/10.1080/07328300008544070.

[39]

X.J. Li, W.R. Bao, C.H. Leung, et al., Chemical structure and immunomodulating activities of an α-glucan purified from Lobelia chinensis Lour, Molecules 21 (2016) 779. https://doi.org/10.3390/molecules21060779.

[40]

A. Percy, H. Ono, D. Watt, et al., Synthesis of β-D-glucopyranosyl-(1→4)-D-arabinose, β-D-glucopyranosyl-(1→4)-l-fucose and β-D-glucopyranosyl-(1→4)-D-altrose catalysed by cellobiose phosphorylase from Cellvibrio gilvus, Carbohydr. Res. 305 (1997) 543-548. https://doi.org/10.1016/S0008-6215(97)00247-4.

[41]

C. Chen, L.L. Wang, Y.Q. Lu, et al., Comparative transcriptional analysis of Lactobacillus plantarum and its ccpA-knockout mutant under galactooligosaccharides and glucose conditions, Front. Microbiol. 10 (2019) 1584. https://doi.org/10.3389/fmicb.2019.01584.

[42]

K. Okano, S. Yoshida, T. Tanaka, et al., Homo-D-lactic acid fermentation from arabinose by redirection of the phosphoketolase pathway to the pentose phosphate pathway in L-lactate dehydrogenase gene-deficient, Appl. Environ. Microbiol. 75 (2009) 5175-5178. https://doi.org/10.1128/AEM.00573-09.

[43]

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.

[44]

H.S. Sung, Y.L. Jo, Purification and characterization of an antibacterial substance from Aerococcus urinaeequi strain HS36, J. Microbiol. Biotechnol. 30 (2020) 93-100. https://doi.org/10.4014/jmb.1910.10015.

[45]

S.J. Yue, D. Zhao, C.X. Peng, et al., Effects of theabrownin on serum metabolites and gut microbiome in rats with a high-sugar diet, Food Funct. 10 (2019) 7063-7080. https://doi.org/10.1039/c9fo01334b.

[46]

F.W. Pan, L.Y. Zhang, M. Li, et al., Predominant gut Lactobacillus murinus strain mediates anti-inflammaging effects in calorie-restricted mice, Microbiome 6 (2018). https://doi.org/10.1186/s40168-018-0440-5.

[47]

L. Delucchi, M. Fraga, K. Perelmuter, et al., Effect of native Lactobacillus murinus LbP2 administration on total fecal IgA in healthy dogs, Can. J. Vet. Res. 78 (2014) 153-155.

[48]

H.F. Ge, Z.Z. Cai, J.L. Chai, et al., Egg white peptides ameliorate dextran sulfate sodium-induced acute colitis symptoms by inhibiting the production of pro-inflammatory cytokines and modulation of gut microbiota composition, Food Chem. 360 (2021) 129981. https://doi.org/10.1016/j.foodchem.2021.129981.

[49]

C. De Luca, J.M. Olefsky, Inflammation and insulin resistance, FEBS Lett. 582 (2008) 97-105. https://doi.org/10.1016/j.febslet.2007.11.057.

[50]

N. Rodríguez-Medina, H. Barrios-Camacho, J. Duran-Bedolla, et al., Klebsiella variicola: an emerging pathogen in humans, Emerg. Microbe. Infec. 8 (2019) 973-988. https://doi.org/10.1080/22221751.2019.1634981.

[51]

A. Ponte, C. Costa. Abcessos hepáticos múltiplos devido a Morganella morganii, Acta Med. Port. 28 (2015) 539. https://doi.org/10.20344/amp.5584.

[52]

A. Gomez-Nguyen, A.R. Basson, L. Dark-Fleury, et al., Parabacteroides distasonis induces depressive-like behavior in a mouse model of Crohn's disease, Brain Behav. Immun. 98 (2021) 245-250. https://doi.org/10.1016/j.bbi.2021.08.218.

[53]

M.E. Perez-Muñoz, K. Bergstrom, V. Peng, et al., Discordance between changes in the gut microbiota and pathogenicity in a mouse model of spontaneous colitis, Gut Microbes. 5 (2014) 286-485. https://doi.org/10.4161/gmic.28622.

Food Science and Human Wellness
Pages 2161-2173
Cite this article:
Hu T, Yu Y, Wu J, et al. Structural elucidation of mulberry leaf oligosaccharide and its selective promotion of gut microbiota to alleviate type 2 diabetes mellitus. Food Science and Human Wellness, 2024, 13(4): 2161-2173. https://doi.org/10.26599/FSHW.2022.9250180

543

Views

47

Downloads

0

Crossref

0

Web of Science

0

Scopus

0

CSCD

Altmetrics

Received: 30 November 2022
Revised: 22 December 2022
Accepted: 07 February 2023
Published: 20 May 2024
© 2024 Beijing Academy of Food Sciences. Publishing services by Tsinghua University Press.

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

Return