Home Food Science and Human Wellness Article
PDF (4.5 MB)
Cite
EndNote(RIS) BibTeX
Collect
Submit Manuscript
Show Outline
Figures (8)

Tables (2)
Table 1
Table 2
Research Article | Open Access

Influence of soaking Malus domeri (Bois) Chev. leaves on gut microbiota and metabolites of long-living elderly individuals in Hezhou city, Guangxi, China

Hui Niea,b, Zhongyang Gaoa,b, Yanghe Luoc, Yajuan Wanga,b, Feiyang Wua,b, Guangqing Mua,b(), Xiaomeng Wua,b()
School of Food Science and Technology, Dalian Polytechnic University, Dalian 116034, China
Dalian Probiotic Function Research Key Laboratory, Dalian Polytechnic University, Dalian 116034, China
Guangxi Key Laboratory of Health Care Food Science and Technology, Hezhou University, Hezhou 542899, China

Peer review under responsibility of Tsinghua University Press.

Show Author Information

Highlights

• The gut microbiota of Hezhou long-lived people were analyzed for the first time.

• Drinking the soaking of Malus domeri (Bois) Chev. leaves regulated the gut microbial composition.

• A total of 106 metabolites were detected in fecal samples of long-living elderly individuals.

Graphical Abstract

View original image Download original image

Abstract

To investigate the effects of drinking the soaking of Malus domeri (Bois) Chev. leaves on gut microbiota and metabolites of long-living elderly individuals in Hezhou city, Guangxi, China. It has been reported that longevity is closely related to metabolism and the gut microbiota. The 16S rRNA sequencing and liquid chromatography-mass spectrometry (LC-MS) were used to analysis fecal samples and explore the factors affecting longevity in the region. Interestingly, we discovered, that elderly individuals who had been drinking the soaking of M. domeri (Bois) Chev. leaves for a long time exhibited higher diversity of the gut microbiota than without drinking the soaking, notably. The proportions of Ruminococcaceae and Prevotella were decreased in those who did not drink this soaking. In addition, a total of 106 metabolites were characterized, and the people of long-lived people (> 90 years old) and elderly people (< 90 years old) who drinking soaking of M. domeri (Bois) Chev. leaves signif icantly altered the gut microbiota and upregulate d levels of haplopine, farnesol, genipic acid, momordicinin, 2-hydroxyestrone, hydroxyphenyllactic acid, caffeic acid, sophoraflavanone B, and soyasaponin I. We preliminarily determined that M. domeri (Bois) Chev. leaves consumption may be an important factor affecting longevity in this area.

Keywords

LongevityMalus domeri (Bois) Chev. leavesGut microbiotaMetabolomics

Electronic Supplementary Material

Download File(s)
fshw-13-3-1311_ESM1.docx (1.2 MB)
fshw-13-3-1311_ESM2.xlsx (44.7 KB)
fshw-13-3-1311_ESM3.docx (11.6 KB)

References

[1]

N. Tuikhar, S. Keisam, R.K. Labala, et al., Comparative analysis of the gut microbiota in centenarians and young adults shows a common signature across genotypically non-related populations, Mech. Ageing Dev. 179 (2019) 23-35. https://doi.org/10.1016/j.mad.2019.02.001.

Crossref Google Scholar
[2]

M.A. Jackson, I.B. Jeffery, M. Beaumont, et al., Signatures of early frailty in the gut microbiota, Genome. Med. 8 (2016) 8. https://doi.org/10.1186/s13073-016-0262-7.

Crossref Google Scholar
[3]

D. Cai, S.C. Zhao, D.L, Li, et al., Nutrient intake is associated with longevity characterization by metabolites and element profiles of healthy centenarians, Nutrients 8 (2016) 2-19. https://doi.org/10.3390/nu8090564.

Crossref Google Scholar
[4]

F. Wang, G.H. Huang, D. Cai, et al., Qualitative and semiquantitative analysis of fecal Bifidobacterium species in centenarians living in Bama, Guangxi, China, Curr. Microbiol. 71 (2015) 143-149. https://doi.org/10.1007/s00284-015-0804-z.

Crossref Google Scholar
[5]

L. Zhao, W. Xu, S.A. Ibrahim, et al., Effects of age and region on fecal microflora in elderly subjects living in Bama, Guangxi, China, Curr. Microbiol. 62 (2011) 64-70. https://doi.org/10.1007/s00284-010-9676-4.

Crossref Google Scholar
[6]

J. Lv, W. Wang, T. Krafft, et al., Effects of several environmental factors on longevity and health of the human population of Zhongxiang, Hubei, China, Biol. Trace Elem. Res. 143 (2011) 702-716. https://doi.org/10.1007/s12011-010-8914-8.

Crossref Google Scholar
[7]

X.M. Yu, S.J. Li, D. Yang, et al., A novel strain of Lactobacillus mucosae isolated from a Gaotian villager improves in vitro and in vivo antioxidant as well as biological properties in D-galactose-induced aging mice, J. Dairy Sci.99 (2015) 1-12. https://doi.org/10.3168/jds.2015-10265.

Crossref Google Scholar
[8]
Accelerate the green rise of Hezhou to create an “Ecological Hezhou and Longevity Resort”, Guangxi Economy (2017) 53-55.
[9]

Q. Zhang, C.X. Chen, Z.L. Chen, et al., Research of compositions and antioxidant activity during natural fermentation of Malus domeri (Bois) Chev. enzyme drink, Food Res. Dev. 22 (2018) 15-19. https://doi.org/10.3969/j.issn.1005-6521.2018.22.003.

Crossref Google Scholar
[10]

Y.J. Wang, Y.F. He, M.P. Rayman, et al., Prospective selective mechanism of emerging senolytic agents derived from flavonoids, J. Agric. Food Chem.69 (2021) 12418-12423. https://doi.org/10.1021/acs.jafc.1c04379.

Crossref Google Scholar
[11]

A.R. Brooks-Wilson, Genetics of healthy aging and longevity, Hum. Genet.132 (2013) 1323-1338. https://doi.org/10.1007/s00439-013-1342-z.

Crossref Google Scholar
[12]

Y. Liu, Y. Li, Y. Jiang, et al., Effects of soil trace elements on longevity population in China, Biol. Trace Elem. Res. 153 (2013) 119-126. https://doi.org/10. 1007/s12011-013-9673-0.

Crossref Google Scholar
[13]

J.M. Robine, F.R. Herrmann, Y. Arai, et al., Exploring the impact of climate on human longevity, Exp. Gerontol. 47 (2012) 660-671. https://doi.org/10.1038/mp.2016.50.

Crossref Google Scholar
[14]

G.B. Rogers, D.J. Keating, R.L. Young, et al., From gut dysbiosis to altered brain function and mental illness: mechanisms and pathways, Mol. Psychiatr.21 (2016) 738-748. https://doi.org/10.1038/mp.2016.50.

Crossref Google Scholar
[15]

C. Grajeda-Iglesias, S. Durand, R. Daillère, et al., Akkermansia muciniphila oral administration of elevates systemic antiaging and anticancer metabolites, Aging (2021) 202739. https://doi.org/10.18632/aging.202739.

Crossref Google Scholar
[16]

F. Kong, Y. Hua, B. Zeng, et al., Gut microbiota signatures of longevity, Curr. Biol. 26 (2016) 832-833. https://doi.org/10.1016/j.cub.2016.08.015.

Crossref Google Scholar
[17]

E. Biagi, C. Franceschi, S. Rampelli, et al., Gut microbiota and extreme longevity. Curr. Biol. 26 (2016) 1480-1485. https://doi.org/10.1016/j.cub.2016.04.016.

Crossref Google Scholar
[18]

T. Odamaki, K. Kato, H. Sugahara, et al., Age-related changes in gut microbiota composition from newborn to centenarian: a cross-sectional study, BMC Microbiol. 16 (2016) 90. https://doi.org/10.1186/s12866-016-0708-5.

Crossref Google Scholar
[19]

L.P. Drago, T. Marco, R. Valentina, et al., Cultivable and pyrosequenced fecal microflora in centenarians and young subjects, J. Clin. Gastroenterol.46 (2012) 81-84. https://doi.org/10.1097/mcg.0b013e3182693982.

Crossref Google Scholar
[20]

Y.J. Lai, R. Dhingra, Z.F. Zhang et al., Toward elucidating the human gut microbiota-brain axis: Molecules, biochemistry, and implications for health and diseases, Biochemistry 61(24) (2022) 2806-2821. https://doi.org/10.1021/acs.biochem.1c00656.

Crossref Google Scholar
[21]

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.

Crossref Google Scholar
[22]

F. Kuipers, V.W. Bloks, A.K. Groen, Beyond intestinal soap bile acids in metabolic control, Nat. Rev. Endocrinol. 10 (2014) 488-498. https://doi.org/10.1038/nrendo.2014.60.

Crossref Google Scholar
[23]

A.V. Golubeva, S.A. Joyce, G. Moloney, et al., Microbiota-related changes in bile acid and tryptophan metabolism are associated with gastrointestinal dysfunction in a mouse model of autism, EBioMedicine 24 (2017) 166-178. https://doi.org/10.1016/j.ebiom.2017.09.020.

Crossref Google Scholar
[24]

S. Pastoriza, M. Mesias, C. Cabrera, et al., Healthy properties of green and white teas: an update, Food Funct. 8 (2017) 2650-2662. https://doi.org/10.1039/c7fo00611j.

Crossref Google Scholar
[25]

V.L. Truong, W.S. Jeong, Antioxidant and anti-inflammatory roles of tea polyphenols in inflammatory bowel diseases, Food Sci. Hum. Well. 11 (2022) 502-511. https://doi.org/10.1016/j.fshw.2021.12.008.

Crossref Google Scholar
[26]

M.R. Wu, X.B, Wu, J.X. Zhu, et al., Selenium-enriched and ordinary green tea extracts prevent high blood pressure and alter gut microbiota composition of hypertensive rats caused by high-salt diet, Food Sci. Hum. Well. 11 (2022) 738-751. http://doi.org/10.1016/j.fshw.2021.12.031.

Crossref Google Scholar
[27]

S.S. Hu, S. Li, Y. Liu, et al., Aged ripe Pu-erh Tea reduced oxidative stressmediated inflammation in dextran sulfate sodium-induced colitis mice by regulating intestinal microbes, J. Agric. Food Chem. 69 (2021) 10592-10605. https://doi.org/10.1021/acs.jafc.1c04032.

Crossref Google Scholar
[28]

X. Huang, J.N. Chen, G. Yao, et al., A TaqMan-probe-based multiplex realtime RT-qPCR for simultaneous detection of porcine enteric coronaviruses, Appl. Microbiol. Biotechnol. 103 (2019) 4943-4952. https://doi.org/10.1007/s00253-019-09835-7.

Crossref Google Scholar
[29]

J.H. Wang, J. Lu, Y.X. Zhang, et al., Microbial ecology might serve as new indicator for the influence of green tide on the coastal water quality:assessment the bioturbation of Ulva prolifera outbreak on bacterial community in coastal waters, Ecol. Indic. 113 (2020) 106211. https://doi.org/10.1016/j.ecolind.2020.106211.

Crossref Google Scholar
[30]

U. Kõljalg, R.H. Nilsson, K. Abarenkov, et al., Towards a unified paradigm for sequence-based identification of fungi, Mol. Ecol. 22 (2013) 5271-5277. https://doi.org/10.1111/mec.12481.

Crossref Google Scholar
[31]

H. Wu, T.Y.C. Lam, T.F. Shum, et al., Hypotensive effect of captopril on deoxycorticosterone acetate-salt-induced hypertensive rat is associated with gut microbiota alteration, Hypertens. Res. 45 (2021) 270-282. https://doi.org/10.1038/s41440-021-00796-x.

Crossref Google Scholar
[32]

H. Nie, H.C. Chen, G.L. Li, et al., Comparison of flavonoids and phenylpropanoids compounds in Chinese water chestnut processed with different methods, Food Chem. 335 (2021) 127662. https://doi.org/10.1016/j.foodchem.2020.127662.

Crossref Google Scholar
[33]

E. Biagi, S. Rampelli, S. Turroni, et al., The gut microbiota of centenarians:signatures of longevity in the gut microbiota profile, Mech. Ageing Dev. 165(2017) 180-184. https://doi.org/10.1016/j.mad.2016.12.013.

Crossref Google Scholar
[34]

C. Yang, Z.X. Qiao, Z.X. Xu, et al., Algal oil rich in docosahexaenoic acid alleviates intestinal inflammation induced by antibiotics associated with the modulation of the gut microbiome and metabolome, J. Agric. Food Chem.69 (2021) 9124-9136. https://doi.org/10.1021/acs.jafc.0c07323.

Crossref Google Scholar
[35]

D. Liang, L. Zhang, H.Z. Chen, et al., Potato resistant starch inhibits dietinduced obesity by modifying the composition of intestinal microbiota and their metabolites in obese mice, Int. J. Biol. Macromol. 180 (2021) 458-469. https://doi.org/10.1016/j.ijbiomac.2021.02.209.

Crossref Google Scholar
[36]

S.Y. Zhang, B. Zeng, Y.F. Chen, et al., Gut microbiota in healthy and unhealthy long-living people, Gene 779 (2021) 145510. https://doi.org/10.1016/j.gene.2021.145510.

Crossref Google Scholar
[37]

J. Ye, Y. Ding, X. Qi, et al., Geographic and position-based variations in phyllospheric bacterial communities present on flue-cured tobacco, Appl. Microbiol. Biotechnol. 18 (2021). https://doi.org/10.1007/s00253-021-11671-7.

Crossref Google Scholar
[38]

H. Singh, M.G. Torralba, K.J. Moncera, et al., Gastro-intestinal and oral microbiome signatures associated with healthy aging, Geroscience 41 (2019) 907-921. https://doi.org/10.1007/s11357-019-00098-8.

Crossref Google Scholar
[39]

J.J. Kiplimo, M.S. Islam, N.A. Koorbanally, A novel flavonoid and furoquinoline alkaloids from Vepris glomerata and their antioxidant activity, Nat. Prod. Commun. 6 (2011) 47-50. https://doi.org/10.1186/s13073-016-0262-7.

Crossref Google Scholar
[40]

T.Y. Kim, Y.J. Kim, J. Jegal, et al., Haplopine ameliorates 2,4-dinitrochlorobenzene-induced atopic dermatitis-like skin lesions in mice and TNF-α/IFN-γ-induced inflammation in human keratinocyte, Antioxidants 10 (2021) 806. https://doi.org/10.3390/antiox10050806.

Crossref Google Scholar
[41]

L.B. Sell, C.C. Ramelow, H.M. Kohl, et al., Farnesol induces protection against murine CNS inflammatory demyelination and modifies gut microbiome, Clin. Immunol. (2021) 108766. https://doi.org/10.1016/j.clim.2021.108766.

Crossref Google Scholar
[42]

P. Kulkarni, S. Lohidasan, K. Mahadik, Bioanalytical method development for momordicinin and its application to long term pharmacokinetics in diabetic rats, Drug Dev. Ind. Pharm. (2021) 1-8. https://doi.org/10.1080/03639045.2021.1908337.

Crossref Google Scholar
[43]

L. Dickson, M. Tenon, L. Svilar, et al., Main human urinary metabolites after genipap (Genipa americana L.) juice intake, Nutrients 10 (2018) 1155. https://doi.org/10.3390/nu10091155.

Crossref Google Scholar
[44]

X.Q. Zhao, S. Guo, Y.Y. Lu, et al., Lycium barbarum L. leaves ameliorate type 2 diabetes in rats by modulating metabolic profiles and gut microbiota composition, Biomed. Pharmacother. 121 (2020) 109559. https://doi.org/10.1016/j.biopha.2019.109559.

Crossref Google Scholar
[45]

N.T. Telang, G. Li, M. Katdare, et al., Epimedium grandiflorum the nutritional herb inhibits the growth in a model for the luminal a molecular subtype of breast cancer, Oncol. Lett. 13 (2017) 2477-2482. https://doi.org/10.3892/ol.2017.5720.

Crossref Google Scholar
[46]

G. Peron, S. Sut, B.S. Dal, et al., Untargeted UPLC-MS metabolomics reveals multiple changes of urine composition in healthy adult volunteers after consumption of Curcuma longa L. extract, Food Res. Int. (2019) 108730. https://doi.org/10.1016/j.foodres.2019.108730.

Crossref Google Scholar
[47]

S.H. Mun, O.H. Kang, D.K. Joung, et al., Combination therapy of sophoraflavanone B against MRSA: in vitro synergy testing, Evid-Based. Compl. Alt. (2013) 823794. https://doi.org/10.1155/2013/823794.

Crossref Google Scholar
[48]

M. Neacsu, V. Raikos, Y. Benavides-Paz, et al., Sapogenol is a major microbial metabolite in human plasma associated with high protein soybased diets: the relevance for functional food formulations, Foods 9 (2020) 422. https://doi.org/10.3390/foods9040422.

Crossref Google Scholar
Food Science and Human Wellness
Volume 13 Issue 3,
May 2024
Pages 1311-1321
DOI: 10.26599/FSHW.2022.9250110
Cite this article:
Nie H, Gao Z, Luo Y, et al. Influence of soaking Malus domeri (Bois) Chev. leaves on gut microbiota and metabolites of long-living elderly individuals in Hezhou city, Guangxi, China. Food Science and Human Wellness, 2024, 13(3): 1311-1321. https://doi.org/10.26599/FSHW.2022.9250110
Metrics & Citations  
Article History
Copyright
Rights and Permissions
Return

The details of subjects in each categorized groups analyzed in this study.

GroupaAverage age (years)bMale/FemaleBMIbNumber of samples
a HZ1, drinking the soaking M. domeri (Bois) Chev. Leaves; YS, younger elderly people drinking the soaking M. domeri (Bois) Chev. leaves (age < 90 years old); AS, long-lived people drinking the soaking M. domeri (Bois) Chev. leaves (age > 90 years old)); HZ2, not drinking soaking solution of M. domeri (Bois) Chev. Leaves; YN, younger elderly people not drinking the soaking M. domeri (Bois) Chev. Leaves; AN, long-lived people not drinking the soaking M. domeri (Bois) Chev. leaves. b Values are means ± standard deviation (SD).
HZ1YS85.50 ± 0.840/622.09 ± 3.206
AS92.63 ± 3.581/721.55 ± 1.838
HZ2YN84.17 ± 2.222/423.75 ± 2.556
AN93.75 ± 5.155/320.20 ± 3.218

KEGG pathway enrichment of the changed metabolites for HZ1 versus HZ2.

KEGG pathwayChanged metaboliteVIPaP valueup/down
a VIP, variable importance in the projection.
Ascorbate and aldarate metabolismD-Glucarate1.68680.03445down
Terpenoid backbone biosynthesisFarnesol2.09380.00958up
N-Glycan biosynthesisFarnesol2.09380.00958up
Anthocyanin biosynthesisPelargonidin2.27810.00259up
Diterpenoid biosynthesisOryzalexin E1.89910.01385up
Zeatin biosynthesisLupinate1.59870.04212up
Linoleic acid metabolism9,10,13-TriHOME2.37730.00282up
Flavonoid biosynthesisPelargonidin2.27810.00260up
Biosynthesis of terpenoids and steroidsFarnesol2.09380.00958up
Tyrosine metabolism2-(4-Hydroxyphenyl) ethanol1.66900.03273up
Alpha-Linolenic acid metabolism9-oxo-Nonanoic acid2.02040.00975up
Phenylpropanoid biosynthesisCaffeic acid1.93260.01213up
Steroid hormone biosynthesis2-Hydroxyestrone1.54450.04915up
Biosynthesis of phenylpropanoidsCaffeic acid1.93260.01213up
Drug metabolism - other enzymesIsonicotinic acid1.79350.01864up