CLC number:
On-line Access: 2025-05-28
Received: 2024-07-08
Revision Accepted: 2024-09-13
Crosschecked: 2025-05-29
Cited: 0
Clicked: 730
Citations: Bibtex RefMan EndNote GB/T7714
Jinyou LI, Yue WU, Yichen YANG, Lufang CHEN, Caihong HE, Shixian ZHOU, Shunmei HUANG, Xia ZHANG, Yuming WANG, Qifeng GUI, Haifeng LU, Qin ZHANG, Yunmei YANG. Metagenomics reveals an increased proportion of an Escherichia coli-dominated enterotype in elderly Chinese people[J]. Journal of Zhejiang University Science B, 2025, 26(5): 477-492.
@article{title="Metagenomics reveals an increased proportion of an Escherichia coli-dominated enterotype in elderly Chinese people",
author="Jinyou LI, Yue WU, Yichen YANG, Lufang CHEN, Caihong HE, Shixian ZHOU, Shunmei HUANG, Xia ZHANG, Yuming WANG, Qifeng GUI, Haifeng LU, Qin ZHANG, Yunmei YANG",
journal="Journal of Zhejiang University Science B",
volume="26",
number="5",
pages="477-492",
year="2025",
publisher="Zhejiang University Press & Springer",
doi="10.1631/jzus.B2400341"
}
%0 Journal Article
%T Metagenomics reveals an increased proportion of an Escherichia coli-dominated enterotype in elderly Chinese people
%A Jinyou LI
%A Yue WU
%A Yichen YANG
%A Lufang CHEN
%A Caihong HE
%A Shixian ZHOU
%A Shunmei HUANG
%A Xia ZHANG
%A Yuming WANG
%A Qifeng GUI
%A Haifeng LU
%A Qin ZHANG
%A Yunmei YANG
%J Journal of Zhejiang University SCIENCE B
%V 26
%N 5
%P 477-492
%@ 1673-1581
%D 2025
%I Zhejiang University Press & Springer
%DOI 10.1631/jzus.B2400341
TY - JOUR
T1 - Metagenomics reveals an increased proportion of an Escherichia coli-dominated enterotype in elderly Chinese people
A1 - Jinyou LI
A1 - Yue WU
A1 - Yichen YANG
A1 - Lufang CHEN
A1 - Caihong HE
A1 - Shixian ZHOU
A1 - Shunmei HUANG
A1 - Xia ZHANG
A1 - Yuming WANG
A1 - Qifeng GUI
A1 - Haifeng LU
A1 - Qin ZHANG
A1 - Yunmei YANG
J0 - Journal of Zhejiang University Science B
VL - 26
IS - 5
SP - 477
EP - 492
%@ 1673-1581
Y1 - 2025
PB - Zhejiang University Press & Springer
ER -
DOI - 10.1631/jzus.B2400341
Abstract: Gut microbial communities are likely remodeled in tandem with accumulated physiological decline during aging, yet there is limited understanding of gut microbiome variation in advanced age. Here, we performed a metagenomics-based enterotype analysis in a geographically homogeneous cohort of 367 enrolled Chinese individuals between the ages of 60 and 94 years, with the goal of characterizing the gut microbiome of elderly individuals and identifying factors linked to enterotype variations. In addition to two adult-like enterotypes dominated by Bacteroides (ET-Bacteroides) and Prevotella (ET-Prevotella), we identified a novel enterotype dominated by Escherichia (ET-Escherichia), whose prevalence increased in advanced age. Our data demonstrated that age explained more of the variance in the gut microbiome than previously identified factors such as type 2 diabetes mellitus (T2DM) or diet. We characterized the distinct taxonomic and functional profiles of ET-Escherichia, and found the strongest cohesion and highest robustness of the microbial co-occurrence network in this enterotype, as well as the lowest species diversity. In addition, we carried out a series of correlation analyses and co-abundance network analyses, which showed that several factors were likely linked to the overabundance of Escherichia members, including advanced age, vegetable intake, and fruit intake. Overall, our data revealed an enterotype variation characterized by Escherichia enrichment in the elderly population. Considering the different age distribution of each enterotype, these findings provide new insights into the changes that occur in the gut microbiome with age and highlight the importance of microbiome-based stratification of elderly individuals.
[1]AbiaALK, Ubomba-JaswaE, 2019. Dirty money on holy ground: isolation of potentially pathogenic bacteria and fungi on money collected from church offerings. Iran J Public Health, 48(5):849-857.
[2]ArumugamM, RaesJ, PelletierE, et al., 2011. Enterotypes of the human gut microbiome. Nature, 473(7346):174-180.
[3]BaumgartnerM, BayerF, Pfrunder-CardozoKR, et al., 2020. Resident microbial communities inhibit growth and antibiotic-resistance evolution of Escherichia coli in human gut microbiome samples. PLoS Biol, 18(4):e3000465.
[4]ChenLM, CollijV, JaegerM, et al., 2020. Gut microbial co-abundance networks show specificity in inflammatory bowel disease and obesity. Nat Commun, 11:4018.
[5]DaviesM, GalazzoG, van HattemJM, et al., 2022. Enterobacteriaceae and Bacteroidaceae provide resistance to travel-associated intestinal colonization by multi-drug resistant Escherichia coli. Gut Microbes, 14(1):2060676.
[6]DiardM, GarciaV, MaierL, et al., 2013. Stabilization of cooperative virulence by the expression of an avirulent phenotype. Nature, 494(7437):353-356.
[7]FengQ, LiangSS, JiaHJ, et al., 2015. Gut microbiome development along the colorectal adenoma–carcinoma sequence. Nat Commun, 6:6528.
[8]FranzosaEA, McIverLJ, RahnavardG, et al., 2018. Species-level functional profiling of metagenomes and metatranscriptomes. Nat Methods, 15(11):962-968.
[9]GacesaR, KurilshikovA, Vich VilaA, et al., 2022. Environmental factors shaping the gut microbiome in a Dutch population. Nature, 604(7907):732-739.
[10]GhoshTS, ShanahanF, O'ToolePW, 2022. The gut microbiome as a modulator of healthy ageing. Nat Rev Gastroenterol Hepatol, 19(9):565-584.
[11]GhoulM, MitriS, 2016. The ecology and evolution of microbial competition. Trends Microbiol, 24(10):833-845.
[12]HanN, PengXH, ZhangTT, et al., 2024. Rapid turnover and short-term blooms of Escherichia coli in the human gut. J Bacteriol, 206(1):e0023923.
[13]HerrenCM, McMahonKD, 2017. Cohesion: a method for quantifying the connectivity of microbial communities. ISME J, 11(11):2426-2438.
[14]JacksonMA, JefferyIB, BeaumontM, et al., 2016. Signatures of early frailty in the gut microbiota. Genome Med, 8:8.
[15]JiaoS, YangYF, XuYQ, et al., 2020. Balance between community assembly processes mediates species coexistence in agricultural soil microbiomes across Eastern China. ISME J, 14(1):202-216.
[16]KongFL, DengFL, LiY, et al., 2019. Identification of gut microbiome signatures associated with longevity provides a promising modulation target for healthy aging. Gut Microbes, 10(2):210-215.
[17]KuntalBK, ChandrakarP, SadhuS, et al., 2019. ‘NetShift’: a methodology for understanding ‘driver microbes’ from healthy and disease microbiome datasets. ISME J, 13(2):442-454.
[18]LarsonPJ, ZhouW, SantiagoA, et al., 2022. Associations of the skin, oral and gut microbiome with aging, frailty and infection risk reservoirs in older adults. Nat Aging, 2(10):941-955.
[19]LeiteG, PimentelM, BarlowGM, et al., 2022. The small bowel microbiome changes significantly with age and aspects of the ageing process. Microb Cell, 9(1):21-23.
[20]LiL, JingS, TangY, et al., 2024. The effects of food provisioning on the gut microbiota community and antibiotic resistance genes of yunnan snub-nosed monkey. Front Microbiol, 15:1361218.
[21]LingZX, LiuX, ChengYW, et al., 2022. Gut microbiota and aging. Crit Rev Food Sci Nutr, 62(13):3509-3534.
[22]LuppC, RobertsonML, WickhamME, et al., 2007. Host-mediated inflammation disrupts the intestinal microbiota and promotes the overgrowth of enterobacteriaceae. Cell Host Microbe, 2(3):204.
[23]MartinsonJNV, WalkST, 2020. Escherichia coli residency in the gut of healthy human adults. EcoSal Plus, 9(1):10.1128/ecosalplus.ESP-0003-2020.
[24]MartinsonJNV, PinkhamNV, PetersGW, et al., 2019. Rethinking gut microbiome residency and the Enterobacteriaceae in healthy human adults. ISME J, 13(9):2306-2318.
[25]Moreira de Gouveia MI, Bernalier-DonadilleA, JubelinG, 2024. Enterobacteriaceae in the human gut: dynamics and ecological roles in health and disease. Biology, 13(3):142.
[26]MossadO, BatutB, YilmazB, et al., 2022. Gut microbiota drives age-related oxidative stress and mitochondrial damage in microglia via the metabolite N 6-carboxymethyllysine. Nat Neurosci, 25(3):295-305.
[27]MottaweaW, ChiangCK, MühlbauerM, et al., 2016. Altered intestinal microbiota–host mitochondria crosstalk in new onset Crohn’s disease. Nat Commun, 7:13419.
[28]O'ToolePW, JefferyIB, 2015. Gut microbiota and aging. Science, 350(6265):1214-1215.
[29]PalS, JuyalD, AdekhandiS, et al., 2015. Mobile phones: reservoirs for the transmission of nosocomial pathogens. Adv Biomed Res, 4(1):144.
[30]PangSF, ChenXD, LuZL, et al., 2023. Longevity of centenarians is reflected by the gut microbiome with youth-associated signatures. Nat Aging, 3(4):436-449.
[31]QiHB, WeiJM, GaoYH, et al., 2020. Reg4 and complement factor D prevent the overgrowth of E. coli in the mouse gut. Commun Biol, 3:483.
[32]QinJJ, LiYR, CaiZM, et al., 2012. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature, 490(7418):55-60.
[33]Roth-SchulzeAJ, PennoMAS, NguiKM, et al., 2021. Type 1 diabetes in pregnancy is associated with distinct changes in the composition and function of the gut microbiome. Microbiome, 9:167.
[34]SalahshouriP, Emadi-BaygiM, JaliliM, et al., 2021. A metabolic model of intestinal secretions: the link between human microbiota and colorectal cancer progression. Metabolites, 11(7):456
[35]TanXJ, WangYZ, GongT, 2023. The interplay between oral microbiota, gut microbiota and systematic diseases. J Oral Microbiol, 15(1):2213112.
[36]ThomasAM, ManghiP, AsnicarF, et al., 2019. Metagenomic analysis of colorectal cancer datasets identifies cross-cohort microbial diagnostic signatures and a link with choline degradation. Nat Med, 25(4):667-678.
[37]VogtmannE, HuaX, ZellerG, et al., 2016. Colorectal cancer and the human gut microbiome: reproducibility with whole-genome shotgun sequencing. PLoS ONE, 11(5):e0155362.
[38]WibowoMC, YangZ, BorryM, et al., 2021. Reconstruction of ancient microbial genomes from the human gut. Nature, 594(7862):234-239.
[39]WirbelJ, PylPT, KartalE, et al., 2019. Meta-analysis of fecal metagenomes reveals global microbial signatures that are specific for colorectal cancer. Nat Med, 25(4):679-689.
[40]XiaoLW, WangJF, ZhengJY, et al., 2021. Deterministic transition of enterotypes shapes the infant gut microbiome at an early age. Genome Biol, 22:243.
[41]YachidaS, MizutaniS, ShiromaH, et al., 2019. Metagenomic and metabolomic analyses reveal distinct stage-specific phenotypes of the gut microbiota in colorectal cancer. Nat Med, 25(6):968-976.
[42]YuLL, PanJN, GuoM, et al., 2023. Gut microbiota and anti-aging: focusing on spermidine. Crit Rev Food Sci Nutr, 64(28):10419-10437.
[43]ZellerG, TapJ, VoigtAY, et al., 2014. Potential of fecal microbiota for early-stage detection of colorectal cancer. Mol Syst Biol, 10(11):766.
Open peer comments: Debate/Discuss/Question/Opinion
<1>