Metagenomics reveals an increased proportion of an <italic style="font-style: italic">Escherichia coli</italic>-dominated enterotype in elderly Chinese people

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

doi:10.1631/jzus.B2400341

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Research Article | Updated：2025-05-28

Metagenomics reveals an increased proportion of an Escherichia coli-dominated enterotype in elderly Chinese people
Metagenomics reveals an increased proportion of an Escherichia coli-dominated enterotype in elderly Chinese people
宏基因组学分析显示大肠杆菌主导的肠型在中国老年人群中比例增加
Journal of Zhejiang University-SCIENCE B (Biomedicine & Biotechnology) Vol. 26, Issue 5, Pages: 477-492(2025)
Affiliations：

1.Zhejiang Key Laboratory for Diagnosis and Treatment of Physic-chemical and Aging-related Injuries, The First Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou 310003, China
2.State Key Laboratory for Diagnosis and Treatment of Infectious Disease, The First Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou 310003, China
Funds：
DOI：10.1631/jzus.B2400341
CLC：
CSTR：
Received：08 July 2024，

Revised：13 September 2024，

Published：28 May 2025
Accepted：

李金优,吴月,杨一晨等.宏基因组学分析显示大肠杆菌主导的肠型在中国老年人群中比例增加[J].浙江大学学报（英文版）（B辑：生物医学和生物技术）,2025,26(05):477-492.

Jinyou LI, Yue WU, Yichen YANG, et al. Metagenomics reveals an increased proportion of an Escherichia coli-dominated enterotype in elderly Chinese people[J]. Journal of zhejiang university-science b (biomedicine & biotechnology), 2025, 26(5): 477-492.
李金优,吴月,杨一晨等.宏基因组学分析显示大肠杆菌主导的肠型在中国老年人群中比例增加[J].浙江大学学报（英文版）（B辑：生物医学和生物技术）,2025,26(05):477-492. DOI： 10.1631/jzus.B2400341.

Jinyou LI, Yue WU, Yichen YANG, et al. Metagenomics reveals an increased proportion of an Escherichia coli-dominated enterotype in elderly Chinese people[J]. Journal of zhejiang university-science b (biomedicine & biotechnology), 2025, 26(5): 477-492. DOI： 10.1631/jzus.B2400341.

摘要

随着宿主衰老过程中生理环境的衰退，肠道微生态可能发生重塑，但目前对中国高龄人群整体的肠道菌群变异情况的了解尚且有限。为了解析高龄人群肠道微生物组特征，并揭示肠型变异的相关影响因素，本研究采用宏基因组学方法，对367名60至94岁中国老年人进行肠型分析。除了拟杆菌（ET-

Bacteroides

）和普雷沃氏菌（ET-

Prevotella

）这

两种主导的成人常见肠型外，本研究新发现一种肠杆菌肠型（ET-

Escherichia

），且其流行率在高龄人群中增加。本研究数据表明，相比2型糖尿病或饮食等已知因素，年龄更能解释肠道菌群的变异。此外，本研究解析了ET-

Escherichia

肠型独特的分类和功能特征，并发现该肠型具有最低的物种多样性，但最强的微生物共现网络凝聚力和最高的鲁棒性。通过进一步相关性分析发现，大肠埃希菌属细菌的过度增殖与高龄、蔬菜及水果摄入量等因素显著相关。本研究聚焦于中国非健康长寿老人的肠型特征分析，重点阐述了以大肠杆菌富集为主要特征的高龄老人肠型。这些发现为揭示肠道菌群随年龄的变化规律提供了新视角，并强调了基于微生物组特征对老年人群进行分层的重要性。

Abstract

Gut microbial communities are likely remodeled in tandem with accumulated physiological decline during aging

yet there is limited under

standing 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.

关键词

Keywords

references

Abia ALK , Ubomba-Jaswa E , 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 . https://doi.org/10.18502/ijph.v48i5.1801 https://doi.org/10.18502/ijph.v48i5.1801

Arumugam M , Raes J , Pelletier E , et al. , 2011 . Enterotypes of the human gut microbiome . Nature , 473 ( 7346 ): 174 - 180 . https://doi.org/10.1038/nature09944 https://doi.org/10.1038/nature09944

Baumgartner M , Bayer F , Pfrunder-Cardozo KR , 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 . https://doi.org/10.1371/journal.pbio.3000465 https://doi.org/10.1371/journal.pbio.3000465

Chen LM , Collij V , Jaeger M , et al. , 2020 . Gut microbial co-abundance networks show specificity in inflammatory bowel disease and obesity . Nat Commun , 11 : 4018 . https://doi.org/10.1038/s41467-020-17840-y https://doi.org/10.1038/s41467-020-17840-y

Davies M , Galazzo G , van Hattem JM , et al. , 2022 . Enterobacteriaceae and Bacteroidaceae provide resistance to travel-associated intestinal colonization by multi-drug resistant Escherichia coli . Gut Microbes , 14 ( 1 ): 2060676 . https://doi.org/10.1080/19490976.2022.2060676 https://doi.org/10.1080/19490976.2022.2060676

Diard M , Garcia V , Maier L , et al. , 2013 . Stabilization of cooperative virulence by the expression of an avirulent phenotype . Nature , 494 ( 7437 ): 353 - 356 . https://doi.org/10.1038/nature11913 https://doi.org/10.1038/nature11913

Feng Q , Liang SS , Jia HJ , et al. , 2015 . Gut microbiome development along the colorectal adenoma‍–‍carcinoma sequence . Nat Commun , 6 : 6528 . https://doi.org/10.1038/ncomms7528 https://doi.org/10.1038/ncomms7528

Franzosa EA , McIver LJ , Rahnavard G , et al. , 2018 . Species-level functional profiling of metagenomes and metatranscriptomes . Nat Methods , 15 ( 11 ): 962 - 968 . https://doi.org/10.1038/s41592-018-0176-y https://doi.org/10.1038/s41592-018-0176-y

Gacesa R , Kurilshikov A , Vich Vila A , et al. , 2022 . Environmental factors shaping the gut microbiome in a Dutch population . Nature , 604 ( 7907 ): 732 - 739 . https://doi.org/10.1038/s41586-022-04567-7 https://doi.org/10.1038/s41586-022-04567-7

Ghosh TS , Shanahan F , O'Toole PW , 2022 . The gut microbiome as a modulator of healthy ageing . Nat Rev Gastroenterol Hepatol , 19 ( 9 ): 565 - 584 . https://doi.org/10.1038/s41575-022-00605-x https://doi.org/10.1038/s41575-022-00605-x

Ghoul M , Mitri S , 2016 . The ecology and evolution of microbial competition . Trends Microbiol , 24 ( 10 ): 833 - 845 . https://doi.org/10.1016/j.tim.2016.06.011 https://doi.org/10.1016/j.tim.2016.06.011

Han N , Peng XH , Zhang TT , et al. , 2024 . Rapid turnover and short-term blooms of Escherichia coli in the human gut . J Bacteriol , 206 ( 1 ): e0023923 . https://doi.org/10.1128/jb.00239-23 https://doi.org/10.1128/jb.00239-23

Herren CM , McMahon KD , 2017 . Cohesion: a method for quantifying the connectivity of microbial communities . ISME J , 11 ( 11 ): 2426 - 2438 . https://doi.org/10.1038/ismej.2017.91 https://doi.org/10.1038/ismej.2017.91

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

Jiao S , Yang YF , Xu YQ , et al. , 2020 . Balance between community assembly processes mediates species coexistence in agricultural soil microbiomes across Eastern China . ISME J , 14 ( 1 ): 202 - 216 . https://doi.org/10.1038/s41396-019-0522-9 https://doi.org/10.1038/s41396-019-0522-9

Kong FL , Deng FL , Li Y , 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 . https://doi.org/10.1080/19490976.2018.1494102 https://doi.org/10.1080/19490976.2018.1494102

Kuntal BK , Chandrakar P , Sadhu S , et al. , 2019 . ‘NetShift’: a methodology for understanding ‘driver microbes’ from healthy and disease microbiome datasets . ISME J , 13 ( 2 ): 442 - 454 . https://doi.org/10.1038/s41396-018-0291-x https://doi.org/10.1038/s41396-018-0291-x

Larson PJ , Zhou W , Santiago A , 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 . https://doi.org/10.1038/s43587-022-00287-9 https://doi.org/10.1038/s43587-022-00287-9

Leite G , Pimentel M , Barlow GM , et al. , 2022 . The small bowel microbiome changes significantly with age and aspects of the ageing process . Microb Cell , 9 ( 1 ): 21 - 23 . https://doi.org/10.15698/mic2022.01.768 https://doi.org/10.15698/mic2022.01.768

Li L , Jing S , Tang Y , 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 . https://doi.org/10.3389/fmicb.2024.1361218 https://doi.org/10.3389/fmicb.2024.1361218

Ling ZX , Liu X , Cheng YW , et al. , 2022 . Gut microbiota and aging . Crit Rev Food Sci Nutr , 62 ( 13 ): 3509 - 3534 . https://doi.org/10.1080/10408398.2020.1867054 https://doi.org/10.1080/10408398.2020.1867054

Lupp C , Robertson ML , Wickham ME , et al. , 2007 . Host-mediated inflammation disrupts the intestinal microbiota and promotes the overgrowth of enterobacteriaceae . Cell Host Microbe , 2 ( 3 ): 204 . https://doi.org/10.1016/j.chom.2007.08.002 https://doi.org/10.1016/j.chom.2007.08.002

Martinson JNV , Walk ST , 2020 . Escherichia coli residency in the gut of healthy human adults . EcoSal Plus , 9 ( 1 ): 10 .1128/ecosalplus.ESP-0003-2020. https://doi.org/10.1128/ecosalplus.ESP-0003-2020 https://doi.org/10.1128/ecosalplus.ESP-0003-2020

Martinson JNV , Pinkham NV , Peters GW , et al. , 2019 . Rethinking gut microbiome residency and the Enterobacteriaceae in healthy human adults . ISME J , 13 ( 9 ):‍ 2306 - 2318 . https://doi.org/10.1038/s41396-019-0435-7 https://doi.org/10.1038/s41396-019-0435-7

Moreira de Gouveia MI , Bernalier-Donadille A , Jubelin G , 2024 . Enterobacteriaceae in the human gut: dynamics and ecological roles in health and disease . Biology , 13 ( 3 ): 142 . https://doi.org/10.3390/biology13030142 https://doi.org/10.3390/biology13030142

Mossad O , Batut B , Yilmaz B , 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 . https://doi.org/10.1038/s41593-022-01027-3 https://doi.org/10.1038/s41593-022-01027-3

Mottawea W , Chiang CK , Mühlbauer M , et al. , 2016 . Altered intestinal microbiota‍‍–‍host mitochondria crosstalk in new onset Crohn’s disease . Nat Commun , 7 : 13419 . https://doi.org/10.1038/ncomms13419 https://doi.org/10.1038/ncomms13419

O'Toole PW , Jeffery IB , 2015 . Gut microbiota and aging . Science , 350 ( 6265 ): 1214 - 1215 . https://doi.org/10.1126/science.aac8469 https://doi.org/10.1126/science.aac8469

Pal S , Juyal D , Adekhandi S , et al. , 2015 . Mobile phones: reservoirs for the transmission of nosocomial pathogens . Adv Biomed Res , 4 ( 1 ): 144 . https://doi.org/10.4103/2277-9175.161553 https://doi.org/10.4103/2277-9175.161553

Pang SF , Chen XD , Lu ZL , et al. , 2023 . Longevity of centenarians is reflected by the gut microbiome with youth-associated signatures . Nat Aging , 3 ( 4 ): 436 - 449 . https://doi.org/10.1038/s43587-023-00389-y https://doi.org/10.1038/s43587-023-00389-y

Qi HB , Wei JM , Gao YH , et al. , 2020 . Reg4 and complement factor D prevent the overgrowth of E . coli in the mouse gut . Commun Biol , 3 : 483 . https://doi.org/10.1038/s42003-020-01219-2 https://doi.org/10.1038/s42003-020-01219-2

Qin JJ , Li YR , Cai ZM , et al. , 2012 . A metagenome-wide association study of gut microbiota in type 2 diabetes . Nature , 490 ( 7418 ): 55 - 60 . https://doi.org/10.1038/nature11450 https://doi.org/10.1038/nature11450

Roth-Schulze AJ , Penno MAS , Ngui KM , 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 . https://doi.org/10.1186/s40168-021-01104-y https://doi.org/10.1186/s40168-021-01104-y

Salahshouri P , Emadi-Baygi M , Jalili M , et al. , 2021 . A metabolic model of intestinal secretions: the link between human microbiota and colorectal cancer progression . Metabolites , 11 ( 7 ): 456 https://doi.org/10.3390/metabo11070456 https://doi.org/10.3390/metabo11070456

Tan XJ , Wang YZ , Gong T , 2023 . The interplay between oral microbiota, gut microbiota and systematic diseases . J Oral Microbiol , 15 ( 1 ): 2213112 . https://doi.org/10.1080/20002297.2023.2213112 https://doi.org/10.1080/20002297.2023.2213112

Thomas AM , Manghi P , Asnicar F , 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 . https://doi.org/10.1038/s41591-019-0405-7 https://doi.org/10.1038/s41591-019-0405-7

Vogtmann E , Hua X , Zeller G , et al. , 2016 . Colorectal cancer and the human gut microbiome: reproducibility with whole-genome shotgun sequencing . PLoS ONE , 11 ( 5 ): e0155362 . https://doi.org/10.1371/journal.pone.0155362 https://doi.org/10.1371/journal.pone.0155362

Wibowo MC , Yang Z , Borry M , et al. , 2021 . Reconstruction of ancient microbial genomes from the human gut . Nature , 594 ( 7862 ): 234 - 239 . https://doi.org/10.1038/s41586-021-03532-0 https://doi.org/10.1038/s41586-021-03532-0

Wirbel J , Pyl PT , Kartal E , et al. , 2019 . Meta-analysis of fecal metagenomes reveals global microbial signatures that are specific for colorectal cancer . Nat Med , 25 ( 4 ): 679 - 689 . https://doi.org/10.1038/s41591-019-0406-6 https://doi.org/10.1038/s41591-019-0406-6

Xiao LW , Wang JF , Zheng JY , et al. , 2021 . Deterministic transition of enterotypes shapes the infant gut microbiome at an early age . Genome Biol , 22 : 243 . https://doi.org/10.1186/s13059-021-02463-3 https://doi.org/10.1186/s13059-021-02463-3

Yachida S , Mizutani S , Shiroma H , 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 . https://doi.org/10.1038/s41591-019-0458-7 https://doi.org/10.1038/s41591-019-0458-7

Yu LL , Pan JN , Guo M , et al. , 2023 . Gut microbiota and anti-aging: focusing on spermidine . Crit Rev Food Sci Nutr , 64 ( 28 ): 10419 - 10437 . https://doi.org/10.1080/10408398.2023.2224867 https://doi.org/10.1080/10408398.2023.2224867

Zeller G , Tap J , Voigt AY , et al. , 2014 . Potential of fecal microbiota for early-stage detection of colorectal cancer . Mol Syst Biol , 10 ( 11 ): 766 . https://doi.org/10.15252/msb.20145645 https://doi.org/10.15252/msb.20145645

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Metagenomics reveals an increased proportion of an Escherichia coli-dominated enterotype in elderly Chinese people

Metagenomics reveals an increased proportion of an Escherichia coli-dominated enterotype in elderly Chinese people

DOI：10.1631/jzus.B2400341

摘要

Abstract

关键词

Keywords

references