Multi-omics insights implicate the remodeling of the intestinal structure and microbiome in aging

BackgroundAging can impair the ability of elderly individuals to fight infections and trigger persistent systemic inflammation, a condition known as inflammaging. However, the mechanisms underlying the development of inflammaging remain unknown.MethodsWe conducted 16S rRNA sequencing of intestinal c...

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Main Authors: Shaohua Chen, Chengbang Wang, Xiong Zou, Hanwen Li, Guanglin Yang, Xiaotao Su, Zengnan Mo
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-11-01
Series:Frontiers in Genetics
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Online Access:https://www.frontiersin.org/articles/10.3389/fgene.2024.1450064/full
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author Shaohua Chen
Shaohua Chen
Chengbang Wang
Xiong Zou
Hanwen Li
Guanglin Yang
Guanglin Yang
Xiaotao Su
Xiaotao Su
Zengnan Mo
Zengnan Mo
author_facet Shaohua Chen
Shaohua Chen
Chengbang Wang
Xiong Zou
Hanwen Li
Guanglin Yang
Guanglin Yang
Xiaotao Su
Xiaotao Su
Zengnan Mo
Zengnan Mo
author_sort Shaohua Chen
collection DOAJ
description BackgroundAging can impair the ability of elderly individuals to fight infections and trigger persistent systemic inflammation, a condition known as inflammaging. However, the mechanisms underlying the development of inflammaging remain unknown.MethodsWe conducted 16S rRNA sequencing of intestinal contents from young and old C57BL/6J mice to elucidate changes in gut microbiota diversity and microbial community composition after aging. Aging-related differential bacterial taxa were then identified, and their abundance trends were validated in human samples. The variances in intestinal barrier function and circulating endotoxin between groups were also assessed. Furthermore, widely targeted metabolomics was conducted to characterize metabolic profiles after aging and to investigate the key metabolic pathways enriched by the differential metabolites.ResultsOur findings demonstrated an increase in relative proportion of pathogenic bacteria with age, a trend also revealed in healthy populations of different age groups. Additionally, aging individuals exhibited reduced intestinal barrier function and increased circulating endotoxin levels. Widely targeted metabolomics revealed a significant increase in various secondary bile acid metabolites after aging, positively correlated with the relative abundance of several aging-related bacterial taxa. Furthermore, old group had lower levels of various anti-inflammatory or beneficial metabolites. Enrichment analysis identified the starch and sucrose metabolism pathway as potentially the most significantly impacted signaling pathway during aging.ConclusionThis study aimed to provide insights into the complex interactions involved in organismal inflammaging through microbial multi-omics. These findings lay a solid foundation for future research aimed at identifying novel biomarkers for the clinical diagnosis of aging-related diseases or potential therapeutic targets.
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spelling doaj-art-0a8c4a01ace4467e83bbca86f8c4264d2024-11-12T06:15:29ZengFrontiers Media S.A.Frontiers in Genetics1664-80212024-11-011510.3389/fgene.2024.14500641450064Multi-omics insights implicate the remodeling of the intestinal structure and microbiome in agingShaohua Chen0Shaohua Chen1Chengbang Wang2Xiong Zou3Hanwen Li4Guanglin Yang5Guanglin Yang6Xiaotao Su7Xiaotao Su8Zengnan Mo9Zengnan Mo10Department of Urology, Guangxi Medical University Cancer Hospital, Nanning, Guangxi, ChinaCenter for Genomic and Personalized Medicine, Guangxi key Laboratory for Genomic and Personalized Medicine, Guangxi Collaborative Innovation Center for Genomic and Personalized Medicine, Guangxi Medical University, Nanning, Guangxi, ChinaCenter for Genomic and Personalized Medicine, Guangxi key Laboratory for Genomic and Personalized Medicine, Guangxi Collaborative Innovation Center for Genomic and Personalized Medicine, Guangxi Medical University, Nanning, Guangxi, ChinaCenter for Genomic and Personalized Medicine, Guangxi key Laboratory for Genomic and Personalized Medicine, Guangxi Collaborative Innovation Center for Genomic and Personalized Medicine, Guangxi Medical University, Nanning, Guangxi, ChinaCenter for Genomic and Personalized Medicine, Guangxi key Laboratory for Genomic and Personalized Medicine, Guangxi Collaborative Innovation Center for Genomic and Personalized Medicine, Guangxi Medical University, Nanning, Guangxi, ChinaDepartment of Urology, Guangxi Medical University Cancer Hospital, Nanning, Guangxi, ChinaCenter for Genomic and Personalized Medicine, Guangxi key Laboratory for Genomic and Personalized Medicine, Guangxi Collaborative Innovation Center for Genomic and Personalized Medicine, Guangxi Medical University, Nanning, Guangxi, ChinaCenter for Genomic and Personalized Medicine, Guangxi key Laboratory for Genomic and Personalized Medicine, Guangxi Collaborative Innovation Center for Genomic and Personalized Medicine, Guangxi Medical University, Nanning, Guangxi, ChinaDepartment of Neurology, First Affiliated Hospital of Guangxi Medical University, Guangxi Medical University, Nanning, Guangxi, ChinaCenter for Genomic and Personalized Medicine, Guangxi key Laboratory for Genomic and Personalized Medicine, Guangxi Collaborative Innovation Center for Genomic and Personalized Medicine, Guangxi Medical University, Nanning, Guangxi, ChinaInstitute of Urology and Nephrology, First Affiliated Hospital of Guangxi Medical University, Guangxi Medical University, Nanning, Guangxi, ChinaBackgroundAging can impair the ability of elderly individuals to fight infections and trigger persistent systemic inflammation, a condition known as inflammaging. However, the mechanisms underlying the development of inflammaging remain unknown.MethodsWe conducted 16S rRNA sequencing of intestinal contents from young and old C57BL/6J mice to elucidate changes in gut microbiota diversity and microbial community composition after aging. Aging-related differential bacterial taxa were then identified, and their abundance trends were validated in human samples. The variances in intestinal barrier function and circulating endotoxin between groups were also assessed. Furthermore, widely targeted metabolomics was conducted to characterize metabolic profiles after aging and to investigate the key metabolic pathways enriched by the differential metabolites.ResultsOur findings demonstrated an increase in relative proportion of pathogenic bacteria with age, a trend also revealed in healthy populations of different age groups. Additionally, aging individuals exhibited reduced intestinal barrier function and increased circulating endotoxin levels. Widely targeted metabolomics revealed a significant increase in various secondary bile acid metabolites after aging, positively correlated with the relative abundance of several aging-related bacterial taxa. Furthermore, old group had lower levels of various anti-inflammatory or beneficial metabolites. Enrichment analysis identified the starch and sucrose metabolism pathway as potentially the most significantly impacted signaling pathway during aging.ConclusionThis study aimed to provide insights into the complex interactions involved in organismal inflammaging through microbial multi-omics. These findings lay a solid foundation for future research aimed at identifying novel biomarkers for the clinical diagnosis of aging-related diseases or potential therapeutic targets.https://www.frontiersin.org/articles/10.3389/fgene.2024.1450064/fullaginginflammaginggut microbiotametabolismintestinal epithelial cells
spellingShingle Shaohua Chen
Shaohua Chen
Chengbang Wang
Xiong Zou
Hanwen Li
Guanglin Yang
Guanglin Yang
Xiaotao Su
Xiaotao Su
Zengnan Mo
Zengnan Mo
Multi-omics insights implicate the remodeling of the intestinal structure and microbiome in aging
Frontiers in Genetics
aging
inflammaging
gut microbiota
metabolism
intestinal epithelial cells
title Multi-omics insights implicate the remodeling of the intestinal structure and microbiome in aging
title_full Multi-omics insights implicate the remodeling of the intestinal structure and microbiome in aging
title_fullStr Multi-omics insights implicate the remodeling of the intestinal structure and microbiome in aging
title_full_unstemmed Multi-omics insights implicate the remodeling of the intestinal structure and microbiome in aging
title_short Multi-omics insights implicate the remodeling of the intestinal structure and microbiome in aging
title_sort multi omics insights implicate the remodeling of the intestinal structure and microbiome in aging
topic aging
inflammaging
gut microbiota
metabolism
intestinal epithelial cells
url https://www.frontiersin.org/articles/10.3389/fgene.2024.1450064/full
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