A Cross-Sectional Study of Compositional and Functional Profiles of Gut Microbiota in Sardinian Centenarians

ABSTRACT Sardinia, Italy, has a high prevalence of residents who live more than 100 years. The reasons for longevity in this isolated region are currently unknown. Gut microbiota may hold a clue. To explore the role gut microbiota may play in healthy aging and longevity, we used metagenomic sequenci...

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Autores principales: Lu Wu, Tiansheng Zeng, Angelo Zinellu, Salvatore Rubino, David J. Kelvin, Ciriaco Carru
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Publicado: American Society for Microbiology 2019
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Acceso en línea:https://doaj.org/article/181b3649996140b2b1bcd3f20a2a59b6
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spelling oai:doaj.org-article:181b3649996140b2b1bcd3f20a2a59b62021-12-02T19:47:35ZA Cross-Sectional Study of Compositional and Functional Profiles of Gut Microbiota in Sardinian Centenarians10.1128/mSystems.00325-192379-5077https://doaj.org/article/181b3649996140b2b1bcd3f20a2a59b62019-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00325-19https://doaj.org/toc/2379-5077ABSTRACT Sardinia, Italy, has a high prevalence of residents who live more than 100 years. The reasons for longevity in this isolated region are currently unknown. Gut microbiota may hold a clue. To explore the role gut microbiota may play in healthy aging and longevity, we used metagenomic sequencing to determine the compositional and functional differences in gut microbiota associated with populations of different ages in Sardinia. Our data revealed that the gut microbiota of both young and elderly Sardinians shared similar taxonomic and functional profiles. A different pattern was found in centenarians. Within the centenarian group, the gut microbiota was correlated with the functional independence measurement of the host. Centenarians had a higher diversity of core microbiota species and microbial genes than those in the young and elderly. We found that the gut microbiota in Sardinian centenarians displayed a rearranged taxonomic pattern compared with those of the young and elderly, featured by depletion of Faecalibacterium prausnitzii and Eubacterium rectale and enriched for Methanobrevibacter smithii and Bifidobacterium adolescentis. Moreover, functional analysis revealed that the microbiota in centenarians had high capacity for central metabolism, especially glycolysis and fermentation to short-chain fatty acids (SCFAs), although the gut microbiota in centenarians was low in genes encoding enzymes involved in degradation of carbohydrates, including fibers and galactose. IMPORTANCE The gut microbiota has been proposed as a promising determinant for human health. Centenarians as a model for extreme aging may help us understand the correlation of gut microbiota with healthy aging and longevity. Here we confirmed that centenarians had microbiota elements usually associated with benefits to health. Our finding of a high capacity of glycolysis and related SCFA production represented a healthy microbiome and environment that is regarded as beneficial for host gut epithelium. The low abundance of genes encoding components of pathways involved in carbohydrate degradation was also found in the gut microbiota of Sardinian centenarians and is often associated with poor gut health. Overall, our study here represents an expansion of previous research investigating the age-related changes in gut microbiota. Furthermore, our study provides a new prospective for potential targets for gut microbiota intervention directed at limiting gut inflammation and pathology and enhancing a healthy gut barrier.Lu WuTiansheng ZengAngelo ZinelluSalvatore RubinoDavid J. KelvinCiriaco CarruAmerican Society for Microbiologyarticlecentenariangut microbiotalongevitymetagenomic sequencingMicrobiologyQR1-502ENmSystems, Vol 4, Iss 4 (2019)
institution DOAJ
collection DOAJ
language EN
topic centenarian
gut microbiota
longevity
metagenomic sequencing
Microbiology
QR1-502
spellingShingle centenarian
gut microbiota
longevity
metagenomic sequencing
Microbiology
QR1-502
Lu Wu
Tiansheng Zeng
Angelo Zinellu
Salvatore Rubino
David J. Kelvin
Ciriaco Carru
A Cross-Sectional Study of Compositional and Functional Profiles of Gut Microbiota in Sardinian Centenarians
description ABSTRACT Sardinia, Italy, has a high prevalence of residents who live more than 100 years. The reasons for longevity in this isolated region are currently unknown. Gut microbiota may hold a clue. To explore the role gut microbiota may play in healthy aging and longevity, we used metagenomic sequencing to determine the compositional and functional differences in gut microbiota associated with populations of different ages in Sardinia. Our data revealed that the gut microbiota of both young and elderly Sardinians shared similar taxonomic and functional profiles. A different pattern was found in centenarians. Within the centenarian group, the gut microbiota was correlated with the functional independence measurement of the host. Centenarians had a higher diversity of core microbiota species and microbial genes than those in the young and elderly. We found that the gut microbiota in Sardinian centenarians displayed a rearranged taxonomic pattern compared with those of the young and elderly, featured by depletion of Faecalibacterium prausnitzii and Eubacterium rectale and enriched for Methanobrevibacter smithii and Bifidobacterium adolescentis. Moreover, functional analysis revealed that the microbiota in centenarians had high capacity for central metabolism, especially glycolysis and fermentation to short-chain fatty acids (SCFAs), although the gut microbiota in centenarians was low in genes encoding enzymes involved in degradation of carbohydrates, including fibers and galactose. IMPORTANCE The gut microbiota has been proposed as a promising determinant for human health. Centenarians as a model for extreme aging may help us understand the correlation of gut microbiota with healthy aging and longevity. Here we confirmed that centenarians had microbiota elements usually associated with benefits to health. Our finding of a high capacity of glycolysis and related SCFA production represented a healthy microbiome and environment that is regarded as beneficial for host gut epithelium. The low abundance of genes encoding components of pathways involved in carbohydrate degradation was also found in the gut microbiota of Sardinian centenarians and is often associated with poor gut health. Overall, our study here represents an expansion of previous research investigating the age-related changes in gut microbiota. Furthermore, our study provides a new prospective for potential targets for gut microbiota intervention directed at limiting gut inflammation and pathology and enhancing a healthy gut barrier.
format article
author Lu Wu
Tiansheng Zeng
Angelo Zinellu
Salvatore Rubino
David J. Kelvin
Ciriaco Carru
author_facet Lu Wu
Tiansheng Zeng
Angelo Zinellu
Salvatore Rubino
David J. Kelvin
Ciriaco Carru
author_sort Lu Wu
title A Cross-Sectional Study of Compositional and Functional Profiles of Gut Microbiota in Sardinian Centenarians
title_short A Cross-Sectional Study of Compositional and Functional Profiles of Gut Microbiota in Sardinian Centenarians
title_full A Cross-Sectional Study of Compositional and Functional Profiles of Gut Microbiota in Sardinian Centenarians
title_fullStr A Cross-Sectional Study of Compositional and Functional Profiles of Gut Microbiota in Sardinian Centenarians
title_full_unstemmed A Cross-Sectional Study of Compositional and Functional Profiles of Gut Microbiota in Sardinian Centenarians
title_sort cross-sectional study of compositional and functional profiles of gut microbiota in sardinian centenarians
publisher American Society for Microbiology
publishDate 2019
url https://doaj.org/article/181b3649996140b2b1bcd3f20a2a59b6
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