Shotgun Metagenomics of Gut Microbiota in Humans with up to Extreme Longevity and the Increasing Role of Xenobiotic Degradation

ABSTRACT The gut microbiome of long-lived people display an increasing abundance of subdominant species, as well as a rearrangement in health-associated bacteria, but less is known about microbiome functions. In order to disentangle the contribution of the gut microbiome to the complex trait of huma...

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Autores principales:	Simone Rampelli, Matteo Soverini, Federica D’Amico, Monica Barone, Teresa Tavella, Daniela Monti, Miriam Capri, Annalisa Astolfi, Patrizia Brigidi, Elena Biagi, Claudio Franceschi, Silvia Turroni, Marco Candela
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Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	microbiome metagenome extreme longevity xenobiotics aging Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/1c9d249f5b1543c5b9f1176e42e18bf6
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spelling	oai:doaj.org-article:1c9d249f5b1543c5b9f1176e42e18bf62021-12-02T18:15:45ZShotgun Metagenomics of Gut Microbiota in Humans with up to Extreme Longevity and the Increasing Role of Xenobiotic Degradation10.1128/mSystems.00124-202379-5077https://doaj.org/article/1c9d249f5b1543c5b9f1176e42e18bf62020-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00124-20https://doaj.org/toc/2379-5077ABSTRACT The gut microbiome of long-lived people display an increasing abundance of subdominant species, as well as a rearrangement in health-associated bacteria, but less is known about microbiome functions. In order to disentangle the contribution of the gut microbiome to the complex trait of human longevity, we here describe the metagenomic change of the human gut microbiome along with aging in subjects with up to extreme longevity, including centenarians (aged 99 to 104 years) and semisupercentenarians (aged 105 to 109 years), i.e., demographically very uncommon subjects who reach the extreme limit of the human life span. According to our findings, the gut microbiome of centenarians and semisupercentenarians is more suited for xenobiotic degradation and shows a rearrangement in metabolic pathways related to carbohydrate, amino acid, and lipid metabolism. Collectively, our data go beyond the relationship between intestinal bacteria and physiological changes that occur with aging by detailing the shifts in the potential metagenomic functions of the gut microbiome of centenarians and semisupercentenarians as a response to progressive dietary and lifestyle modifications. IMPORTANCE The study of longevity may help us understand how human beings can delay or survive the most frequent age-related diseases and morbidities. In this scenario, the gut microbiome has been proposed as one of the variables to monitor and possibly support healthy aging. Indeed, the disruption of host-gut microbiome homeostasis has been associated with inflammation and intestinal permeability as well as a general decline in bone and cognitive health. Here, we performed a metagenomic assessment of fecal samples from semisupercentenarians, i.e., 105 to 109 years old, in comparison to young adults, the elderly, and centenarians, shedding light on the longest compositional and functional trajectory of the human gut microbiome with aging. In addition to providing a fine taxonomic resolution down to the species level, our study emphasizes the progressive age-related increase in degradation pathways of pervasive xenobiotics in Western societies, possibly as a result of a supportive process within the molecular continuum characterizing aging.Simone RampelliMatteo SoveriniFederica D’AmicoMonica BaroneTeresa TavellaDaniela MontiMiriam CapriAnnalisa AstolfiPatrizia BrigidiElena BiagiClaudio FranceschiSilvia TurroniMarco CandelaAmerican Society for Microbiologyarticlemicrobiomemetagenomeextreme longevityxenobioticsagingMicrobiologyQR1-502ENmSystems, Vol 5, Iss 2 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	microbiome metagenome extreme longevity xenobiotics aging Microbiology QR1-502
spellingShingle	microbiome metagenome extreme longevity xenobiotics aging Microbiology QR1-502 Simone Rampelli Matteo Soverini Federica D’Amico Monica Barone Teresa Tavella Daniela Monti Miriam Capri Annalisa Astolfi Patrizia Brigidi Elena Biagi Claudio Franceschi Silvia Turroni Marco Candela Shotgun Metagenomics of Gut Microbiota in Humans with up to Extreme Longevity and the Increasing Role of Xenobiotic Degradation
description	ABSTRACT The gut microbiome of long-lived people display an increasing abundance of subdominant species, as well as a rearrangement in health-associated bacteria, but less is known about microbiome functions. In order to disentangle the contribution of the gut microbiome to the complex trait of human longevity, we here describe the metagenomic change of the human gut microbiome along with aging in subjects with up to extreme longevity, including centenarians (aged 99 to 104 years) and semisupercentenarians (aged 105 to 109 years), i.e., demographically very uncommon subjects who reach the extreme limit of the human life span. According to our findings, the gut microbiome of centenarians and semisupercentenarians is more suited for xenobiotic degradation and shows a rearrangement in metabolic pathways related to carbohydrate, amino acid, and lipid metabolism. Collectively, our data go beyond the relationship between intestinal bacteria and physiological changes that occur with aging by detailing the shifts in the potential metagenomic functions of the gut microbiome of centenarians and semisupercentenarians as a response to progressive dietary and lifestyle modifications. IMPORTANCE The study of longevity may help us understand how human beings can delay or survive the most frequent age-related diseases and morbidities. In this scenario, the gut microbiome has been proposed as one of the variables to monitor and possibly support healthy aging. Indeed, the disruption of host-gut microbiome homeostasis has been associated with inflammation and intestinal permeability as well as a general decline in bone and cognitive health. Here, we performed a metagenomic assessment of fecal samples from semisupercentenarians, i.e., 105 to 109 years old, in comparison to young adults, the elderly, and centenarians, shedding light on the longest compositional and functional trajectory of the human gut microbiome with aging. In addition to providing a fine taxonomic resolution down to the species level, our study emphasizes the progressive age-related increase in degradation pathways of pervasive xenobiotics in Western societies, possibly as a result of a supportive process within the molecular continuum characterizing aging.
format	article
author	Simone Rampelli Matteo Soverini Federica D’Amico Monica Barone Teresa Tavella Daniela Monti Miriam Capri Annalisa Astolfi Patrizia Brigidi Elena Biagi Claudio Franceschi Silvia Turroni Marco Candela
author_facet	Simone Rampelli Matteo Soverini Federica D’Amico Monica Barone Teresa Tavella Daniela Monti Miriam Capri Annalisa Astolfi Patrizia Brigidi Elena Biagi Claudio Franceschi Silvia Turroni Marco Candela
author_sort	Simone Rampelli
title	Shotgun Metagenomics of Gut Microbiota in Humans with up to Extreme Longevity and the Increasing Role of Xenobiotic Degradation
title_short	Shotgun Metagenomics of Gut Microbiota in Humans with up to Extreme Longevity and the Increasing Role of Xenobiotic Degradation
title_full	Shotgun Metagenomics of Gut Microbiota in Humans with up to Extreme Longevity and the Increasing Role of Xenobiotic Degradation
title_fullStr	Shotgun Metagenomics of Gut Microbiota in Humans with up to Extreme Longevity and the Increasing Role of Xenobiotic Degradation
title_full_unstemmed	Shotgun Metagenomics of Gut Microbiota in Humans with up to Extreme Longevity and the Increasing Role of Xenobiotic Degradation
title_sort	shotgun metagenomics of gut microbiota in humans with up to extreme longevity and the increasing role of xenobiotic degradation
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/1c9d249f5b1543c5b9f1176e42e18bf6
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Shotgun Metagenomics of Gut Microbiota in Humans with up to Extreme Longevity and the Increasing Role of Xenobiotic Degradation

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