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...
| Main Authors: | , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2020-04-01
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| Series: | mSystems |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/mSystems.00124-20 |
| _version_ | 1818691869483204608 |
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| 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 |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-12-17T12:48:45Z |
| format | Article |
| id | doaj.art-1c9d249f5b1543c5b9f1176e42e18bf6 |
| institution | Directory Open Access Journal |
| issn | 2379-5077 |
| language | English |
| last_indexed | 2024-12-17T12:48:45Z |
| publishDate | 2020-04-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mSystems |
| spelling | doaj.art-1c9d249f5b1543c5b9f1176e42e18bf62022-12-21T21:47:40ZengAmerican Society for MicrobiologymSystems2379-50772020-04-015210.1128/mSystems.00124-20Shotgun Metagenomics of Gut Microbiota in Humans with up to Extreme Longevity and the Increasing Role of Xenobiotic DegradationSimone Rampelli0Matteo Soverini1Federica D’Amico2Monica Barone3Teresa Tavella4Daniela Monti5Miriam Capri6Annalisa Astolfi7Patrizia Brigidi8Elena Biagi9Claudio Franceschi10Silvia Turroni11Marco Candela12Unit of Microbial Ecology of Health, Department of Pharmacy and Biotechnology, University of Bologna, Bologna, ItalyUnit of Microbial Ecology of Health, Department of Pharmacy and Biotechnology, University of Bologna, Bologna, ItalyUnit of Microbial Ecology of Health, Department of Pharmacy and Biotechnology, University of Bologna, Bologna, ItalyUnit of Microbial Ecology of Health, Department of Pharmacy and Biotechnology, University of Bologna, Bologna, ItalyUnit of Microbial Ecology of Health, Department of Pharmacy and Biotechnology, University of Bologna, Bologna, ItalyDepartment of Experimental and Clinical Biomedical Sciences Mario Serio, University of Florence, Florence, ItalyDepartment of Experimental, Diagnostic and Specialty Medicine, University of Bologna, Bologna, ItalyGiorgio Prodi Cancer Research Center, University of Bologna, Bologna, ItalyUnit of Microbial Ecology of Health, Department of Pharmacy and Biotechnology, University of Bologna, Bologna, ItalyUnit of Microbial Ecology of Health, Department of Pharmacy and Biotechnology, University of Bologna, Bologna, ItalyIRCCS, Institute of Neurologic Sciences of Bologna, Bellaria Hospital, Bologna, ItalyUnit of Microbial Ecology of Health, Department of Pharmacy and Biotechnology, University of Bologna, Bologna, ItalyUnit of Microbial Ecology of Health, Department of Pharmacy and Biotechnology, University of Bologna, Bologna, ItalyABSTRACT 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.https://journals.asm.org/doi/10.1128/mSystems.00124-20microbiomemetagenomeextreme longevityxenobioticsaging |
| spellingShingle | 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 mSystems microbiome metagenome extreme longevity xenobiotics aging |
| title | 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_short | 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 |
| topic | microbiome metagenome extreme longevity xenobiotics aging |
| url | https://journals.asm.org/doi/10.1128/mSystems.00124-20 |
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