Integrative metagenomic analysis reveals distinct gut microbial signatures related to obesity

Abstract Obesity is a metabolic disorder closely associated with profound alterations in gut microbial composition. However, the dynamics of species composition and functional changes in the gut microbiome in obesity remain to be comprehensively investigated. In this study, we conducted a meta-analy...

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Main Authors: Xinliang Hu, Chong Yu, Yuting He, Songling Zhu, Shuang Wang, Ziqiong Xu, Shaohui You, Yanlei Jiao, Shu-Lin Liu, Hongxia Bao
Format: Article
Language:English
Published: BMC 2024-04-01
Series:BMC Microbiology
Subjects:
Online Access:https://doi.org/10.1186/s12866-024-03278-5
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author Xinliang Hu
Chong Yu
Yuting He
Songling Zhu
Shuang Wang
Ziqiong Xu
Shaohui You
Yanlei Jiao
Shu-Lin Liu
Hongxia Bao
author_facet Xinliang Hu
Chong Yu
Yuting He
Songling Zhu
Shuang Wang
Ziqiong Xu
Shaohui You
Yanlei Jiao
Shu-Lin Liu
Hongxia Bao
author_sort Xinliang Hu
collection DOAJ
description Abstract Obesity is a metabolic disorder closely associated with profound alterations in gut microbial composition. However, the dynamics of species composition and functional changes in the gut microbiome in obesity remain to be comprehensively investigated. In this study, we conducted a meta-analysis of metagenomic sequencing data from both obese and non-obese individuals across multiple cohorts, totaling 1351 fecal metagenomes. Our results demonstrate a significant decrease in both the richness and diversity of the gut bacteriome and virome in obese patients. We identified 38 bacterial species including Eubacterium sp. CAG:274, Ruminococcus gnavus, Eubacterium eligens and Akkermansia muciniphila, and 1 archaeal species, Methanobrevibacter smithii, that were significantly altered in obesity. Additionally, we observed altered abundance of five viral families: Mesyanzhinovviridae, Chaseviridae, Salasmaviridae, Drexlerviridae, and Casjensviridae. Functional analysis of the gut microbiome indicated distinct signatures associated to obesity and identified Ruminococcus gnavus as the primary driver for function enrichment in obesity, and Methanobrevibacter smithii, Akkermansia muciniphila, Ruminococcus bicirculans, and Eubacterium siraeum as functional drivers in the healthy control group. Additionally, our results suggest that antibiotic resistance genes and bacterial virulence factors may influence the development of obesity. Finally, we demonstrated that gut vOTUs achieved a diagnostic accuracy with an optimal area under the curve of 0.766 for distinguishing obesity from healthy controls. Our findings offer comprehensive and generalizable insights into the gut bacteriome and virome features associated with obesity, with the potential to guide the development of microbiome-based diagnostics.
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spelling doaj.art-d2cf2da90eb64eecbb94672b695cd1c42024-04-07T11:10:22ZengBMCBMC Microbiology1471-21802024-04-0124111610.1186/s12866-024-03278-5Integrative metagenomic analysis reveals distinct gut microbial signatures related to obesityXinliang Hu0Chong Yu1Yuting He2Songling Zhu3Shuang Wang4Ziqiong Xu5Shaohui You6Yanlei Jiao7Shu-Lin Liu8Hongxia Bao9Genomics Research Center, Key Laboratory of Gut Microbiota and Pharmacogenomics of Heilongjiang Province, State-Province Key Laboratory of Biomedicine-Pharmaceutics of China, College of Pharmacy, Harbin Medical UniversityGenomics Research Center, Key Laboratory of Gut Microbiota and Pharmacogenomics of Heilongjiang Province, State-Province Key Laboratory of Biomedicine-Pharmaceutics of China, College of Pharmacy, Harbin Medical UniversityGenomics Research Center, Key Laboratory of Gut Microbiota and Pharmacogenomics of Heilongjiang Province, State-Province Key Laboratory of Biomedicine-Pharmaceutics of China, College of Pharmacy, Harbin Medical UniversityGenomics Research Center, Key Laboratory of Gut Microbiota and Pharmacogenomics of Heilongjiang Province, State-Province Key Laboratory of Biomedicine-Pharmaceutics of China, College of Pharmacy, Harbin Medical UniversityDepartment of Biopharmaceutical Sciences (State-Province Key Laboratories of Biomedicine-Pharmaceutics of China), College of Pharmacy, Harbin Medical UniversityGenomics Research Center, Key Laboratory of Gut Microbiota and Pharmacogenomics of Heilongjiang Province, State-Province Key Laboratory of Biomedicine-Pharmaceutics of China, College of Pharmacy, Harbin Medical UniversityGenomics Research Center, Key Laboratory of Gut Microbiota and Pharmacogenomics of Heilongjiang Province, State-Province Key Laboratory of Biomedicine-Pharmaceutics of China, College of Pharmacy, Harbin Medical UniversityGenomics Research Center, Key Laboratory of Gut Microbiota and Pharmacogenomics of Heilongjiang Province, State-Province Key Laboratory of Biomedicine-Pharmaceutics of China, College of Pharmacy, Harbin Medical UniversityGenomics Research Center, Key Laboratory of Gut Microbiota and Pharmacogenomics of Heilongjiang Province, State-Province Key Laboratory of Biomedicine-Pharmaceutics of China, College of Pharmacy, Harbin Medical UniversityGenomics Research Center, Key Laboratory of Gut Microbiota and Pharmacogenomics of Heilongjiang Province, State-Province Key Laboratory of Biomedicine-Pharmaceutics of China, College of Pharmacy, Harbin Medical UniversityAbstract Obesity is a metabolic disorder closely associated with profound alterations in gut microbial composition. However, the dynamics of species composition and functional changes in the gut microbiome in obesity remain to be comprehensively investigated. In this study, we conducted a meta-analysis of metagenomic sequencing data from both obese and non-obese individuals across multiple cohorts, totaling 1351 fecal metagenomes. Our results demonstrate a significant decrease in both the richness and diversity of the gut bacteriome and virome in obese patients. We identified 38 bacterial species including Eubacterium sp. CAG:274, Ruminococcus gnavus, Eubacterium eligens and Akkermansia muciniphila, and 1 archaeal species, Methanobrevibacter smithii, that were significantly altered in obesity. Additionally, we observed altered abundance of five viral families: Mesyanzhinovviridae, Chaseviridae, Salasmaviridae, Drexlerviridae, and Casjensviridae. Functional analysis of the gut microbiome indicated distinct signatures associated to obesity and identified Ruminococcus gnavus as the primary driver for function enrichment in obesity, and Methanobrevibacter smithii, Akkermansia muciniphila, Ruminococcus bicirculans, and Eubacterium siraeum as functional drivers in the healthy control group. Additionally, our results suggest that antibiotic resistance genes and bacterial virulence factors may influence the development of obesity. Finally, we demonstrated that gut vOTUs achieved a diagnostic accuracy with an optimal area under the curve of 0.766 for distinguishing obesity from healthy controls. Our findings offer comprehensive and generalizable insights into the gut bacteriome and virome features associated with obesity, with the potential to guide the development of microbiome-based diagnostics.https://doi.org/10.1186/s12866-024-03278-5ObesityGut microbiotaMetagenomicsMicrobiomeVirome
spellingShingle Xinliang Hu
Chong Yu
Yuting He
Songling Zhu
Shuang Wang
Ziqiong Xu
Shaohui You
Yanlei Jiao
Shu-Lin Liu
Hongxia Bao
Integrative metagenomic analysis reveals distinct gut microbial signatures related to obesity
BMC Microbiology
Obesity
Gut microbiota
Metagenomics
Microbiome
Virome
title Integrative metagenomic analysis reveals distinct gut microbial signatures related to obesity
title_full Integrative metagenomic analysis reveals distinct gut microbial signatures related to obesity
title_fullStr Integrative metagenomic analysis reveals distinct gut microbial signatures related to obesity
title_full_unstemmed Integrative metagenomic analysis reveals distinct gut microbial signatures related to obesity
title_short Integrative metagenomic analysis reveals distinct gut microbial signatures related to obesity
title_sort integrative metagenomic analysis reveals distinct gut microbial signatures related to obesity
topic Obesity
Gut microbiota
Metagenomics
Microbiome
Virome
url https://doi.org/10.1186/s12866-024-03278-5
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