Body Mass Index and Sex Affect Diverse Microbial Niches within the Gut

Gut microbiota is considered a separate organ with endocrine capabilities, actively contributing to tissue homeostasis. It consists of at least two separate microbial populations, the lumen-associated (LAM) and the mucosa-associated microbiota (MAM). In the present study, we compared LAM and MAM, by...

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Main Authors: Francesca Borgo, Stefania Garbossa, Alessandra Riva, Marco Severgnini, Carmelo Luigiano, Albero Benetti, Antonio E. Pontiroli, Giulia Morace, Elisa Borghi
Format: Article
Language:English
Published: Frontiers Media S.A. 2018-02-01
Series:Frontiers in Microbiology
Subjects:
sex
Online Access:http://journal.frontiersin.org/article/10.3389/fmicb.2018.00213/full
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spelling doaj-6e4ad5d98ddd46119af61c669c6b1f502020-11-24T23:56:55ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2018-02-01910.3389/fmicb.2018.00213334465Body Mass Index and Sex Affect Diverse Microbial Niches within the GutFrancesca Borgo0Stefania Garbossa1Alessandra Riva2Alessandra Riva3Marco Severgnini4Carmelo Luigiano5Albero Benetti6Antonio E. Pontiroli7Antonio E. Pontiroli8Giulia Morace9Elisa Borghi10Department of Health Sciences, Università degli Studi di Milano, Milan, ItalyASST Santi Paolo e Carlo Hospital, Milan, ItalyDepartment of Health Sciences, Università degli Studi di Milano, Milan, ItalyDivision of Microbial Ecology, Department of Microbiology and Ecosystem Science, Research Network “Chemistry meets Microbiology”, University of Vienna, Vienna, AustriaInstitute of Biomedical Technologies, National Research Council, Segrate, ItalyASST Santi Paolo e Carlo Hospital, Milan, ItalyASST Santi Paolo e Carlo Hospital, Milan, ItalyDepartment of Health Sciences, Università degli Studi di Milano, Milan, ItalyASST Santi Paolo e Carlo Hospital, Milan, ItalyDepartment of Health Sciences, Università degli Studi di Milano, Milan, ItalyDepartment of Health Sciences, Università degli Studi di Milano, Milan, ItalyGut microbiota is considered a separate organ with endocrine capabilities, actively contributing to tissue homeostasis. It consists of at least two separate microbial populations, the lumen-associated (LAM) and the mucosa-associated microbiota (MAM). In the present study, we compared LAM and MAM, by collecting stools and sigmoid brush samples of forty adults without large-bowel symptoms, and through a 16S rRNA gene next-generation sequencing (NGS) approach. MAM sample analysis revealed enrichment in aerotolerant Proteobacteria, probably selected by a gradient of oxygen that decreases from tissue to lumen, and in Streptococcus and Clostridium spp., highly fermenting bacteria. On the other hand, LAM microbiota showed an increased abundance in Bacteroides, Prevotella, and Oscillospira, genera able to digest and to degrade biopolymers in the large intestine. Predicted metagenomic analysis showed LAM to be enriched in genes encoding enzymes mostly involved in energy extraction from carbohydrates and lipids, whereas MAM in amino acid and vitamin metabolism. Moreover, LAM and MAM communities seemed to be influenced by different host factors, such as diet and sex. LAM is affected by body mass index (BMI) status. Indeed, BMI negatively correlates with Faecalibacterium prausnitzii and Flavonifractor plautii abundance, putative biomarkers of healthy status. In contrast, MAM microbial population showed a significant grouping according to sex. Female MAM was enriched in Actinobacteria (with an increased trend of the genus Bifidobacterium), and a significant depletion in Veillonellaceae. Interestingly, we found the species Gemmiger formicilis to be associated with male and Bifidobacterium adolescentis, with female MAM samples. In conclusion, our results suggest that gut harbors microbial niches that differ in both composition and host factor susceptibility, and their richness and diversity may be overlooked evaluating only fecal samples.http://journal.frontiersin.org/article/10.3389/fmicb.2018.00213/fullluminal microbiotamucosa-associated microbiotabody mass indexsexindicative species
collection DOAJ
language English
format Article
sources DOAJ
author Francesca Borgo
Stefania Garbossa
Alessandra Riva
Alessandra Riva
Marco Severgnini
Carmelo Luigiano
Albero Benetti
Antonio E. Pontiroli
Antonio E. Pontiroli
Giulia Morace
Elisa Borghi
spellingShingle Francesca Borgo
Stefania Garbossa
Alessandra Riva
Alessandra Riva
Marco Severgnini
Carmelo Luigiano
Albero Benetti
Antonio E. Pontiroli
Antonio E. Pontiroli
Giulia Morace
Elisa Borghi
Body Mass Index and Sex Affect Diverse Microbial Niches within the Gut
Frontiers in Microbiology
luminal microbiota
mucosa-associated microbiota
body mass index
sex
indicative species
author_facet Francesca Borgo
Stefania Garbossa
Alessandra Riva
Alessandra Riva
Marco Severgnini
Carmelo Luigiano
Albero Benetti
Antonio E. Pontiroli
Antonio E. Pontiroli
Giulia Morace
Elisa Borghi
author_sort Francesca Borgo
title Body Mass Index and Sex Affect Diverse Microbial Niches within the Gut
title_short Body Mass Index and Sex Affect Diverse Microbial Niches within the Gut
title_full Body Mass Index and Sex Affect Diverse Microbial Niches within the Gut
title_fullStr Body Mass Index and Sex Affect Diverse Microbial Niches within the Gut
title_full_unstemmed Body Mass Index and Sex Affect Diverse Microbial Niches within the Gut
title_sort body mass index and sex affect diverse microbial niches within the gut
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2018-02-01
description Gut microbiota is considered a separate organ with endocrine capabilities, actively contributing to tissue homeostasis. It consists of at least two separate microbial populations, the lumen-associated (LAM) and the mucosa-associated microbiota (MAM). In the present study, we compared LAM and MAM, by collecting stools and sigmoid brush samples of forty adults without large-bowel symptoms, and through a 16S rRNA gene next-generation sequencing (NGS) approach. MAM sample analysis revealed enrichment in aerotolerant Proteobacteria, probably selected by a gradient of oxygen that decreases from tissue to lumen, and in Streptococcus and Clostridium spp., highly fermenting bacteria. On the other hand, LAM microbiota showed an increased abundance in Bacteroides, Prevotella, and Oscillospira, genera able to digest and to degrade biopolymers in the large intestine. Predicted metagenomic analysis showed LAM to be enriched in genes encoding enzymes mostly involved in energy extraction from carbohydrates and lipids, whereas MAM in amino acid and vitamin metabolism. Moreover, LAM and MAM communities seemed to be influenced by different host factors, such as diet and sex. LAM is affected by body mass index (BMI) status. Indeed, BMI negatively correlates with Faecalibacterium prausnitzii and Flavonifractor plautii abundance, putative biomarkers of healthy status. In contrast, MAM microbial population showed a significant grouping according to sex. Female MAM was enriched in Actinobacteria (with an increased trend of the genus Bifidobacterium), and a significant depletion in Veillonellaceae. Interestingly, we found the species Gemmiger formicilis to be associated with male and Bifidobacterium adolescentis, with female MAM samples. In conclusion, our results suggest that gut harbors microbial niches that differ in both composition and host factor susceptibility, and their richness and diversity may be overlooked evaluating only fecal samples.
topic luminal microbiota
mucosa-associated microbiota
body mass index
sex
indicative species
url http://journal.frontiersin.org/article/10.3389/fmicb.2018.00213/full
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