Colonic Butyrate-Producing Communities in Humans: an Overview Using Omics Data

ABSTRACT Given the key role of butyrate for host health, understanding the ecology of intestinal butyrate-producing communities is a top priority for gut microbiota research. To this end, we performed a pooled analysis on 2,387 metagenomic/transcriptomic samples from 15 publicly available data sets...

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Autores principales:	Marius Vital, André Karch, Dietmar H. Pieper
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2017
Materias:	butyrate cardiometabolic disease ecology functional stability gut microbiota Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/f50940553e43478ca74f349f11ae2972
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spelling	oai:doaj.org-article:f50940553e43478ca74f349f11ae29722021-12-02T19:45:29ZColonic Butyrate-Producing Communities in Humans: an Overview Using Omics Data10.1128/mSystems.00130-172379-5077https://doaj.org/article/f50940553e43478ca74f349f11ae29722017-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00130-17https://doaj.org/toc/2379-5077ABSTRACT Given the key role of butyrate for host health, understanding the ecology of intestinal butyrate-producing communities is a top priority for gut microbiota research. To this end, we performed a pooled analysis on 2,387 metagenomic/transcriptomic samples from 15 publicly available data sets that originated from three continents and encompassed eight diseases as well as specific interventions. For analyses, a gene catalogue was constructed from gene-targeted assemblies of all genes from butyrate synthesis pathways of all samples and from an updated reference database derived from genome screenings. We demonstrate that butyrate producers establish themselves within the first year of life and display high abundances (>20% of total bacterial community) in adults regardless of origin. Various bacteria form this functional group, exhibiting a biochemical diversity including different pathways and terminal enzymes, where one carbohydrate-fueled pathway was dominant with butyryl coenzyme A (CoA):acetate CoA transferase as the main terminal enzyme. Subjects displayed a high richness of butyrate producers, and 17 taxa, primarily members of the Lachnospiraceae and Ruminococcaceae along with some Bacteroidetes, were detected in >70% of individuals, encompassing ~85% of the total butyrate-producing potential. Most of these key taxa were also found to express genes for butyrate formation, indicating that butyrate producers occupy various niches in the gut ecosystem, concurrently synthesizing that compound. Furthermore, results from longitudinal analyses propose that diversity supports functional stability during ordinary life disturbances and during interventions such as antibiotic treatment. A reduction of the butyrate-producing potential along with community alterations was detected in various diseases, where patients suffering from cardiometabolic disorders were particularly affected. IMPORTANCE Studies focusing on taxonomic compositions of the gut microbiota are plentiful, whereas its functional capabilities are still poorly understood. Specific key functions deserve detailed investigations, as they regulate microbiota-host interactions and promote host health and disease. The production of butyrate is among the top targets since depletion of this microbe-derived metabolite is linked to several emerging noncommunicable diseases and was shown to facilitate establishment of enteric pathogens by disrupting colonization resistance. In this study, we established a workflow to investigate in detail the composition of the polyphyletic butyrate-producing community from omics data extracting its biochemical and taxonomic diversity. By combining information from various publicly available data sets, we identified universal ecological key features of this functional group and shed light on its role in health and disease. Our results will assist the development of precision medicine to combat functional dysbiosis.Marius VitalAndré KarchDietmar H. PieperAmerican Society for Microbiologyarticlebutyratecardiometabolic diseaseecologyfunctional stabilitygut microbiotaMicrobiologyQR1-502ENmSystems, Vol 2, Iss 6 (2017)
institution	DOAJ
collection	DOAJ
language	EN
topic	butyrate cardiometabolic disease ecology functional stability gut microbiota Microbiology QR1-502
spellingShingle	butyrate cardiometabolic disease ecology functional stability gut microbiota Microbiology QR1-502 Marius Vital André Karch Dietmar H. Pieper Colonic Butyrate-Producing Communities in Humans: an Overview Using Omics Data
description	ABSTRACT Given the key role of butyrate for host health, understanding the ecology of intestinal butyrate-producing communities is a top priority for gut microbiota research. To this end, we performed a pooled analysis on 2,387 metagenomic/transcriptomic samples from 15 publicly available data sets that originated from three continents and encompassed eight diseases as well as specific interventions. For analyses, a gene catalogue was constructed from gene-targeted assemblies of all genes from butyrate synthesis pathways of all samples and from an updated reference database derived from genome screenings. We demonstrate that butyrate producers establish themselves within the first year of life and display high abundances (>20% of total bacterial community) in adults regardless of origin. Various bacteria form this functional group, exhibiting a biochemical diversity including different pathways and terminal enzymes, where one carbohydrate-fueled pathway was dominant with butyryl coenzyme A (CoA):acetate CoA transferase as the main terminal enzyme. Subjects displayed a high richness of butyrate producers, and 17 taxa, primarily members of the Lachnospiraceae and Ruminococcaceae along with some Bacteroidetes, were detected in >70% of individuals, encompassing ~85% of the total butyrate-producing potential. Most of these key taxa were also found to express genes for butyrate formation, indicating that butyrate producers occupy various niches in the gut ecosystem, concurrently synthesizing that compound. Furthermore, results from longitudinal analyses propose that diversity supports functional stability during ordinary life disturbances and during interventions such as antibiotic treatment. A reduction of the butyrate-producing potential along with community alterations was detected in various diseases, where patients suffering from cardiometabolic disorders were particularly affected. IMPORTANCE Studies focusing on taxonomic compositions of the gut microbiota are plentiful, whereas its functional capabilities are still poorly understood. Specific key functions deserve detailed investigations, as they regulate microbiota-host interactions and promote host health and disease. The production of butyrate is among the top targets since depletion of this microbe-derived metabolite is linked to several emerging noncommunicable diseases and was shown to facilitate establishment of enteric pathogens by disrupting colonization resistance. In this study, we established a workflow to investigate in detail the composition of the polyphyletic butyrate-producing community from omics data extracting its biochemical and taxonomic diversity. By combining information from various publicly available data sets, we identified universal ecological key features of this functional group and shed light on its role in health and disease. Our results will assist the development of precision medicine to combat functional dysbiosis.
format	article
author	Marius Vital André Karch Dietmar H. Pieper
author_facet	Marius Vital André Karch Dietmar H. Pieper
author_sort	Marius Vital
title	Colonic Butyrate-Producing Communities in Humans: an Overview Using Omics Data
title_short	Colonic Butyrate-Producing Communities in Humans: an Overview Using Omics Data
title_full	Colonic Butyrate-Producing Communities in Humans: an Overview Using Omics Data
title_fullStr	Colonic Butyrate-Producing Communities in Humans: an Overview Using Omics Data
title_full_unstemmed	Colonic Butyrate-Producing Communities in Humans: an Overview Using Omics Data
title_sort	colonic butyrate-producing communities in humans: an overview using omics data
publisher	American Society for Microbiology
publishDate	2017
url	https://doaj.org/article/f50940553e43478ca74f349f11ae2972
work_keys_str_mv	AT mariusvital colonicbutyrateproducingcommunitiesinhumansanoverviewusingomicsdata AT andrekarch colonicbutyrateproducingcommunitiesinhumansanoverviewusingomicsdata AT dietmarhpieper colonicbutyrateproducingcommunitiesinhumansanoverviewusingomicsdata
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Colonic Butyrate-Producing Communities in Humans: an Overview Using Omics Data

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