Revealing the Bacterial Butyrate Synthesis Pathways by Analyzing (Meta)genomic Data

ABSTRACT Butyrate-producing bacteria have recently gained attention, since they are important for a healthy colon and when altered contribute to emerging diseases, such as ulcerative colitis and type II diabetes. This guild is polyphyletic and cannot be accurately detected by 16S rRNA gene sequencin...

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Autores principales:	Marius Vital, Adina Chuang Howe, James M. Tiedje
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2014
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/ae2f35fd9bbf4e04a302c3944af5d418
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spelling	oai:doaj.org-article:ae2f35fd9bbf4e04a302c3944af5d4182021-11-15T15:45:13ZRevealing the Bacterial Butyrate Synthesis Pathways by Analyzing (Meta)genomic Data10.1128/mBio.00889-142150-7511https://doaj.org/article/ae2f35fd9bbf4e04a302c3944af5d4182014-05-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00889-14https://doaj.org/toc/2150-7511ABSTRACT Butyrate-producing bacteria have recently gained attention, since they are important for a healthy colon and when altered contribute to emerging diseases, such as ulcerative colitis and type II diabetes. This guild is polyphyletic and cannot be accurately detected by 16S rRNA gene sequencing. Consequently, approaches targeting the terminal genes of the main butyrate-producing pathway have been developed. However, since additional pathways exist and alternative, newly recognized enzymes catalyzing the terminal reaction have been described, previous investigations are often incomplete. We undertook a broad analysis of butyrate-producing pathways and individual genes by screening 3,184 sequenced bacterial genomes from the Integrated Microbial Genome database. Genomes of 225 bacteria with a potential to produce butyrate were identified, including many previously unknown candidates. The majority of candidates belong to distinct families within the Firmicutes, but members of nine other phyla, especially from Actinobacteria, Bacteroidetes, Fusobacteria, Proteobacteria, Spirochaetes, and Thermotogae, were also identified as potential butyrate producers. The established gene catalogue (3,055 entries) was used to screen for butyrate synthesis pathways in 15 metagenomes derived from stool samples of healthy individuals provided by the HMP (Human Microbiome Project) consortium. A high percentage of total genomes exhibited a butyrate-producing pathway (mean, 19.1%; range, 3.2% to 39.4%), where the acetyl-coenzyme A (CoA) pathway was the most prevalent (mean, 79.7% of all pathways), followed by the lysine pathway (mean, 11.2%). Diversity analysis for the acetyl-CoA pathway showed that the same few firmicute groups associated with several Lachnospiraceae and Ruminococcaceae were dominating in most individuals, whereas the other pathways were associated primarily with Bacteroidetes. IMPORTANCE Microbiome research has revealed new, important roles of our gut microbiota for maintaining health, but an understanding of effects of specific microbial functions on the host is in its infancy, partly because in-depth functional microbial analyses are rare and publicly available databases are often incomplete/misannotated. In this study, we focused on production of butyrate, the main energy source for colonocytes, which plays a critical role in health and disease. We have provided a complete database of genes from major known butyrate-producing pathways, using in-depth genomic analysis of publicly available genomes, filling an important gap to accurately assess the butyrate-producing potential of complex microbial communities from “-omics”-derived data. Furthermore, a reference data set containing the abundance and diversity of butyrate synthesis pathways from the healthy gut microbiota was established through a metagenomics-based assessment. This study will help in understanding the role of butyrate producers in health and disease and may assist the development of treatments for functional dysbiosis.Marius VitalAdina Chuang HoweJames M. TiedjeAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 5, Iss 2 (2014)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Marius Vital Adina Chuang Howe James M. Tiedje Revealing the Bacterial Butyrate Synthesis Pathways by Analyzing (Meta)genomic Data
description	ABSTRACT Butyrate-producing bacteria have recently gained attention, since they are important for a healthy colon and when altered contribute to emerging diseases, such as ulcerative colitis and type II diabetes. This guild is polyphyletic and cannot be accurately detected by 16S rRNA gene sequencing. Consequently, approaches targeting the terminal genes of the main butyrate-producing pathway have been developed. However, since additional pathways exist and alternative, newly recognized enzymes catalyzing the terminal reaction have been described, previous investigations are often incomplete. We undertook a broad analysis of butyrate-producing pathways and individual genes by screening 3,184 sequenced bacterial genomes from the Integrated Microbial Genome database. Genomes of 225 bacteria with a potential to produce butyrate were identified, including many previously unknown candidates. The majority of candidates belong to distinct families within the Firmicutes, but members of nine other phyla, especially from Actinobacteria, Bacteroidetes, Fusobacteria, Proteobacteria, Spirochaetes, and Thermotogae, were also identified as potential butyrate producers. The established gene catalogue (3,055 entries) was used to screen for butyrate synthesis pathways in 15 metagenomes derived from stool samples of healthy individuals provided by the HMP (Human Microbiome Project) consortium. A high percentage of total genomes exhibited a butyrate-producing pathway (mean, 19.1%; range, 3.2% to 39.4%), where the acetyl-coenzyme A (CoA) pathway was the most prevalent (mean, 79.7% of all pathways), followed by the lysine pathway (mean, 11.2%). Diversity analysis for the acetyl-CoA pathway showed that the same few firmicute groups associated with several Lachnospiraceae and Ruminococcaceae were dominating in most individuals, whereas the other pathways were associated primarily with Bacteroidetes. IMPORTANCE Microbiome research has revealed new, important roles of our gut microbiota for maintaining health, but an understanding of effects of specific microbial functions on the host is in its infancy, partly because in-depth functional microbial analyses are rare and publicly available databases are often incomplete/misannotated. In this study, we focused on production of butyrate, the main energy source for colonocytes, which plays a critical role in health and disease. We have provided a complete database of genes from major known butyrate-producing pathways, using in-depth genomic analysis of publicly available genomes, filling an important gap to accurately assess the butyrate-producing potential of complex microbial communities from “-omics”-derived data. Furthermore, a reference data set containing the abundance and diversity of butyrate synthesis pathways from the healthy gut microbiota was established through a metagenomics-based assessment. This study will help in understanding the role of butyrate producers in health and disease and may assist the development of treatments for functional dysbiosis.
format	article
author	Marius Vital Adina Chuang Howe James M. Tiedje
author_facet	Marius Vital Adina Chuang Howe James M. Tiedje
author_sort	Marius Vital
title	Revealing the Bacterial Butyrate Synthesis Pathways by Analyzing (Meta)genomic Data
title_short	Revealing the Bacterial Butyrate Synthesis Pathways by Analyzing (Meta)genomic Data
title_full	Revealing the Bacterial Butyrate Synthesis Pathways by Analyzing (Meta)genomic Data
title_fullStr	Revealing the Bacterial Butyrate Synthesis Pathways by Analyzing (Meta)genomic Data
title_full_unstemmed	Revealing the Bacterial Butyrate Synthesis Pathways by Analyzing (Meta)genomic Data
title_sort	revealing the bacterial butyrate synthesis pathways by analyzing (meta)genomic data
publisher	American Society for Microbiology
publishDate	2014
url	https://doaj.org/article/ae2f35fd9bbf4e04a302c3944af5d418
work_keys_str_mv	AT mariusvital revealingthebacterialbutyratesynthesispathwaysbyanalyzingmetagenomicdata AT adinachuanghowe revealingthebacterialbutyratesynthesispathwaysbyanalyzingmetagenomicdata AT jamesmtiedje revealingthebacterialbutyratesynthesispathwaysbyanalyzingmetagenomicdata
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Revealing the Bacterial Butyrate Synthesis Pathways by Analyzing (Meta)genomic Data

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