Revealing the bacterial butyrate synthesis pathways by analyzing (meta)genomic data
- PMID: 24757212
- PMCID: PMC3994512
- DOI: 10.1128/mBio.00889-14
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 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.
Figures






Similar articles
-
Decrease in acetyl-CoA pathway utilizing butyrate-producing bacteria is a key pathogenic feature of alcohol-induced functional gut microbial dysbiosis and development of liver disease in mice.Gut Microbes. 2021 Jan-Dec;13(1):1946367. doi: 10.1080/19490976.2021.1946367. Gut Microbes. 2021. PMID: 34369304 Free PMC article.
-
Colonic Butyrate-Producing Communities in Humans: an Overview Using Omics Data.mSystems. 2017 Dec 5;2(6):e00130-17. doi: 10.1128/mSystems.00130-17. eCollection 2017 Nov-Dec. mSystems. 2017. PMID: 29238752 Free PMC article.
-
Cultivable butyrate-producing bacteria of elderly Japanese diagnosed with Alzheimer's disease.J Microbiol. 2018 Oct;56(10):760-771. doi: 10.1007/s12275-018-8297-7. Epub 2018 Aug 22. J Microbiol. 2018. PMID: 30136260
-
[Genes and gene clusters involved in microbial butyrate-producing pathway of human and animal gastrointestinal tract].Wei Sheng Wu Xue Bao. 2012 Oct 4;52(10):1181-6. Wei Sheng Wu Xue Bao. 2012. PMID: 23289315 Review. Chinese.
-
Therapeutic Potential of Butyrate for Treatment of Type 2 Diabetes.Front Endocrinol (Lausanne). 2021 Oct 19;12:761834. doi: 10.3389/fendo.2021.761834. eCollection 2021. Front Endocrinol (Lausanne). 2021. PMID: 34737725 Free PMC article. Review.
Cited by
-
Yeast β-Glucan Improves Insulin Sensitivity and Hepatic Lipid Metabolism in Mice Humanized with Obese Type 2 Diabetic Gut Microbiota.Mol Nutr Food Res. 2022 Nov;66(22):e2100819. doi: 10.1002/mnfr.202100819. Epub 2022 Oct 1. Mol Nutr Food Res. 2022. PMID: 36038526 Free PMC article.
-
Pediococcus pentosaceus MIANGUAN2 Alleviates Influenza Virus Infection by Modulating Gut Microbiota and Enhancing Short-Chain Fatty Acid Production.Nutrients. 2024 Jun 18;16(12):1923. doi: 10.3390/nu16121923. Nutrients. 2024. PMID: 38931277 Free PMC article.
-
Role of short-chain fatty acids in host physiology.Animal Model Exp Med. 2024 Oct;7(5):641-652. doi: 10.1002/ame2.12464. Epub 2024 Jun 28. Animal Model Exp Med. 2024. PMID: 38940192 Free PMC article. Review.
-
The Effect of Dietary Mushroom Agaricus bisporus on Intestinal Microbiota Composition and Host Immunological Function.Nutrients. 2018 Nov 9;10(11):1721. doi: 10.3390/nu10111721. Nutrients. 2018. PMID: 30424006 Free PMC article.
-
The human microbiota is associated with cardiometabolic risk across the epidemiologic transition.PLoS One. 2019 Jul 24;14(7):e0215262. doi: 10.1371/journal.pone.0215262. eCollection 2019. PLoS One. 2019. PMID: 31339887 Free PMC article.
References
-
- Paillard D, McKain N, Chaudhary LC, Walker ND, Pizette F, Koppova I, McEwan NR, Kopecný J, Vercoe PE, Louis P, Wallace RJ. 2007. Relation between phylogenetic position, lipid metabolism and butyrate production by different Butyrivibrio-like bacteria from the rumen. Antonie Van Leeuwenhoek 91:417–422. 10.1007/s10482-006-9121-7 - DOI - PubMed
Publication types
MeSH terms
Substances
Grants and funding
LinkOut - more resources
Full Text Sources
Other Literature Sources
Medical
Molecular Biology Databases
Miscellaneous