Butyrate producers, “The Sentinel of Gut”: Their intestinal significance with and beyond butyrate, and prospective use as microbial therapeutics

Gut-microbial butyrate is a short-chain fatty acid (SCFA) of significant physiological importance than the other major SCFAs (acetate and propionate). Most butyrate producers belong to the Clostridium cluster of the phylum Firmicutes, such as Faecalibacterium, Roseburia, Eubacterium, Anaerostipes, C...

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Main Authors: Vineet Singh, GyuDae Lee, HyunWoo Son, Hong Koh, Eun Soo Kim, Tatsuya Unno, Jae-Ho Shin
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-01-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2022.1103836/full
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author Vineet Singh
GyuDae Lee
HyunWoo Son
Hong Koh
Eun Soo Kim
Tatsuya Unno
Jae-Ho Shin
Jae-Ho Shin
author_facet Vineet Singh
GyuDae Lee
HyunWoo Son
Hong Koh
Eun Soo Kim
Tatsuya Unno
Jae-Ho Shin
Jae-Ho Shin
author_sort Vineet Singh
collection DOAJ
description Gut-microbial butyrate is a short-chain fatty acid (SCFA) of significant physiological importance than the other major SCFAs (acetate and propionate). Most butyrate producers belong to the Clostridium cluster of the phylum Firmicutes, such as Faecalibacterium, Roseburia, Eubacterium, Anaerostipes, Coprococcus, Subdoligranulum, and Anaerobutyricum. They metabolize carbohydrates via the butyryl-CoA: acetate CoA-transferase pathway and butyrate kinase terminal enzymes to produce most of butyrate. Although, in minor fractions, amino acids can also be utilized to generate butyrate via glutamate and lysine pathways. Butyrogenic microbes play a vital role in various gut-associated metabolisms. Butyrate is used by colonocytes to generate energy, stabilizes hypoxia-inducible factor to maintain the anaerobic environment in the gut, maintains gut barrier integrity by regulating Claudin-1 and synaptopodin expression, limits pro-inflammatory cytokines (IL-6, IL-12), and inhibits oncogenic pathways (Akt/ERK, Wnt, and TGF-β signaling). Colonic butyrate producers shape the gut microbial community by secreting various anti-microbial substances, such as cathelicidins, reuterin, and β-defensin-1, and maintain gut homeostasis by releasing anti-inflammatory molecules, such as IgA, vitamin B, and microbial anti-inflammatory molecules. Additionally, butyrate producers, such as Roseburia, produce anti-carcinogenic metabolites, such as shikimic acid and a precursor of conjugated linoleic acid. In this review, we summarized the significance of butyrate, critically examined the role and relevance of butyrate producers, and contextualized their importance as microbial therapeutics.
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spelling doaj.art-b20243efe723446ea74cb36279c26edf2023-01-12T05:07:35ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-01-011310.3389/fmicb.2022.11038361103836Butyrate producers, “The Sentinel of Gut”: Their intestinal significance with and beyond butyrate, and prospective use as microbial therapeuticsVineet Singh0GyuDae Lee1HyunWoo Son2Hong Koh3Eun Soo Kim4Tatsuya Unno5Jae-Ho Shin6Jae-Ho Shin7Department of Applied Biosciences, Kyungpook National University, Daegu, Republic of KoreaDepartment of Applied Biosciences, Kyungpook National University, Daegu, Republic of KoreaDepartment of Applied Biosciences, Kyungpook National University, Daegu, Republic of KoreaDepartment of Pediatrics, Severance Fecal Microbiota Transplantation Center, Severance Hospital, Yonsei University College of Medicine, Seoul, Republic of KoreaDepartment of Internal Medicine, School of Medicine, Kyungpook National University, Daegu, Republic of KoreaFaculty of Biotechnology, School of Life Sciences, SARI, Jeju National University, Jeju, Republic of KoreaDepartment of Applied Biosciences, Kyungpook National University, Daegu, Republic of KoreaDepartment of Integrative Biotechnology, Kyungpook National University, Daegu, Republic of KoreaGut-microbial butyrate is a short-chain fatty acid (SCFA) of significant physiological importance than the other major SCFAs (acetate and propionate). Most butyrate producers belong to the Clostridium cluster of the phylum Firmicutes, such as Faecalibacterium, Roseburia, Eubacterium, Anaerostipes, Coprococcus, Subdoligranulum, and Anaerobutyricum. They metabolize carbohydrates via the butyryl-CoA: acetate CoA-transferase pathway and butyrate kinase terminal enzymes to produce most of butyrate. Although, in minor fractions, amino acids can also be utilized to generate butyrate via glutamate and lysine pathways. Butyrogenic microbes play a vital role in various gut-associated metabolisms. Butyrate is used by colonocytes to generate energy, stabilizes hypoxia-inducible factor to maintain the anaerobic environment in the gut, maintains gut barrier integrity by regulating Claudin-1 and synaptopodin expression, limits pro-inflammatory cytokines (IL-6, IL-12), and inhibits oncogenic pathways (Akt/ERK, Wnt, and TGF-β signaling). Colonic butyrate producers shape the gut microbial community by secreting various anti-microbial substances, such as cathelicidins, reuterin, and β-defensin-1, and maintain gut homeostasis by releasing anti-inflammatory molecules, such as IgA, vitamin B, and microbial anti-inflammatory molecules. Additionally, butyrate producers, such as Roseburia, produce anti-carcinogenic metabolites, such as shikimic acid and a precursor of conjugated linoleic acid. In this review, we summarized the significance of butyrate, critically examined the role and relevance of butyrate producers, and contextualized their importance as microbial therapeutics.https://www.frontiersin.org/articles/10.3389/fmicb.2022.1103836/fullbutyrate producersmicrobial homeostasisgut epithelial barrierimmunomodulationgut inflammationcolorectal cancer
spellingShingle Vineet Singh
GyuDae Lee
HyunWoo Son
Hong Koh
Eun Soo Kim
Tatsuya Unno
Jae-Ho Shin
Jae-Ho Shin
Butyrate producers, “The Sentinel of Gut”: Their intestinal significance with and beyond butyrate, and prospective use as microbial therapeutics
Frontiers in Microbiology
butyrate producers
microbial homeostasis
gut epithelial barrier
immunomodulation
gut inflammation
colorectal cancer
title Butyrate producers, “The Sentinel of Gut”: Their intestinal significance with and beyond butyrate, and prospective use as microbial therapeutics
title_full Butyrate producers, “The Sentinel of Gut”: Their intestinal significance with and beyond butyrate, and prospective use as microbial therapeutics
title_fullStr Butyrate producers, “The Sentinel of Gut”: Their intestinal significance with and beyond butyrate, and prospective use as microbial therapeutics
title_full_unstemmed Butyrate producers, “The Sentinel of Gut”: Their intestinal significance with and beyond butyrate, and prospective use as microbial therapeutics
title_short Butyrate producers, “The Sentinel of Gut”: Their intestinal significance with and beyond butyrate, and prospective use as microbial therapeutics
title_sort butyrate producers the sentinel of gut their intestinal significance with and beyond butyrate and prospective use as microbial therapeutics
topic butyrate producers
microbial homeostasis
gut epithelial barrier
immunomodulation
gut inflammation
colorectal cancer
url https://www.frontiersin.org/articles/10.3389/fmicb.2022.1103836/full
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