Microbial interaction between the succinate‐utilizing bacterium <i>Phascolarctobacterium faecium</i> and the gut commensal <i>Bacteroides thetaiotaomicron</i>

Ikeyama, Nao; Murakami, Takumi; Toyoda, Atsushi; Mori, Hiroshi; Iino, Takao; Ohkuma, Moriya; Sakamoto, Mitsuo

doi:10.1002/mbo3.1111

Cited by 55 publications

(20 citation statements)

References 47 publications

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“…Based on the conserved synteny, phylogeny, and the involvement of all GAD-system genes in pH homeostasis mechanisms, it is conceivable that the entire gene set could be co-regulated; a notion illustrated by similar transcription pattern of all GAD-system genes throughout growth as retrieved from "Theta-Base" (Ryan et al, 2020), but also by another recent study with B. thetaiotaomicron DSM 2079 where gadB, glsA, gadC and the K + channel encoding gene were all downregulated when co-cultivated with Phascolarctobacterium faecium (Ikeyama et al, 2020). Among the 961 Bacteroides strains analyzed, all four genes of the GAD-system were conjointly present in 90% of all genomes, or 96% when considering human gut isolates only.…”

Section: Discussionmentioning

confidence: 97%

GABA Production by Human Intestinal Bacteroides spp.: Prevalence, Regulation, and Role in Acid Stress Tolerance

Otaru

Mujezinovic

et al. 2021

Front. Microbiol.

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The high neuroactive potential of metabolites produced by gut microbes has gained traction over the last few years, with metagenomic-based studies suggesting an important role of microbiota-derived γ-aminobutyric acid (GABA) in modulating mental health. Emerging evidence has revealed the presence of the glutamate decarboxylase (GAD)-encoding gene, a key enzyme to produce GABA, in the prominent human intestinal genus Bacteroides. Here, we investigated GABA production by Bacteroides in culture and metabolic assays combined with comparative genomics and phylogenetics. A total of 961 Bacteroides genomes were analyzed in silico and 17 metabolically and genetically diverse human intestinal isolates representing 11 species were screened in vitro. Using the model organism Bacteroides thetaiotaomicron DSM 2079, we determined GABA production kinetics, its impact on milieu pH, and we assessed its role in mitigating acid-induced cellular damage. We showed that the GAD-system consists of at least four highly conserved genes encoding a GAD, a glutaminase, a glutamate/GABA antiporter, and a potassium channel. We demonstrated a high prevalence of the GAD-system among Bacteroides with 90% of all Bacteroides genomes (96% in human gut isolates only) harboring all genes of the GAD-system and 16 intestinal Bacteroides strains producing GABA in vitro (ranging from 0.09 to 60.84 mM). We identified glutamate and glutamine as precursors of GABA production, showed that the production is regulated by pH, and that the GAD-system acts as a protective mechanism against acid stress in Bacteroides, mitigating cell death and preserving metabolic activity. Our data also indicate that the GAD-system might represent the only amino acid-dependent acid tolerance system in Bacteroides. Altogether, our results suggest an important contribution of Bacteroides in the regulation of the GABAergic system in the human gut.

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Section: Discussionmentioning

confidence: 97%

GABA Production by Human Intestinal Bacteroides spp.: Prevalence, Regulation, and Role in Acid Stress Tolerance

Otaru

Mujezinovic

et al. 2021

Front. Microbiol.

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“… 63–65 Other potential succinate consumers were identified in our study, including a known consumer, B. thetaiotaomicron. 66 The inverse relationship observed between time in Canada and abundance of D. succinatiphilus and B. thetaiotaomicron suggests a shift in succinate consumers.…”

Section: Discussionmentioning

confidence: 99%

The Impact of Migration on the Gut Metagenome of South Asian Canadians

et al. 2021

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South Asian (SA) Canadian immigrants have a higher risk of developing certain immune-mediated inflammatory diseases compared to non-migrant SAs. We sought to investigate the effect of migration on the gut metagenome and to identify microbiological associations between migration and conditions that may influence the development of immune-mediated inflammatory diseases. Metagenomic analysis of 58 first-generation (GEN1) SA immigrants and 38 unrelated Canadian born children-of-immigrants (GEN2) determined that the time lived in Canada was associated with continued changes in gut microbial communities. Migration of GEN1 to Canada early in life results in a gut community with similarities to GEN2 SA Canadians and non-SA North Americans. Conversely, GEN1 immigrants who arrived recently to Canada exhibited pronounced differences from GEN2, while displaying microbial similarities to a non-migrating SA cohort. Multivariate analysis identified that community composition was primarily influenced by high abundance taxa. Prevotella copri dominated in GEN1 and non-migrant SAs. Clostridia and functionally related Bacteroidia spp. replaced P. copri dominance over generations in Canada. Mutually exclusive Dialister species occurred at differing relative abundances over time and generations in Canada. This shift in species composition is accompanied by a change in genes associated with carbohydrate utilization and short-chain fatty acid production. Total energy derived from carbohydrates compared to protein consumption was significantly higher for GEN1 recent immigrants, which may influence the functional requirements of the gut community. This study demonstrates the associations between migration and the gut microbiome, which may be further associated with the altered risk of immune-mediated inflammatory diseases observed for SA Canadians.

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“…The levels of Phascolarctobacterium were lower in 26 patients with postpartum depressive disorder (PPD) compared to 16 health controls [ 40 ]. P. faecium uses succinate as substrate [ 41 ]. Succinate takes part in GABA synthesis and recycle [ 42 ].…”

Section: Discussionmentioning

confidence: 99%

Habitual Sleep Duration and the Colonic Mucosa-Associated Gut Microbiota in Humans—A Pilot Study

et al. 2021

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We examined the association between the colonic adherent microbiota and nocturnal sleep duration in humans. In a cross-sectional study, 63 polyp-free adults underwent a colonoscopy and donated 206 mucosal biopsies. The gut microbiota was profiled using the 16S rRNA gene sequencing targeting the V4 region. The sequence reads were processed using UPARSE and DADA2, respectively. Lifestyle factors, including sleep habits, were obtained using an interviewer-administered questionnaire. We categorized the participants into short sleepers (<6 h per night; n = 16) and normal sleepers (6–8 h per night; n = 47) based on self-reported data. Differences in bacterial biodiversity and the taxonomic relative abundance were compared between short vs. normal sleepers, followed by multivariable analysis. A false discovery rate-adjusted p value (q value) < 0.05 indicated statistical significance. The bacterial community composition differed in short and normal sleepers. The relative abundance of Sutterella was significantly lower (0.38% vs. 1.25%) and that of Pseudomonas was significantly higher (0.14% vs. 0.08%) in short sleepers than in normal sleepers (q values < 0.01). The difference was confirmed in the multivariable analysis. Nocturnal sleep duration was associated with the bacterial community composition and structure in the colonic gut microbiota in adults.

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Microbial interaction between the succinate‐utilizing bacterium Phascolarctobacterium faecium and the gut commensal Bacteroides thetaiotaomicron

Abstract: This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

Cited by 55 publications

References 47 publications

GABA Production by Human Intestinal Bacteroides spp.: Prevalence, Regulation, and Role in Acid Stress Tolerance

GABA Production by Human Intestinal Bacteroides spp.: Prevalence, Regulation, and Role in Acid Stress Tolerance

The Impact of Migration on the Gut Metagenome of South Asian Canadians

Habitual Sleep Duration and the Colonic Mucosa-Associated Gut Microbiota in Humans—A Pilot Study

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