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 73 publications

(40 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

et al. 2021

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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

et al. 2021

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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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“…When the genomes of organisms are well annotated, transcriptomic analysis of interacting microbial pairs can be particularly useful to decipher functional interactions such as metabolite exchange. As an example, the investigation of the microbial interaction between Phascolarctobacterium faecium and the gut commensal Bacteroides thetaiotaomicron using RNA sequencing pointed to the exchange of several metabolites including succinate, vitamin B 12 , and glutamate ( Ikeyama et al, 2020 ). Altogether, omic methods contribute to a better understanding of the mechanisms at play between interacting species, as they allow to systematically measure all molecular phenotypes of a given type at once.…”

Section: Measuring the Functional Dimension Of Microbial Interactionsmentioning

confidence: 99%

Leveraging Experimental Strategies to Capture Different Dimensions of Microbial Interactions

2021

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Microorganisms are a fundamental part of virtually every ecosystem on earth. Understanding how collectively they interact, assemble, and function as communities has become a prevalent topic both in fundamental and applied research. Owing to multiple advances in technology, answering questions at the microbial system or network level is now within our grasp. To map and characterize microbial interaction networks, numerous computational approaches have been developed; however, experimentally validating microbial interactions is no trivial task. Microbial interactions are context-dependent, and their complex nature can result in an array of outcomes, not only in terms of fitness or growth, but also in other relevant functions and phenotypes. Thus, approaches to experimentally capture microbial interactions involve a combination of culture methods and phenotypic or functional characterization methods. Here, through our perspective of food microbiologists, we highlight the breadth of innovative and promising experimental strategies for their potential to capture the different dimensions of microbial interactions and their high-throughput application to answer the question; are microbial interaction patterns or network architecture similar along different contextual scales? We further discuss the experimental approaches used to build various types of networks and study their architecture in the context of cell biology and how they translate at the level of microbial ecosystem.

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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 73 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

Leveraging Experimental Strategies to Capture Different Dimensions of Microbial Interactions

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