Dataset Information

Mobilization of vitamin B₁₂ transporters alters competitive dynamics in a human gut microbe.

ABSTRACT: The functional and genomic diversity of the human gut microbiome is shaped by horizontal transfer of mobile genetic elements (MGEs). Characterized MGEs can encode genes beneficial for their host's self-defense (e.g., antibiotic resistance) or ability to compete for essential or limited resources (e.g., vitamins). Vitamin B₁₂ and related compounds (corrinoids) are critical nutrients that enable colonization by members of the common gut microbe phylum, the Bacteroidetes. Herein, we identify a distinct class of MGEs in the Bacteroidetes responsible for the mobilization and exchange of the genes required for transport of corrinoids, a group of cyclic tetrapyrrole cofactors including vitamin B₁₂ (btuGBFCD). This class includes two distinct groups of conjugative transposons (CTns) and one group of phage. Conjugative transfer and vitamin B₁₂ transport activity of two of the CTns were confirmed in vitro and in vivo, demonstrating the important role MGEs play in distribution of corrinoid transporters in the Bacteroidetes.

SUBMITTER: Frye KA

PROVIDER: S-EPMC8759732 | biostudies-literature | 2021 Dec

REPOSITORIES: biostudies-literature

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Mobilization of vitamin B<sub>12</sub> transporters alters competitive dynamics in a human gut microbe.

Frye Katie A KA Piamthai Varadh V Hsiao Ansel A Degnan Patrick H PH

Cell reports 20211201 13

The functional and genomic diversity of the human gut microbiome is shaped by horizontal transfer of mobile genetic elements (MGEs). Characterized MGEs can encode genes beneficial for their host's self-defense (e.g., antibiotic resistance) or ability to compete for essential or limited resources (e.g., vitamins). Vitamin B<sub>12</sub> and related compounds (corrinoids) are critical nutrients that enable colonization by members of the common gut microbe phylum, the Bacteroidetes. Herein, we iden ...[more]

PMID: 34965410

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Project description:Nematode predation plays an essential role in determining changes in the rhizosphere microbiome. These changes affect the local nutrient balance and cycling of essential nutrients by selectively structuring interactions across functional taxa in the system. Currently, it is largely unknown to what extent nematode predation induces shifts in the microbiome associated with different rates of soil phosphorous (P) mineralization. Here, we performed an 7-year field experiment to investigate the importance of nematode predation influencing P availability and cycling. These were tracked via the changes in the alkaline phosphomonoesterase (ALP)-producing bacterial community and ALP activity in the rhizosphere of rapeseed. Here, we found that the nematode addition led to high predation pressure and thereby caused shifts in the abundance and composition of the ALP-producing bacterial community. Further analyses based on cooccurrence networks and metabolomics consistently showed that nematode addition induced competitive interactions between potentially keystone ALP-producing bacteria and other members within the community. Structural equation modeling revealed that the outcome of this competition induced by stronger predation pressure of nematodes was significantly associated with higher diversity of ALP-producing bacteria, thereby enhancing ALP activity and P availability. Taken together, our results provide evidence for the importance of predator-prey and competitive interactions in soil biology and their direct influences on nutrient cycling dynamics. IMPORTANCE Nematode predation plays an essential role in determining the rhizosphere microbiome. In doing so, predation dynamically affects the soil nutrient cycling, for instance, by shifting the availability of phosphorus (P) for plant uptake. However, the role of nematode predation inducing selective changes in the microbiome and affecting rates of P mineralization remains still largely unknown. Here, we used a field site treated with different fertilizers to investigate the importance of nematode predation influencing P availability and plant productivity, via changes in bacterial taxa producing alkaline phosphomonoesterases (ALP) and ALP activity in the rhizosphere of rapeseed. We integrated field and laboratory experiments to show that nematode predation induces bacterial keystone taxa to compete with the connected members and results in the modulation of ALP-producing bacterial populations and ALP activity in the rhizosphere. Taken together, our study provides novel insights into microbially mediated mechanisms of competitive interaction induced by nematode predation in enhancing P availability in the plant rhizosphere.

Project description:BackgroundVitamin B12 supplements typically contain doses that far exceed the recommended daily amount, and high exposures are generally considered safe. Competitive and syntrophic interactions for B12 exist between microbes in the gut. Yet, to what extent excessive levels contribute to the activities of the gut microbiota remains unclear. The objective of this study was to evaluate the effect of B12 on microbial ecology using a B12 supplemented mouse model with Citrobacter rodentium, a mouse-specific pathogen. Mice were fed a standard chow diet and received either water or water supplemented with B12 (cyanocobalamin: ~120 μg/day), which equates to approximately 25 mg in humans. Infection severity was determined by body weight, pathogen load, and histopathologic scoring. Host biomarkers of inflammation were assessed in the colon before and after the pathogen challenge.ResultsCyanocobalamin supplementation enhanced pathogen colonization at day 1 (P < 0.05) and day 3 (P < 0.01) postinfection. The impact of B12 on gut microbial communities, although minor, was distinct and attributed to the changes in the Lachnospiraceae populations and reduced alpha diversity. Cyanocobalamin treatment disrupted the activity of the low-abundance community members of the gut microbiota. It enhanced the amount of interleukin-12 p40 subunit protein (IL12/23p40; P < 0.001) and interleukin-17a (IL-17A; P < 0.05) in the colon of naïve mice. This immune phenotype was microbe dependent, and the response varied based on the baseline microbiota. The cecal metatranscriptome revealed that excessive cyanocobalamin decreased the expression of glucose utilizing genes by C. rodentium, a metabolic attribute previously associated with pathogen virulence.ConclusionsOral vitamin B12 supplementation promoted C. rodentium colonization in mice by altering the activities of the Lachnospiraceae populations in the gut. A lower abundance of select Lachnospiraceae species correlated to higher p40 subunit levels, while the detection of Parasutterella exacerbated inflammatory markers in the colon of naïve mice. The B12-induced change in gut ecology enhanced the ability of C. rodentium colonization by impacting key microbe-host interactions that help with pathogen exclusion. This research provides insight into how B12 impacts the gut microbiota and highlights potential consequences of disrupting microbial B12 competition/sharing through over-supplementation. Video Abstract.

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Project description:Vitamin B12 (cobalamin, herein B12) is a key cofactor for most organisms being involved in essential metabolic processes. In microbial communities, B12 is often scarce, largely because only few prokaryotes can synthesize B12 de novo and are thus considered B12-prototrophs. B12-auxotrophy is mostly manifested by the absence of the B12-independent methionine synthase, MetE. Here, we focus on bacteria that we classified as facultative B12 consumers as they encode both B12-independent and -dependent (MetH) methionine synthases yet largely cannot synthesize B12 de novo. The genus Vibrio belongs to this group, and our work shows that upon B12 supply growth of Vibrio campbellii is accelerated and autoinducer-2 (AI-2) concentrations are enhanced. We speculate that methionine synthesis efficiency, dependent on B12 availability, is linked to AI-2 synthesis. The precursor for AI-2 synthesis is S-adenosyl-L-homocysteine (SAH), which in turn requires methionine as a precursor. In almost all Vibrio species studied, btuF (B12-binding protein), which is required for B12 uptake, and cobD (Adenosylcobinamide-phosphate synthase), which enables remodeling of B12-like compounds, are encoded on the same operon as pfs (or mtnN, Adenosylhomocysteine nucleosidase), the first enzyme in the two-step AI-2 synthesis reaction. Transcriptomic analyses show that virulence factors, such as toxin synthesis, fimbriae formation, and activation of the type-6 secretion system, which have been shown to be regulated by quorum sensing via AI-2, are significantly upregulated in V. campbellii when B12 is available. Our results demonstrate that V. campbellii is a facultative B12 consumer and indicate that B12 availability affects AI-2 levels and thus potentially virulence factor regulation.IMPORTANCEMetabolites play a key role in microbial metabolism and communication. While vitamin B12 is an essential cofactor for important enzymatic reactions, autoinducer-2 mediates interspecies signaling and can regulate the expression of genes that are crucial for virulence and survival. In our study, we hypothesize and present findings how these two important metabolites are linked in Vibrio species. Vibrio campbellii grows without B12 but at an accelerated rate when B12 is present, and we detect higher AI-2 values in cultures with B12 amendment. Transcriptome analyses show how vitamin B12 availability significantly upregulates gene expression of virulence factors such as toxin synthesis, fimbrial formation, and activation of the type-6 secretion system in V. campbellii.

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Mobilization of vitamin B₁₂ transporters alters competitive dynamics in a human gut microbe.

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Mobilization of vitamin B<sub>12</sub> transporters alters competitive dynamics in a human gut microbe.

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Mobilization of vitamin B12 transporters alters competitive dynamics in a human gut microbe.

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Mobilization of vitamin B<sub>12</sub> transporters alters competitive dynamics in a human gut microbe.

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OmicsDI is part of the ELIXIR infrastructure

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Mobilization of vitamin B₁₂ transporters alters competitive dynamics in a human gut microbe.