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Cofunctioning of bacterial exometabolites drives root microbiota establishment.

ABSTRACT: Soil-dwelling microbes are the principal inoculum for the root microbiota, but our understanding of microbe-microbe interactions in microbiota establishment remains fragmentary. We tested 39,204 binary interbacterial interactions for inhibitory activities in vitro, allowing us to identify taxonomic signatures in bacterial inhibition profiles. Using genetic and metabolomic approaches, we identified the antimicrobial 2,4-diacetylphloroglucinol (DAPG) and the iron chelator pyoverdine as exometabolites whose combined functions explain most of the inhibitory activity of the strongly antagonistic Pseudomonas brassicacearum R401. Microbiota reconstitution with a core of Arabidopsis thaliana root commensals in the presence of wild-type or mutant strains revealed a root niche-specific cofunction of these exometabolites as root competence determinants and drivers of predictable changes in the root-associated community. In natural environments, both the corresponding biosynthetic operons are enriched in roots, a pattern likely linked to their role as iron sinks, indicating that these cofunctioning exometabolites are adaptive traits contributing to pseudomonad pervasiveness throughout the root microbiota.

SUBMITTER: Getzke F

PROVIDER: S-EPMC10104540 | biostudies-literature | 2023 Apr

REPOSITORIES: biostudies-literature

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Cofunctioning of bacterial exometabolites drives root microbiota establishment.

Getzke Felix F Hassani M Amine MA Crüsemann Max M Malisic Milena M Zhang Pengfan P Ishigaki Yuji Y Böhringer Nils N Jiménez Fernández Alicia A Wang Lei L Ordon Jana J Ma Ka-Wai KW Thiergart Thorsten T Harbort Christopher J CJ Wesseler Hidde H Miyauchi Shingo S Garrido-Oter Ruben R Shirasu Ken K Schäberle Till F TF Hacquard Stéphane S Schulze-Lefert Paul P

Proceedings of the National Academy of Sciences of the United States of America 20230405 15

Soil-dwelling microbes are the principal inoculum for the root microbiota, but our understanding of microbe-microbe interactions in microbiota establishment remains fragmentary. We tested 39,204 binary interbacterial interactions for inhibitory activities in vitro, allowing us to identify taxonomic signatures in bacterial inhibition profiles. Using genetic and metabolomic approaches, we identified the antimicrobial 2,4-diacetylphloroglucinol (DAPG) and the iron chelator pyoverdine as exometaboli ...[more]

PMID: 37018204

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Project description:During prolonged resource limitation, bacterial cells can persist in metabolically active states of non-growth. These maintenance periods, such as those experienced in stationary phase, can include upregulation of secondary metabolism and release of exometabolites into the local environment. As resource limitation is common in many environmental microbial habitats, we hypothesized that neighboring bacterial populations employ exometabolites to compete or cooperate during maintenance and that these exometabolite-facilitated interactions can drive community outcomes. Here, we evaluated the consequences of exometabolite interactions over the stationary phase among three environmental strains: Burkholderia thailandensis E264, Chromobacterium subtsugae ATCC 31532, and Pseudomonas syringae pv. tomato DC3000. We assembled them into synthetic communities that only permitted chemical interactions. We compared the responses (transcripts) and outputs (exometabolites) of each member with and without neighbors. We found that transcriptional dynamics were changed with different neighbors and that some of these changes were coordinated between members. The dominant competitor B. thailandensis consistently upregulated biosynthetic gene clusters to produce bioactive exometabolites for both exploitative and interference competition. These results demonstrate that competition strategies during maintenance can contribute to community-level outcomes. It also suggests that the traditional concept of defining competitiveness by growth outcomes may be narrow and that maintenance competition could be an additional or alternative measure.ImportanceFree-living microbial populations often persist and engage in environments that offer few or inconsistently available resources. Thus, it is important to investigate microbial interactions in this common and ecologically relevant condition of non-growth. This work investigates the consequences of resource limitation for community metabolic output and for population interactions in simple synthetic bacterial communities. Despite non-growth, we observed active, exometabolite-mediated competition among the bacterial populations. Many of these interactions and produced exometabolites were dependent on the community composition but we also observed that one dominant competitor consistently produced interfering exometabolites regardless. These results are important for predicting and understanding microbial interactions in resource-limited environments.

Project description:In addition to the rhizobia, other non-rhizobial endophytes (NREs) have been simultaneously isolated from the root nodules. The existence of NREs in leguminous root nodules is a universal phenomenon, and they have the potential to enhance legume survival, especially under conditions of environmental stress. However, the diversity and biogeographic patterns of microbial communities inhabiting root nodules are not well studied or understood. Here, we explored and characterized the diversity of NRE bacteria by using 16S rRNA gene high-throughput amplicon sequencing. Additionally, we compared the biogeography and co-occurrence patterns in review of the bacterial microbiota inhabiting the rhizosphere, the bulk soil and the root nodule bacterial communities associated with Sophora davidii, a native N-fixing wild leguminous shrub in hilly and gully regions of the Loess Plateau of China. The results showed the presence of a large diversity of bacteria belonging to 81 phyla, 154 classes, 333 orders, 463 families, and 732 genera inside the nodules. Proteobacteria were dominant in the nodule and rhizosphere soil samples, and Actinomycetes were dominant in the bulk soil samples. Mesorhizobium was the dominant genus in the nodules, accounting for between 60.15 and 83.74% of the bacteria. The microbial community composition of the NRE in the root nodules differed from that in the rhizosphere soil and the bulk soil of S. davidii. Moreover, we found that the biogeographic patterns and assembly process of the rhizobia and non-rhizobia communities differed in the root nodule, the rhizosphere soil and the bulk soil. Furthermore, the correlation analysis between the soil's physical and chemical properties and the bacteria showed that available phosphorus was the predominant factor affecting the bacterial diversity within the rhizosphere soil. Finally, our results revealed that the microbial network diagram of co-occurrence patterns showed more complexes in the soil than in the root nodules. This indicates that only specific microorganisms could colonize and thrive in the rhizosphere through the selection and filtering effects of roots. In conclusion, there are significant differences in bacterial community composition in the nodules, rhizosphere and bulk soil in the hilly and gully region of the Loess Plateau, which is the result of environmental filtration. Our study improves the understanding of the biogeographic patterns and diversity of bacterial microbiota inhabiting root nodules and can help quantify and define the root nodule assemblage process of S. davidii.

Project description:BackgroundEmerging evidences have indicated that the composition of gut microbiota was significantly influenced by central nervous system diseases. The digestion and metabolism disturbances of patients with amyotrophic lateral sclerosis (ALS) might be strongly associated with ALS; however, this has rarely been evaluated in these populations. This study was to evaluate bacterial and archaeal composition of gut flora and the corresponding metabolism performance of these micro-organisms in fecal samples of patients with ALS.MethodsA comparative study was performed on the intestinal microbiota from eight patients with ALS and eight healthy individuals at Huadong Hospital during November 2017 to April 2018; meanwhile, the metabolite concentrations of human endotoxin, short-chain fatty acids (SCFA), NO2-N/NO3-N, and γ-aminobutyric acid were also evaluated by spectrophotometry methods. The correlations between intestinal microbiota and metabolite concentration were compared between the two groups using one-way analysis of variance; the relative abundance of beneficial and harmful micro-organisms in fecal samples was also analyzed.ResultsIn general, the richness and evenness of bacterial and archaeal communities of healthy individuals were healthier than that of patients with ALS. The phylum Firmicutes/Bacteroidetes ratio, genus Methanobrevibacter showed an enhancive tendency in patients with ALS, whereas the relative abundance of beneficial micro-organisms (genera Faecalibacterium and Bacteroides) presented a significant decrease tendency in patients with ALS. In addition, the average concentrations of human endotoxin, SCFA, NO2-N/NO3-N, and γ-aminobutyric acid in patients with ALS and healthy individuals were 64.2 vs. 65.3 EU/mL, 57.5 vs. 55.3 μg/mL, 5.7 vs. 5.3 ng/mL, and 6.1 vs. 5.4 μmol/L, respectively, indicating that the digestion and metabolism functions of gastrointestinal tract of patients might decline with this disease.ConclusionsThe relative abundance of beneficial and harmful micro-organisms respectively showed decrease and increase tendency in patients with ALS.

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Cofunctioning of bacterial exometabolites drives root microbiota establishment.

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Cofunctioning of bacterial exometabolites drives root microbiota establishment.

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