Pangenome analysis of Enterobacteria reveals richness of secondary metabolite gene clusters and their associated gene sets

Mohite, Omkar S.; Lloyd, Colton J.; Monk, Jonathan M.; Weber, Tilmann; Palsson, Bernhard Ø.

doi:10.1016/j.synbio.2022.04.011

Cited by 12 publications

(14 citation statements)

References 59 publications

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“…Actinobacteria currently represent the main source of antibiotics for clinical and agricultural uses (Krell and Matilla, 2022). However, as this study has confirmed, plantassociated bacteria represent a potential source for novel antibiotics (Gavriilidou et al, 2022;Matilla et al, 2022;Mohite et al, 2022). Remarkably, the biosynthesis of specific antibiotic compounds by plant-associated bacteria has been shown to play a key role in the protection of agricultural crops by beneficial microbes (Mendes et al, 2011;Carrión et al, 2019;Hou and Kolodkin-Gal, 2020).…”

Section: Discussionmentioning

confidence: 84%

“…Genome mining approaches have estimated that only approximately 3% of the bacterial secondary biosynthetic potential has been assessed experimentally (Gavriilidou et al, 2022 ) and Enterobacteria, including those that live in association with plants, are among the taxonomic groups with the highest biosynthetic potential (Gavriilidou et al, 2022 ; Mohite et al, 2022 ). PKS and NRPS gene clusters were found among the most abundant secondary metabolite gene clusters in plant‐associated bacteria (Blair et al, 2018 ; Carrión et al, 2019 ; Helfrich et al, 2018 ).…”

Section: Introductionmentioning

confidence: 99%

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Herbicolin A production and its modulation by quorum sensing in aPantoea agglomeransrhizobacterium bioactive against a broad spectrum of plant‐pathogenic fungi

Matilla

Evans

Martín

et al. 2022

Microbial Biotechnology

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Global population growth makes it necessary to increase agricultural production yields.However, climate change impacts and diseases caused by plant pathogens are challenging modern agriculture. Therefore, it is necessary to look for alternatives to the excessive use of chemical fertilizers and pesticides. The plant microbiota plays an essential role in plant nutrition and health, and offers enormous potential to meet future challenges of agriculture. In this context, here we characterized the antifungal properties of the rhizosphere bacterium Pantoea agglomerans 9Rz4, which is active against a broad spectrum of plant pathogenic fungi. Chemical analyses revealed that strain 9Rz4 produces the antifungal herbicolin A and its biosynthetic gene cluster was identified and characterized. We found that the only acyl-homoserine lactone-based quorum sensing system of 9Rz4 modulates herbicolin A gene cluster expression. No role of plasmid carriage in the production of herbicolin A was observed. Plant assays revealed that herbicolin A biosynthesis does not affect the root colonization ability of P. agglomerans 9Rz4. Current legislative restrictions are aimed at reducing the use of chemical pesticides in agriculture, and the results derived from this study may lay the foundations for the development of novel biopesticides from rhizosphere microorganisms.

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Section: Discussionmentioning

confidence: 84%

Section: Introductionmentioning

confidence: 99%

Herbicolin A production and its modulation by quorum sensing in aPantoea agglomeransrhizobacterium bioactive against a broad spectrum of plant‐pathogenic fungi

Matilla

Evans

Martín

et al. 2022

Microbial Biotechnology

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“…Pangenome analysis may be useful for redefining the taxonomic and pathogenic positions, as already demonstrated on species of the genus Shigella and Escherichia coli strains [ 248 ], but also as a promising tool for identifying novel secondary metabolites through microbial communality profiling. Mohite et al reported in 2019 the (pan)genome mining of 2627 enterobacterial genomes, which resulted in the detection of 8604 BCGs, corresponding to 212 BGC families, of which only 20 were associated with previously characterized BGCs from the MIBIG database as siderophores, antibiotics, and genotoxins [ 249 ].…”

Section: Genome Sequencing Methods For Dereplication and Structure El...mentioning

confidence: 99%

Advanced Methods for Natural Products Discovery: Bioactivity Screening, Dereplication, Metabolomics Profiling, Genomic Sequencing, Databases and Informatic Tools, and Structure Elucidation

et al. 2023

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Natural Products (NP) are essential for the discovery of novel drugs and products for numerous biotechnological applications. The NP discovery process is expensive and time-consuming, having as major hurdles dereplication (early identification of known compounds) and structure elucidation, particularly the determination of the absolute configuration of metabolites with stereogenic centers. This review comprehensively focuses on recent technological and instrumental advances, highlighting the development of methods that alleviate these obstacles, paving the way for accelerating NP discovery towards biotechnological applications. Herein, we emphasize the most innovative high-throughput tools and methods for advancing bioactivity screening, NP chemical analysis, dereplication, metabolite profiling, metabolomics, genome sequencing and/or genomics approaches, databases, bioinformatics, chemoinformatics, and three-dimensional NP structure elucidation.

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“…Large-scale pangenome mining studies help to understand the evolutionary patterns of biosynthetic gene clusters (BGCs) along with a deep characterization of the biosynthetic repertoire of a given bacterial species or genus [12][13][14][15]. Detailed comparative studies are now gathering evidence that vertical inheritance facilitates the diversification of BGCs more frequently than horizontal gene transfer [16].…”

Section: Introductionmentioning

confidence: 99%

Pangenome mining of theStreptomycesgenus redefines their biosynthetic potential

Mohite,

Jørgensen,

Booth

et al. 2024

Preprint

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BackgroundStreptomycesis a highly diverse genus known for the production of secondary or specialized metabolites with a wide range of applications in the medical and agricultural industries. Several thousand complete or nearly-completeStreptomycesgenome sequences are now available, affording the opportunity to deeply investigate the biosynthetic potential within these organisms and to advance natural product discovery initiatives.ResultWe performed pangenome analysis on 2,371Streptomycesgenomes, including approximately 1,200 complete assemblies. Employing a data-driven approach based on genome similarities, theStreptomycesgenus was classified into 7 primary and 42 secondary MASH-clusters, forming the basis for a comprehensive pangenome mining. A refined workflow for grouping biosynthetic gene clusters (BGCs) redefined their diversity across different MASH-clusters. This workflow also reassigned 2,729 known BGC families to only 440 families, a reduction caused by inaccuracies in BGC boundary detections. When the genomic location of BGCs is included in the analysis, a conserved genomic structure (synteny) among BGCs becomes apparent within species and MASH-clusters. This synteny suggests that vertical inheritance is a major factor in the acquisition of new BGCs.ConclusionOur analysis of a genomic dataset at a scale of thousands of genomes refined predictions of BGC diversity using MASH-clusters as a basis for pangenome analysis. The observed conservation in the order of BGCs’ genomic locations showed that the BGCs are vertically inherited. The presented workflow and the in-depth analysis pave the way for large-scale pangenome investigations and enhance our understanding of the biosynthetic potential of theStreptomycesgenus.

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Pangenome analysis of Enterobacteria reveals richness of secondary metabolite gene clusters and their associated gene sets

Cited by 12 publications

References 59 publications

Herbicolin A production and its modulation by quorum sensing in aPantoea agglomeransrhizobacterium bioactive against a broad spectrum of plant‐pathogenic fungi

Herbicolin A production and its modulation by quorum sensing in aPantoea agglomeransrhizobacterium bioactive against a broad spectrum of plant‐pathogenic fungi

Advanced Methods for Natural Products Discovery: Bioactivity Screening, Dereplication, Metabolomics Profiling, Genomic Sequencing, Databases and Informatic Tools, and Structure Elucidation

Pangenome mining of theStreptomycesgenus redefines their biosynthetic potential

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