Dataset Information

Bipartite interactions, antibiotic production and biosynthetic potential of the Arabidopsis leaf microbiome.

ABSTRACT: Plants are colonized by phylogenetically diverse microorganisms that affect plant growth and health. Representative genome-sequenced culture collections of bacterial isolates from model plants, including Arabidopsis thaliana, have recently been established. These resources provide opportunities for systematic interaction screens combined with genome mining to discover uncharacterized natural products. Here, we report on the biosynthetic potential of 224 strains isolated from the A. thaliana phyllosphere. Genome mining identified more than 1,000 predicted natural product biosynthetic gene clusters (BGCs), hundreds of which are unknown compared to the MIBiG database of characterized BGCs. For functional validation, we used a high-throughput screening approach to monitor over 50,000 binary strain combinations. We observed 725 inhibitory interactions, with 26 strains contributing to the majority of these. A combination of imaging mass spectrometry and bioactivity-guided fractionation of the most potent inhibitor, the BGC-rich Brevibacillus sp. Leaf182, revealed three distinct natural product scaffolds that contribute to the observed antibiotic activity. Moreover, a genome mining-based strategy led to the isolation of a trans-acyltransferase polyketide synthase-derived antibiotic, macrobrevin, which displays an unprecedented natural product structure. Our findings demonstrate that the phyllosphere is a valuable environment for the identification of antibiotics and natural products with unusual scaffolds.

SUBMITTER: Helfrich EJN

PROVIDER: S-EPMC7115891 | biostudies-literature | 2018 Aug

REPOSITORIES: biostudies-literature

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Bipartite interactions, antibiotic production and biosynthetic potential of the Arabidopsis leaf microbiome.

Helfrich Eric J N EJN Vogel Christine M CM Ueoka Reiko R Schäfer Martin M Ryffel Florian F Müller Daniel B DB Probst Silke S Kreuzer Markus M Piel Jörn J Vorholt Julia A JA

Nature microbiology 20180723 8

Plants are colonized by phylogenetically diverse microorganisms that affect plant growth and health. Representative genome-sequenced culture collections of bacterial isolates from model plants, including Arabidopsis thaliana, have recently been established. These resources provide opportunities for systematic interaction screens combined with genome mining to discover uncharacterized natural products. Here, we report on the biosynthetic potential of 224 strains isolated from the A. thaliana phyl ...[more]

PMID: 30038309

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Project description:Natural products (NPs) isolated from bacteria have dramatically advanced human society, especially in medicine and agriculture. The rapidity and ease of genome sequencing have enabled bioinformatics-guided NP discovery and characterization. As a result, NP potential and diversity within a complex community, such as the microbiome of a plant, are rapidly expanding areas of scientific exploration. Here, we assess biosynthetic diversity in the Populus microbiome by analyzing both bacterial isolate genomes and metagenome samples. We utilize the fully sequenced genomes of isolates from the Populus root microbiome to characterize a subset of organisms for NP potential. The more than 3,400 individual gene clusters identified in 339 bacterial isolates, including 173 newly sequenced organisms, were diverse across NP types and distinct from known NP clusters. The ribosomally synthesized and posttranslationally modified peptides were both widespread and divergent from previously characterized molecules. Lactones and siderophores were prevalent in the genomes, suggesting a high level of communication and pressure to compete for resources. We then consider the overall bacterial diversity and NP variety of metagenome samples compared to the sequenced isolate collection and other plant microbiomes. The sequenced collection, curated to reflect the phylogenetic diversity of the Populus microbiome, also reflects the overall NP diversity trends seen in the metagenomic samples. In our study, only about 1% of all clusters from sequenced isolates were positively matched to a previously characterized gene cluster, suggesting a great opportunity for the discovery of novel NPs involved in communication and control in the Populus root microbiome. IMPORTANCE The plant root microbiome is one of the most diverse and abundant biological communities known. Plant-associated bacteria can have a profound effect on plant growth and development, and especially on protection from disease and environmental stress. These organisms are also known to be a rich source of antibiotic and antifungal drugs. In order to better understand the ways bacterial communities influence plant health, we evaluated the diversity and uniqueness of the natural product gene clusters in bacteria isolated from poplar trees. The complex molecule clusters are abundant, and the majority are unique, suggesting a great potential to discover new molecules that could not only affect plant health but also could have applications as antibiotic agents.

Project description:Leaves are primarily responsible for the plant's photosynthetic activity. Thus, changes in the leaf microbiota, which includes deleterious and beneficial microbes, can have far-reaching effects on plant fitness and productivity. Identifying the processes and microorganisms that drive these changes over a plant's lifetime is, therefore, crucial. In this study, we analyzed the temporal dynamics in the leaf microbiome of Arabidopsis thaliana, integrating changes in both composition and microbe-microbe interactions via the study of microbial networks. Field-grown Arabidopsis were used to monitor leaf bacterial, fungal and oomycete communities throughout the plant's natural growing season (extending from November to March) over three consecutive years. Our results revealed the existence of conserved temporal patterns, with microbial communities and networks going through a stabilization phase of decreased diversity and variability at the beginning of the plant's growing season. Despite a high turnover in these communities, we identified 19 "core" taxa persisting on Arabidopsis leaves across time and plant generations. With the hypothesis these microbes could be playing key roles in the structuring of leaf microbial communities, we conducted a time-informed microbial network analysis which showed core taxa are not necessarily highly connected network "hubs," and "hubs" alternate with time. Our study shows that leaf microbial communities exhibit reproducible dynamics and patterns, suggesting the potential of using our understanding of temporal trajectories in microbial community composition to design experiments aimed at driving these communities toward desired states. IMPORTANCE Utilizing plant microbiota to promote plant growth and plant health is key to more environmentally friendly agriculture. A major bottleneck in the engineering of plant-beneficial microbial communities is the low persistence of applied microbes under filed conditions, especially considering plant leaves. Indeed, although many leaf-associated microorganisms have the potential to promote plant growth and protect plants from pathogens, few of them are able to survive and thrive over time. In our study, we could show that leaf microbial communities are very variable at the beginning of the plant growing season but become more and more similar and less variable as the season progresses. We further identify a cohort of 19 "core" microbes, systematically present on plant leaves that would make these microbes exceptional candidates for future agricultural applications.

Dataset Information

Bipartite interactions, antibiotic production and biosynthetic potential of the Arabidopsis leaf microbiome.

Publications

Bipartite interactions, antibiotic production and biosynthetic potential of the Arabidopsis leaf microbiome.

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