Abstract
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.
Original language | English |
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Article number | e0004518 |
Journal | mSystems |
Volume | 3 |
Issue number | 5 |
DOIs | |
State | Published - Sep 1 2018 |
Funding
This article has been authored by UT-Battelle, LLC, under contract DE-AC05-00OR22725 with the U.S. Department of Energy (DOE). This research was funded by the U.S. DOE Office of Biological and Environmental Research, Genomic Science Program as part of the Plant Microbe Interfaces Scientific Focus Area (http://pmi.ornl.gov). Oak Ridge National Laboratory is managed by UT-Battelle, LLC, for the U.S. Department of Energy under contract DE-AC05-00OR22725. The sequencing work was conducted by the U.S. Department of Energy Joint Genome Institute, a DOE Office of Science User Facility, is supported by the Office of Science of the U.S. Department of Energy under contract DE-AC02-05CH11231. The sequencing work was conducted using JGI CSP1429 under project manager Nichole Shapiro. P.M.B. designed, performed, and analyzed experiments and wrote the article. M.L.L., D.A.J., and M.J.P. conducted bioinformatic data collection. T.-Y.S.L. isolated strains and genomic DNA (gDNA). D.A.P. and M.J.D. designed experiments and edited the manuscript. All authors read and approved the final manuscript.
Keywords
- Biosynthetic gene clusters
- Natural product biosynthesis
- Plant-microbe interactions
- Quorum sensing
- Rhizosphere-inhabiting microbes
- Siderophores