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Exploration of the Biosynthetic Potential of the Populus Microbiome

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 co...

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Autores principales: Blair, Patricia M., Land, Miriam L., Piatek, Marek J., Jacobson, Daniel A., Lu, Tse-Yuan S., Doktycz, Mitchel J., Pelletier, Dale A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6172771/
https://www.ncbi.nlm.nih.gov/pubmed/30320216
http://dx.doi.org/10.1128/mSystems.00045-18
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author Blair, Patricia M.
Land, Miriam L.
Piatek, Marek J.
Jacobson, Daniel A.
Lu, Tse-Yuan S.
Doktycz, Mitchel J.
Pelletier, Dale A.
author_facet Blair, Patricia M.
Land, Miriam L.
Piatek, Marek J.
Jacobson, Daniel A.
Lu, Tse-Yuan S.
Doktycz, Mitchel J.
Pelletier, Dale A.
author_sort Blair, Patricia M.
collection PubMed
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.
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spelling pubmed-61727712018-10-12 Exploration of the Biosynthetic Potential of the Populus Microbiome Blair, Patricia M. Land, Miriam L. Piatek, Marek J. Jacobson, Daniel A. Lu, Tse-Yuan S. Doktycz, Mitchel J. Pelletier, Dale A. mSystems Research Article 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. American Society for Microbiology 2018-10-02 /pmc/articles/PMC6172771/ /pubmed/30320216 http://dx.doi.org/10.1128/mSystems.00045-18 Text en https://doi.org/10.1128/AuthorWarrantyLicense.v1 This is a work of the U.S. Government and is not subject to copyright protection in the United States. Foreign copyrights may apply.
spellingShingle Research Article
Blair, Patricia M.
Land, Miriam L.
Piatek, Marek J.
Jacobson, Daniel A.
Lu, Tse-Yuan S.
Doktycz, Mitchel J.
Pelletier, Dale A.
Exploration of the Biosynthetic Potential of the Populus Microbiome
title Exploration of the Biosynthetic Potential of the Populus Microbiome
title_full Exploration of the Biosynthetic Potential of the Populus Microbiome
title_fullStr Exploration of the Biosynthetic Potential of the Populus Microbiome
title_full_unstemmed Exploration of the Biosynthetic Potential of the Populus Microbiome
title_short Exploration of the Biosynthetic Potential of the Populus Microbiome
title_sort exploration of the biosynthetic potential of the populus microbiome
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6172771/
https://www.ncbi.nlm.nih.gov/pubmed/30320216
http://dx.doi.org/10.1128/mSystems.00045-18
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