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Global landscape of phenazine biosynthesis and biodegradation reveals species-specific colonization patterns in agricultural soils and crop microbiomes

Dar, Daniel and Thomashow, Linda S. and Weller, David M. and Newman, Dianne K. (2020) Global landscape of phenazine biosynthesis and biodegradation reveals species-specific colonization patterns in agricultural soils and crop microbiomes. eLife, 2020 (9). Art. No. e59726. ISSN 2050-084X. https://resolver.caltech.edu/CaltechAUTHORS:20200609-075446759

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Abstract

Phenazines are natural bacterial antibiotics that can protect crops from disease. However, for most crops it is unknown which producers and specific phenazines are ecologically relevant, and whether phenazine biodegradation can counter their effects. To better understand their ecology, we developed and environmentally-validated a quantitative metagenomic approach to mine for phenazine biosynthesis and biodegradation genes, applying it to >800 soil and plant-associated shotgun-metagenomes. We discover novel producer-crop associations and demonstrate that phenazine biosynthesis is prevalent across habitats and preferentially enriched in rhizospheres, whereas biodegrading bacteria are rare. We validate an association between maize and Dyella japonica, a putative producer abundant in crop microbiomes. D. japonica upregulates phenazine biosynthesis during phosphate limitation and robustly colonizes maize seedling roots. This work provides a global picture of phenazines in natural environments and highlights plant-microbe associations of agricultural potential. Our metagenomic approach may be extended to other metabolites and functional traits in diverse ecosystems.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.7554/eLife.59726DOIArticle
https://doi.org/10.1101/2020.06.05.136879DOIDiscussion Paper
https://github.com/daniedar/phenazinesRelated ItemCode
ORCID:
AuthorORCID
Dar, Daniel0000-0002-6650-5488
Thomashow, Linda S.0000-0002-0809-3606
Weller, David M.0000-0001-8533-7136
Newman, Dianne K.0000-0003-1647-1918
Additional Information:© 2020 Dar et al. This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited. Received: 05 June 2020; Accepted: 02 September 2020; Published: 15 September 2020. We thank Jeff Dangl and Adam Deutschbauer for kindly providing us with the D. japonica UNC79MFTsu3.2 strain. We also thank Darcy McRose for help with LC-MS sample preparation and analysis, Megan Bergkessel and Kurt Dahlstrom for their help with mutant generation, Will DePas for assistance with HCR, as well as the rest of the Newman lab for fruitful discussions and comments. We also thank Gil Sharon and Alon Philosof for critically reading the manuscript. We thank Mingming Yang with assistance in collecting, processing, and performing viable counts of phenazine-producing pseudomonads from Washington State University’s Lind Dryland Research Station. We also thank Bruce Sauer and Brian Fode for plot maintenance. Grants to DKN from the NIH (1R01AI127850-01A1) and ARO (W911NF-17-1-0024) supported this work. DD was supported by the Rothschild foundation, EMBO Long-Term, and the Helen Hay Whitney postdoctoral fellowships, as well as a Geobiology Postdoctoral Fellowship from the Division of Geological and Planetary Sciences, Caltech. The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication. Data and software availability: The metagenomic DNA-sequencing data generated in this study were deposited in the Sequence Read Archive (SRA) under accession PRJNA634917. All public SRA samples analyzed in this study are indicated in Supplementary file 4. Code can be found at: https://github.com/daniedar/phenazines (Dar, 2020; copy archived at https://github.com/elifesciences-publications/phenazines). Author contributions: Daniel Dar, Conceptualization, Data curation, Formal analysis, Funding acquisition, Validation, Investigation, Visualization, Methodology, Writing - original draft, Writing - review and editing; Linda S Thomashow, David M Weller, Investigation, Writing - review and editing; Dianne K Newman, Conceptualization, Supervision, Funding acquisition, Writing - original draft, Writing - review and editing.
Funders:
Funding AgencyGrant Number
NIH1R01AI127850-01A1
Army Research Office (ARO)W911NF-17-1-0024
Rothschild FoundationUNSPECIFIED
European Molecular Biology Organization (EMBO)UNSPECIFIED
Helen Hay Whitney FoundationUNSPECIFIED
Caltech Division of Geological and Planetary SciencesUNSPECIFIED
Issue or Number:9
Record Number:CaltechAUTHORS:20200609-075446759
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20200609-075446759
Official Citation:Global landscape of phenazine biosynthesis and biodegradation reveals species-specific colonization patterns in agricultural soils and crop microbiomes. eLife 2020;9:e59726; DOI: 10.7554/eLife.59726
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:103785
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:09 Jun 2020 17:47
Last Modified:06 Nov 2020 17:11

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