Global landscape of phenazine biosynthesis and biodegradation reveals species-specific colonization patterns in agricultural soils and crop microbiomes
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.
Data 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 table S4. Code can be found at: https://github.com/daniedar/phenazines.
Article and author information
Author details
Funding
Helen Hay Whitney Foundation
- Daniel Dar
Army Research Office (W911NF-17-1-0024)
- Dianne K Newman
National Institutes of Health (1R01AI127850-01A1)
- Dianne K Newman
Rothschild Foundation
- Daniel Dar
GPS Division Geobiology Postdoctoral Fellowship
- Daniel Dar
EMBO Long-Term Postdoctoral Fellowship
- Daniel Dar
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- María Mercedes Zambrano, CorpoGen, Colombia
Version history
- Received: June 5, 2020
- Accepted: September 2, 2020
- Accepted Manuscript published: September 15, 2020 (version 1)
- Version of Record published: October 27, 2020 (version 2)
Copyright
© 2020, Dar et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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