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

  1. Daniel Dar
  2. Linda S Thomashow
  3. David M Weller
  4. Dianne K Newman  Is a corresponding author
  1. California Institute of Technology, United States
  2. USDA Agricultural Research Service, United States

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.

The following data sets were generated

Article and author information

Author details

  1. Daniel Dar

    Division of Geological and Planetary Sciences, California Institute of Technology, Pasadena, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Linda S Thomashow

    Wheat Health, Genetics and Quality Research Unit, USDA Agricultural Research Service, Pullman, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. David M Weller

    Wheat Health, Genetics and Quality Research Unit, USDA Agricultural Research Service, Pullman, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Dianne K Newman

    Division of Biology and Biological Engineering, Division of Geological and Planetary Sciences, California Institute of Technology, Pasadena, United States
    For correspondence
    dkn@caltech.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1647-1918

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

  1. María Mercedes Zambrano, CorpoGen, Colombia

Publication history

  1. Received: June 5, 2020
  2. Accepted: September 2, 2020
  3. Accepted Manuscript published: September 15, 2020 (version 1)
  4. 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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  1. Daniel Dar
  2. Linda S Thomashow
  3. David M Weller
  4. Dianne K Newman
(2020)
Global landscape of phenazine biosynthesis and biodegradation reveals species-specific colonization patterns in agricultural soils and crop microbiomes
eLife 9:e59726.
https://doi.org/10.7554/eLife.59726
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