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

Elife. 2020 Sep 15:9:e59726. doi: 10.7554/eLife.59726.

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.

Keywords: Dyella japonica; ecology; infectious disease; metagenomics; microbiology; phenazines.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Agriculture
  • Biodegradation, Environmental
  • Crops, Agricultural / microbiology*
  • Gammaproteobacteria / physiology
  • Metagenomics*
  • Microbiota*
  • Phenazines / metabolism*
  • Soil / chemistry*
  • Soil Microbiology*
  • Soil Pollutants / metabolism*
  • Species Specificity
  • Up-Regulation
  • Zea mays / microbiology

Substances

  • Phenazines
  • Soil
  • Soil Pollutants
  • phenazine

Supplementary concepts

  • Dyella japonica