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

Daniel Dar,Linda S Thomashow,David M Weller,Dianne K Newman

doi:10.7554/elife.59726

Daniel Dar, Linda S Thomashow + Show 2 more

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https://doi.org/10.7554/elife.59726

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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.

Highlights

Phenazines are heterotricyclic N-containing metabolites mainly produced by bacteria in soil and plant-root microbiomes (Biessy and Filion, 2018; Mavrodi et al, 2010), though some are important in chronic human infections (Sismaet et al, 2016; Wilson et al, 1988)
Root hair tips appeared to be preferentially colonized by D. japonica (Figure 6E). This is the first study to quantitatively chart the biogeographic distribution of phenazine biosynthesis and biodegradation genes in natural and agricultural habitats
We developed and field-validated a computational method to analyze >800 metagenomes from across the world and show that phenazine biosynthesis is a highly prevalent trait that is enriched in plant microbiomes relative to bulk soils

Summary

Introduction

Phenazines are heterotricyclic N-containing metabolites mainly produced by bacteria in soil and plant-root microbiomes (Biessy and Filion, 2018; Mavrodi et al, 2010), though some are important in chronic human infections (Sismaet et al, 2016; Wilson et al, 1988). Members of this diverse family of redox-active metabolites act as broad-spectrum antibiotics by generating toxic reactive oxygen species (ROS) as well as interfering with cellular respiration chains (Baron et al, 1989; Perry and Newman, 2019).

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