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.

Bidirectional redox cycling of phenazine-1-carboxylic acid byCitrobacter portucalensisMBL drives increased nitrate reduction

“…Nitrate-dependent PCA red oxidation is likely to be common in anoxic environments, such as soils, as it is not species-specific and occurs readily. If the outsized effect of PCA red oxidation on nitrate reduction that we observe generalizes to other species, the production and reduction of phenazines by organisms like Pseudomonads likely affects the rate of nitrate consumption in their environs, adding another function to the phenazine arsenal (18). We propose that cells may catalyze a PCA redox cycle whenever they have internal stores of reducing equivalents and a usable terminal electron acceptor (Fig 2B).…”

Paraburkholderia edwiniiprotectsAspergillussp. from phenazines by acting as a toxin sponge

“…We believe the answer is yes for several reasons. First, phenazine producers are widespread in nature 6 and thus odds are high that fungi will encounter them. Second, we were able to readily isolate a variety of such partnerships.…”

“…Finally, plant associated fungi known as mycorrhizae play an outsized role in carbon sequestration: mycorrhizae-associated vegetation sequester approximately 350 gigatons of carbon a year compared to 29 gigatons stored by nonmycorrhizae-associated vegetation 3 . Notably, phenazine producers are found in diverse environments beyond food crops, including in forests and grasslands, thus pointing to another niche of consequence where fungi must navigate phenazine assault 6 .…”

“…Important amongst these are phenazines, redox active compounds that can restrict fungal growth and have been shown to be responsible for excluding fungi from agriculturally important microbial communities 4,5 . A recent metagenomic study revealed that phenazine biosynthesis capacity is widespread in agricultural soils and crop microbiomes 6 . Given that drier soils are also associated with higher rates of phenazine producers colonizing wheat, this suggests that soil fungi may need to contend with higher concentrations of phenazines as the climate shifts 7,8 .…”

“…Notably, phenazine producers are found in diverse environments beyond food crops, including in forests and grasslands, thus pointing to another niche of consequence where fungi must navigate phenazine assault 6 .…”