Soil bacteria protect fungi from phenazines by acting as toxin sponges

Abstract

Many environmentally and clinically important fungi are sensitive to toxic, bacterially produced, redox-active molecules called phenazines. Despite being vulnerable to phenazine assault, fungi inhabit microbial communities that contain phenazine producers. Because many fungi cannot withstand phenazine challenge but some bacterial species can, we hypothesized that bacterial partners may protect fungi in phenazine-replete environments. From a single soil sample, we were able to co-isolate several such physically associated pairings. We discovered the novel species Paraburkholderia edwinii and demonstrated it can protect a co-isolated Aspergillus species from phenazine-1-carboxylic acid (PCA) by sequestering it, acting as a toxin sponge; in turn, it also gains protection. When challenged with PCA, P. edwinii changes its morphology, forming aggregates within the growing fungal colony. Further, the fungal partner triggers P. edwinii to sequester PCA and maintains conditions that limit PCA toxicity by promoting an anoxic and highly reducing environment. A mutagenic screen of P. edwinii revealed this protective program depends on the stress-inducible transcriptional repressor HrcA. We show that one relevant stressor in response to PCA challenge is fungal acidification and that acid stress causes P. edwinii to behave as though the fungus were present. Finally, we reveal this phenomenon as widespread among Paraburkholderia with moderate specificity among bacterial and fungal partners, including plant and human pathogens. Our discovery suggests a common mechanism by which fungi can gain access to phenazine-replete environments and provides a tractable model system for its study. These results have implications for how microbial communities in the rhizosphere as well as in plant and human infection sites negotiate community membership via a chemical dialectic.