Soil bacteria protect fungi from phenazines by acting as toxin sponges

Area of Science:

• Microbiology
• Mycology
• Biochemistry

Background:

• Fungi are sensitive to phenazines, toxic molecules produced by bacteria.
• Fungi often coexist with phenazine-producing bacteria in various environments.
• Bacterial partners may offer protection to fungi in phenazine-rich habitats.

Purpose of the Study:

• To investigate the hypothesis that bacterial partners protect fungi from phenazine toxicity.
• To discover and characterize novel bacterial species involved in fungal-bacterial mutualism.
• To elucidate the mechanisms underlying fungal protection against phenazines.

Main Methods:

• Co-isolation of fungal and bacterial species from soil samples.
• Identification of a novel bacterial species, Paraburkholderia edwinii.
• Phenazine-1-carboxylic acid (PCA) challenge assays with co-isolated partners.
• Morphological and environmental analyses of P. edwinii in response to PCA.
• Mutagenic screening of P. edwinii to identify key regulatory genes (e.g., HrcA).
• Investigation of fungal acidification as a trigger for bacterial protective responses.

Main Results:

• Discovery of Paraburkholderia edwinii, a novel bacterial species that protects a co-isolated Aspergillus fungus from phenazine-1-carboxylic acid (PCA).
• P. edwinii sequesters PCA, acting as a "toxin sponge," and alters its morphology by forming aggregates within the fungal colony.
• The fungal partner induces PCA sequestration by P. edwinii and creates an anoxic, reducing environment to mitigate PCA toxicity.
• The protective mechanism in P. edwinii is regulated by the stress-inducible transcriptional repressor HrcA.
• Fungal acidification was identified as a key stressor that triggers P. edwinii's protective response, mimicking the presence of the fungus.
• This protective phenomenon is widespread among Paraburkholderia species and shows moderate specificity among bacterial and fungal partners, including pathogens.

Conclusions:

• Bacterial sequestration of phenazines provides a crucial protective mechanism for fungi in environments where these toxins are prevalent.
• The interaction between P. edwinii and its fungal partner demonstrates a novel form of microbial mutualism driven by chemical signaling and environmental modification.
• The HrcA regulatory pathway in P. edwinii is central to its ability to sense and respond to fungal-associated stressors, leading to phenazine detoxification.
• This study reveals a common strategy employed by fungi to inhabit phenazine-replete environments, with significant implications for understanding microbial community dynamics in diverse ecosystems, including plant and human infections.