"Bacterium Protects Fungal Partner by Acting as a Toxin Sponge"

Abstract:

Many environmentally and clinically important fungi are suspectable to assault from bacterially-produced, redox-active molecules called phenazines. Despite being vulnerable to phenazine-assault, many fungi are found living within microbial communities that contain phenazine producers. Because many fungi cannot withstand phenazine challenge, but some bacterial species can, I hypothesized that a bacterial partner may be responsible for protecting fungi in these communities. In the first soil sample collected, I co-isolated several such physically associated pairings that appear to represent this hypothetical partnership class. I discovered the novel species Paraburkholderia edwinii and demonstrated that, when in the presence of a co-isolated Aspergillus species, the bacterium will protect its partner fungus from phenazine assault by sequestering the molecule and acting as a toxin sponge. When challenged with phenazines, P. edwinii changes its morphology to create bacterial aggregates within the growing fungal colony, and the bacterium creates an anoxic and reducing environment, conditions that would be expected to limit the toxicity of phenazines. A mutagenic screen revealed this program to be partially regulated by the stress-inducible transcriptional repressor HrcA, and the deletion of the hrcA gene results in a strain more capable of providing protection against phenazine assault. One relevant stressor is fungal acidification in response to phenazine challenge, and when challenged with acid P. edwinii can be made to sequester phenazines, triggering the protection response as though its fungal partner were present even when absent.

Paraburkholderia species collected from geographically diverse sites also demonstrate this protective ability toward several groups of fungi when paired in the lab, including plant and human pathogens. Finally, efforts to reproduce co-isolations of this class from the rhizosphere of citrus trees revealed such protective interactions to be common, highlighting the potential widespread nature of such mechanisms. These results have consequential implications for how microbial communities in the rhizosphere as well as plant and human infection sites are policed for membership to include or exclude certain fungal groups.