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Paraburkholderia edwinii protects Aspergillus sp. from phenazines by acting as a toxin sponge

Dahlstrom, Kurt M. and Newman, Dianne K. (2021) Paraburkholderia edwinii protects Aspergillus sp. from phenazines by acting as a toxin sponge. . (Unpublished) https://resolver.caltech.edu/CaltechAUTHORS:20210419-152102811

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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. In the first soil sample we collected, we co-isolated 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 revealed this 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 rhizosphere microbial communities as well as plant and human infection sites are policed for fungal membership.


Item Type:Report or Paper (Discussion Paper)
Related URLs:
URLURL TypeDescription
https://doi.org/10.1101/2021.03.28.437412DOIDiscussion Paper
ORCID:
AuthorORCID
Dahlstrom, Kurt M.0000-0001-6590-6020
Newman, Dianne K.0000-0003-1647-1918
Additional Information:The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license. This version posted March 28, 2021. We thank members of the Newman lab for constructive feedback on the project and the manuscript, and The Millard and Muriel Jacobs Genetics and Genomics Laboratory at Caltech and Igor Antoshechkin for support during library preparation and sequencing. We thank Marko Kojic for help screening transposon mutants, as well as Robert Cramer, Deborah Hogan, and Jeff Holloman for sharing their expertise in mycology. This work was supported by the Life Sciences Research Foundation (postdoctoral fellowship to K.M.D.), the Resnick Institute (K.M.D. and D.K.N.) and the NIH (1R01AI127850-01A1 to D.K.N.). Author Contributions: K.M.D. performed the experiments. K.M.D and D.K.N. designed the research strategy, analyzed data, and wrote the paper. The authors have declared no competing interest.
Group:Resnick Sustainability Institute, Caltech Center for Environmental Microbial Interactions (CEMI), Millard and Muriel Jacobs Genetics and Genomics Laboratory
Funders:
Funding AgencyGrant Number
Life Sciences Research FoundationUNSPECIFIED
Resnick Sustainability InstituteUNSPECIFIED
NIH1R01AI127850-01A1
Subject Keywords:phenazines, bacteria, fungi, protective partnership, microbial interactions, inter-kingdom
Record Number:CaltechAUTHORS:20210419-152102811
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20210419-152102811
Official Citation:Paraburkholderia edwinii protects Aspergillus sp. from phenazines by acting as a toxin sponge. Kurt M. Dahlstrom, Dianne K. Newman. bioRxiv 2021.03.28.437412; doi: https://doi.org/10.1101/2021.03.28.437412
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:108762
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:19 Apr 2021 22:39
Last Modified:19 Apr 2021 22:39

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