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Soil bacteria protect fungi from phenazines by acting as toxin sponges

Dahlstrom, Kurt M. and Newman, Dianne K. (2022) Soil bacteria protect fungi from phenazines by acting as toxin sponges. Current Biology, 32 (2). pp. 275-288. ISSN 0960-9822. doi:10.1016/j.cub.2021.11.002.

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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.

Item Type:Article
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URLURL TypeDescription
Dahlstrom, Kurt M.0000-0001-6590-6020
Newman, Dianne K.0000-0003-1647-1918
Additional Information:© 2021 Elsevier Inc. Received 28 March 2021, Revised 12 August 2021, Accepted 1 November 2021, Available online 22 November 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. We thank Susan Duffy for skillful instruction in biology and the belief that substantial goals are achievable when we work together. This work was supported by the Life Sciences Research Foundation (postdoctoral fellowship to K.M.D.), the Resnick Sustainability Institute (K.M.D. and D.K.N.), and the NIH (1R01AI127850-01A1 to D.K.N.). The ORCIDs for this article are as follows: 0000-0001-6590-6020 (K.M.D.) and 0000-0003-1647-1918 (D.K.N.). Author contributions. K.M.D. performed the experiments and wrote the original draft. D.K.N. supervised the project. K.M.D. and D.K.N. designed the research strategy, analyzed data, acquired funding for the project, and re-wrote, reviewed, and edited the paper. Declaration of interests. The authors have filed a provisional patent (CIT-8617-P) “Biocontrol strain to protect fungi from phenazine antibiotics” based on this work. Data and code availability. Genomic data generated in this study to characterize the co-isolated Aspergillus species and P. edwinii, and used to generate in-frame deletions for P. edwinii, have been deposited with GenBank under accession numbers Genbank: JAHXQV000000000 (Aspergillus whole genome shotgun sequence) and Genbank: CP080095-CP080096 (full chromosomes for P. edwinii) and are available as of the date of publication. This study does not report any original code. Microscopy data reported in this paper will be shared by the lead contact upon request, and any additional information required to reanalyze the data reported in this paper is available from the lead contact upon request.
Group:Resnick Sustainability Institute
Funding AgencyGrant Number
Life Sciences Research FoundationUNSPECIFIED
Resnick Sustainability InstituteUNSPECIFIED
Subject Keywords:phenazines; bacteria; fungi; protective partnership; microbial interactions; inter-kingdom; rhizosphere; community
Issue or Number:2
Record Number:CaltechAUTHORS:20211208-560304000
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Official Citation:Kurt M. Dahlstrom, Dianne K. Newman, Soil bacteria protect fungi from phenazines by acting as toxin sponges, Current Biology, Volume 32, Issue 2, 2022, Pages 275-288.e5, ISSN 0960-9822, (
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:112285
Deposited By: George Porter
Deposited On:09 Dec 2021 17:58
Last Modified:25 Jan 2022 22:39

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