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Prevalence and Correlates of Phenazine Resistance in Culturable Bacteria from a Dryland Wheat Field

Perry, Elena K. and Newman, Dianne K. (2022) Prevalence and Correlates of Phenazine Resistance in Culturable Bacteria from a Dryland Wheat Field. Applied and Environmental Microbiology, 88 (6). Art. No. e02320-21. ISSN 0099-2240. PMCID PMC8939311. doi:10.1128/aem.02320-21. https://resolver.caltech.edu/CaltechAUTHORS:20211129-175740276

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Abstract

Phenazines are a class of bacterially produced redox-active natural antibiotics that have demonstrated potential as a sustainable alternative to traditional pesticides for the biocontrol of fungal crop diseases. However, the prevalence of bacterial resistance to agriculturally relevant phenazines is poorly understood, limiting both the understanding of how these molecules might shape rhizosphere bacterial communities and the ability to perform a risk assessment for off-target effects. Here, we describe profiles of susceptibility to the antifungal agent phenazine-1-carboxylic acid (PCA) across more than 100 bacterial strains isolated from a wheat field where PCA producers are indigenous and abundant. We found that Gram-positive bacteria are typically more sensitive to PCA than Gram-negative bacteria, and there was significant variability in susceptibility both within and across phyla. Phenazine-resistant strains were more likely to be isolated from the wheat rhizosphere, where PCA producers were also more abundant, compared to bulk soil. Furthermore, PCA toxicity was pH-dependent for most susceptible strains and broadly correlated with PCA reduction rates, suggesting that uptake and redox-cycling were important determinants of phenazine toxicity. Our results shed light on which classes of bacteria are most likely to be susceptible to phenazine toxicity in acidic or neutral soils. In addition, the taxonomic and phenotypic diversity of our strain collection represents a valuable resource for future studies on the role of natural antibiotics in shaping wheat rhizosphere communities.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1128/aem.02320-21DOIArticle
https://doi.org/10.1101/2021.11.23.469799DOIDiscussion Paper
https://www.ncbi.nlm.nih.gov/bioproject/?term=PRJNA521160Related ItemData
ORCID:
AuthorORCID
Perry, Elena K.0000-0002-7151-1479
Newman, Dianne K.0000-0003-1647-1918
Alternate Title:Phenazine resistance in wheat rhizosphere community
Additional Information:© 2022 American Society for Microbiology. Received 23 November 2021; Accepted 1 February 2022; Accepted manuscript posted online 9 February 2022; Published 22 March 2022. We thank Linda Thomashow and David Weller of the USDA Agricultural Research Service for providing the wheat rhizosphere and soil samples used in this study, and the members of the Newman lab for helpful feedback throughout the process of designing and analyzing the results of the PCA resistance screen. We also thank Zevin Condiotte for assistance with the initial rounds of testing the design of the PCA resistance screen and Richard Horak for assistance with extracting genomic DNA. This material is based upon work supported by the National Science Foundation Graduate Research Fellowship under Grant no. DGE‐1745301. This work was also supported by grants to D.K.N. from the ARO (W911NF-17-1-0024), NIH (1R01AI127850-01A1), and the Resnick Sustainability Institute at Caltech. We also thank the Doren Family Foundation for their support. We declare no conflict of interest. Data availability: The metagenomic sequencing data generated in this study were deposited in the Sequence Read Archive (SRA) under accession PRJNA521160.
Group:Resnick Sustainability Institute
Funders:
Funding AgencyGrant Number
NSF Graduate Research FellowshipDGE-1745301
Army Research Office (ARO)W911NF-17-1-0024
NIH1R01AI127850-01A1
Resnick Sustainability InstituteUNSPECIFIED
Doren Family FoundationUNSPECIFIED
Subject Keywords:correlates, dryland wheat, efflux pumps, phenazines, resistance, rhizosphere, toxicity
Issue or Number:6
PubMed Central ID:PMC8939311
DOI:10.1128/aem.02320-21
Record Number:CaltechAUTHORS:20211129-175740276
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20211129-175740276
Official Citation:erry EK, Newman DK. Prevalence and Correlates of Phenazine Resistance in Culturable Bacteria from a Dryland Wheat Field. Appl Environ Microbiol. 2022 Mar 22;88(6):e0232021. doi: 10.1128/aem.02320-21.
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:112067
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:29 Nov 2021 18:16
Last Modified:06 Apr 2022 18:58

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