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The transcription factors ActR and SoxR differentially affect the phenazine tolerance of Agrobacterium tumefaciens

Perry, Elena K. and Newman, Dianne K. (2019) The transcription factors ActR and SoxR differentially affect the phenazine tolerance of Agrobacterium tumefaciens. Molecular Microbiology, 112 (1). pp. 199-218. ISSN 0950-382X. PMCID PMC6615960. https://resolver.caltech.edu/CaltechAUTHORS:20190419-100142089

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Abstract

Bacteria in soils encounter redox‐active compounds, such as phenazines, that can generate oxidative stress, but the mechanisms by which different species tolerate these compounds are not fully understood. Here, we identify two transcription factors, ActR and SoxR, that play contrasting yet complementary roles in the tolerance of the soil bacterium Agrobacterium tumefaciens to phenazines. We show that ActR promotes phenazine tolerance by proactively driving expression of a more energy‐efficient terminal oxidase at the expense of a less efficient alternative, which may affect the rate at which phenazines abstract electrons from the electron transport chain (ETC) and thereby generate reactive oxygen species. SoxR, on the other hand, responds to phenazines by inducing expression of several efflux pumps and redox‐related genes, including one of three copies of superoxide dismutase and five novel members of its regulon that could not be computationally predicted. Notably, loss of ActR is far more detrimental than loss of SoxR at low concentrations of phenazines, and also increases dependence on the otherwise functionally redundant SoxR‐regulated superoxide dismutase. Our results thus raise the intriguing possibility that the composition of an organism's ETC may be the driving factor in determining sensitivity or tolerance to redox‐active compounds.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1111/mmi.14263DOIArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6615960/PubMed CentralArticle
ORCID:
AuthorORCID
Newman, Dianne K.0000-0003-1647-1918
Additional Information:© 2019 John Wiley & Sons. Issue Online: 09 July 2019; Version of Record online: 03 May 2019; Accepted manuscript online: 19 April 2019; Manuscript accepted: 13 April 2019. We thank all members of the Newman lab for helpful advice, discussions and feedback on the manuscript, and Clay Fuqua for generously providing pNPTS138. We also thank the Marine Biological Laboratory Microbial Diversity Course, Class of 2017, for assistance with screening transposon mutants. 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 the Millard and Muriel Jacobs Genetics and Genomics Laboratory at the California Institute of Technology (Caltech), the Caltech Electron Paramagnetic Resonance Spectroscopy Facility and grants to DKN from the ARO (W911NF‐17‐1‐0024) and NIH 341 (1R01AI127850‐01A1). Data availability statement: The data that support the findings of this study are available from the corresponding author upon reasonable request. Author contributions: EKP and DKN conceived the study and designed the experiments. EKP performed the experiments, analyzed and interpreted data and wrote the manuscript. DKN contributed to data interpretation, obtained funding and edited the manuscript.
Funders:
Funding AgencyGrant Number
NSF Graduate Research FellowshipDGE‐1745301
Millard and Muriel Jacobs Genetics and Genomics LaboratoryUNSPECIFIED
Army Research Office (ARO)W911NF-17-1-0024
NIH1R01AI127850-01A1
Subject Keywords:phenazines, oxidative stress, gene expression regulation, Agrobacterium tumefaciens, transcription factors, oxidation-reduction
Issue or Number:1
PubMed Central ID:PMC6615960
Record Number:CaltechAUTHORS:20190419-100142089
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20190419-100142089
Official Citation:Perry, E. K. and Newman, D. K. (2019), The transcription factors ActR and SoxR differentially affect the phenazine tolerance of Agrobacterium tumefaciens. Mol Microbiol, 112: 199-218. doi:10.1111/mmi.14263
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:94806
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:22 Apr 2019 22:53
Last Modified:03 Oct 2019 21:07

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