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Nitrate Reduction Stimulates and Is Stimulated by Phenazine-1-Carboxylic Acid Oxidation by Citrobacter portucalensis MBL

Tsypin, Lev M. and Newman, Dianne K. (2021) Nitrate Reduction Stimulates and Is Stimulated by Phenazine-1-Carboxylic Acid Oxidation by Citrobacter portucalensis MBL. mBio, 12 (4). Art. No. e02265-21. ISSN 2150-7511. doi:10.1128/mBio.02265-21. https://resolver.caltech.edu/CaltechAUTHORS:20210607-115053770

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Abstract

Phenazines are secreted metabolites that microbes use in diverse ways, from quorum sensing to antimicrobial warfare to energy conservation. Phenazines are able to contribute to these activities due to their redox activity. The physiological consequences of cellular phenazine reduction have been extensively studied, but the counterpart phenazine oxidation has been largely overlooked. Phenazine-1-carboxylic acid (PCA) is common in the environment and readily reduced by its producers. Here, we describe its anaerobic oxidation by Citrobacter portucalensis strain MBL, which was isolated from topsoil in Falmouth, MA, and which does not produce phenazines itself. This activity depends on the availability of a suitable terminal electron acceptor, specifically nitrate. When C. portucalensis MBL is provided reduced PCA and nitrate, it oxidizes the PCA at a rate that is environmentally relevant. We compared this terminal electron acceptor-dependent PCA-oxidizing activity of C. portucalensis MBL to that of several other gammaproteobacteria with various capacities to respire nitrate. We found that PCA oxidation by these strains in a nitrate-dependent manner is decoupled from growth and strain dependent. We infer that bacterial PCA oxidation is widespread and genetically determined. Notably, oxidizing PCA enhances the rate of nitrate reduction to nitrite by C. portucalensis MBL beyond the stoichiometric exchange of electrons from PCA to nitrate, which we attribute to C. portucalensis MBL’s ability to also reduce oxidized PCA, thereby catalyzing a complete PCA redox cycle. This bidirectionality highlights the versatility of PCA as a biological redox agent.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1128/mBio.02265-21DOIArticle
https://doi.org/10.1101/2021.06.04.447179DOIDiscussion Paper
https://github.com/ltsypin/Cportucalensis_observationRelated ItemCode
ORCID:
AuthorORCID
Tsypin, Lev M.0000-0002-0642-8468
Newman, Dianne K.0000-0003-1647-1918
Alternate Title:C. portucalensis MBL links PCA and nitrate redox cycles
Additional Information:© 2021 Tsypin and Newman. This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license. Received 27 July 2021; Accepted 4 August 2021; Published 31 August 2021. We thank the members of the Newman lab, and especially Scott Saunders, Darcy McRose, Avi Flamholz, John Ciemniecki, Chelsey VanDrisse, and Justin Bois for their insight and helpful discussions throughout this work. We are grateful to Nathan Dalleska at the Water and Environment Laboratory at Caltech for training L.M.T. on the Dionex instrument and providing a facility for analytical chemistry. L.M.T. was supported by the Rosen Endowment Fellowship at Caltech and the National Science Foundation Graduate Research Fellowship (DGE‐1745301). Additional support to D.K.N. came from NIH (1R01AI127850-01A1 and 1R01HL152190-01) and ARO (W911NF-17-1-0024) grants.
Group:Rosen Bioengineering Center
Funders:
Funding AgencyGrant Number
Donna and Benjamin M. Rosen Bioengineering CenterUNSPECIFIED
NSF Graduate Research FellowshipDGE‐1745301
NIH1R01AI127850-01A1
NIH1R01HL152190-01
Army Research Office (ARO)W911NF-17-1-0024
Subject Keywords:Citrobacter, biological oxidation, denitrification, nitrate reduction, phenazines, redox cycling
Issue or Number:4
DOI:10.1128/mBio.02265-21
Record Number:CaltechAUTHORS:20210607-115053770
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20210607-115053770
Official Citation:Tsypin LM, Newman DK. 2021. Nitrate reduction stimulates and is stimulated by phenazine-1-carboxylic acid oxidation by Citrobacter portucalensis MBL. mBio 12:e02265-21. https://doi.org/10.1128/mBio.02265-21.
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:109415
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:07 Jun 2021 22:08
Last Modified:13 Sep 2021 18:47

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