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Published November 24, 2020 | Supplemental Material + Submitted
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Bidirectional redox cycling of phenazine-1-carboxylic acid by Citrobacter portucalensis MBL drives increased nitrate reduction

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 or fumarate. When C. portucalensis MBL is provided reduced PCA and either nitrate or fumarate, it continuously oxidizes the PCA. We compared this terminal electron acceptor-dependent PCA-oxidizing activity of C. portucalensis MBL to that of several other γ-proteobacteria with varying capacities to respire nitrate and/or fumarate. We found that PCA oxidation by these strains in a fumarate-or nitrate-dependent manner is decoupled from growth and correlated with their possession of the fumarate or periplasmic nitrate reductases, respectively. We infer that bacterial PCA oxidation is widespread and genetically determined. Notably, reduced PCA enhances the rate of nitrate reduction to nitrite by C. portucalensis MBL beyond the stoichiometric prediction, 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.

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. Version 1 (November 24, 2020 - 08:09); this version posted November 25, 2020. We would like to 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 Environmental Analysis Center at Caltech for training LMT on the Dionex instrument and providing a facility for analytical chemistry. LMT was supported by the Rosen Endowment Fellowship at Caltech and the National Science Foundation Graduate Research Fellowship (DGE‐1745301). Additional support to DKN came from NIH (1R01AI127850-01A1 and 1R01HL152190-01) and ARO (W911NF-17-1-0024) grants.

Attached Files

Submitted - 2020.11.23.395335v2.full.pdf

Supplemental Material - media-1.pdf

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Additional details

Created:
August 20, 2023
Modified:
December 22, 2023