Genetically dissecting the electron transport chain of a soil bacterium reveals a generalizable mechanism for biological phenazine-1-carboxylic acid oxidation

The capacity for bacterial extracellular electron transfer via secreted metabolites is widespread in natural, clinical, and industrial environments. Recently, we discovered biological oxidation of phenazine-1-carboxylic acid (PCA), the first example of biological regeneration of a naturally produced...

Full description

Saved in:
Bibliographic Details
Published in:PLoS genetics 2024-05, Vol.20 (5), p.e1011064-e1011064
Main Authors: Tsypin, Lev M Z, Saunders, Scott H, Chen, Allen W, Newman, Dianne K
Format: Article
Language:English
Subjects:
Acids
Anaerobic respiration
Analysis
Bacteria
Biology and Life Sciences
Carboxylic acids
Catalytic subunits
Cytoplasmic membranes
Dimethyl sulfoxide
Electron transfer
Electron transport
Electron transport chain
Electrons
Enzymes
Genetic engineering
Heterocyclic compounds
Identification and classification
Medicine and Health Sciences
Metabolites
Methods
Nitrates
Oxidation
Oxidation-reduction reaction
Phenazine-1-carboxylic acid
Physical Sciences
Properties
Quinone
Respiration
Soil microbiology
Soil microorganisms
Trimethylamine
Trimethylamine-N-oxide
Citations: Items that this one cites
Online Access:Get full text
Tags: Add Tag
No Tags, Be the first to tag this record!
Description
Summary:The capacity for bacterial extracellular electron transfer via secreted metabolites is widespread in natural, clinical, and industrial environments. Recently, we discovered biological oxidation of phenazine-1-carboxylic acid (PCA), the first example of biological regeneration of a naturally produced extracellular electron shuttle. However, it remained unclear how PCA oxidation was catalyzed. Here, we report the mechanism, which we uncovered by genetically perturbing the branched electron transport chain (ETC) of the soil isolate Citrobacter portucalensis MBL. Biological PCA oxidation is coupled to anaerobic respiration with nitrate, fumarate, dimethyl sulfoxide, or trimethylamine-N-oxide as terminal electron acceptors. Genetically inactivating the catalytic subunits for all redundant complexes for a given terminal electron acceptor abolishes PCA oxidation. In the absence of quinones, PCA can still donate electrons to certain terminal reductases, albeit much less efficiently. In C. portucalensis MBL, PCA oxidation is largely driven by flux through the ETC, which suggests a generalizable mechanism that may be employed by any anaerobically respiring bacterium with an accessible cytoplasmic membrane. This model is supported by analogous genetic experiments during nitrate respiration by Pseudomonas aeruginosa.
ISSN:1553-7404
1553-7390
1553-7404
DOI:10.1371/journal.pgen.1011064