Investigating the interaction between Shewanella oneidensis and phenazine 1-carboxylic acid in the microbial electrochemical processes

Abstract

Many exoelectrogens utilize small redox mediators for extracellular electron transfer (EET). Notable examples include Shewanella species, which synthesize flavins, and Pseudomonas species, which produce phenazines. In natural and engineered environments, redox-active metabolites from different organisms coexist. The interaction between Shewanella oneidensis and phenazine 1-carboxylic acid (PCA, a representative phenazine compound) was investigated to demonstrate exoelectrogens utilizing metabolites secreted by other organisms as redox mediators. After 24 h in a reactor with and without added PCA (1 μM), the anodic current generated by Shewanella was 235 ± 11 and 51.7 ± 2.8 μA, respectively. Shewanella produced oxidative current approximately three times as high with medium containing PCA as with medium containing the same concentration of riboflavin. PCA also stimulated inward EET in Shewanella. The strong effect of PCA on EET was attributed to its enrichment at the biofilm/electrode interface. The PCA voltammetric peak heights with a Shewanella bioanode were 25–30 times higher than under abiotic conditions. The electrochemical properties of PCA were also altered by the transition from two-electron to single-electron electrochemistry, which suggests PCA was bound between the electrode and cell surface redox proteins. This behavior would benefit electroactive bacteria, which usually dwell in open systems where mediators are present in low concentrations. Like flavins, PCA can be immobilized under both bioanode and biocathode conditions but not under metabolically inactive conditions. Shewanella rapidly transfers electrons to PCA via its Mtr pathway. Compared with wild-type Shewanella, the PCA reduction ability was decreased in gene knockout mutants lacking Mtr pathway cytochromes, especially in the mutants with severely undermined electrode-reduction capacities. These strains also lost the ability to immobilize PCA, even under current-generating conditions.