Strain- and Substrate-Dependent Redox Mediator and Electricity Production by Pseudomonas aeruginosa

Abstract

Pseudomonas aeruginosa is an important, thriving member of microbial communities of microbial bioelectrochemical systems (BES) through the production of versatile phenazine redox mediators. Pure culture experiments with a model strain revealed synergistic interactions of P. aeruginosa with fermenting microorganisms whereby the synergism was mediated through the shared fermentation product 2,3-butanediol. Our work here shows that the behavior and efficiency of P. aeruginosa in mediated current production is strongly dependent on the strain of P. aeruginosa. We compared levels of phenazine production by the previously investigated model strain P. aeruginosa PA14, the alternative model strain P. aeruginosa PAO1, and the BES isolate Pseudomonas sp. strain KRP1 with glucose and the fermentation products 2,3-butanediol and ethanol as carbon substrates. We found significant differences in substrate-dependent phenazine production and resulting anodic current generation for the three strains, with the BES isolate KRP1 being overall the best current producer and showing the highest electrochemical activity with glucose as a substrate (19 A cm ؊2 with ϳ150 g ml ؊1 phenazine carboxylic acid as a redox mediator). Surprisingly, P. aeruginosa PAO1 showed very low phenazine production and electrochemical activity under all tested conditions. IMPORTANCEMicrobial fuel cells and other microbial bioelectrochemical systems hold great promise for environmental technologies such as wastewater treatment and bioremediation. While there is much emphasis on the development of materials and devices to realize such systems, the investigation and a deeper understanding of the underlying microbiology and ecology are lagging behind. Physiological investigations focus on microorganisms exhibiting direct electron transfer in pure culture systems. Meanwhile, mediated electron transfer with natural redox compounds produced by, for example, Pseudomonas aeruginosa might enable an entire microbial community to access a solid electrode as an alternative electron acceptor. To better understand the ecological relationships between mediator producers and mediator utilizers, we here present a comparison of the phenazine-dependent electroactivities of three Pseudomonas strains. This work forms the foundation for more complex coculture investigations of mediated electron transfer in microbial fuel cells. Bioelectrochemical systems (BES), including their most important variant, the microbial fuel cell (MFC), are rapidly developing and promising technologies for renewable energy production and wastewater treatment, among other applications (1, 2). The MFC technology aims at generating electrical current through extracellular transfer of electrons, which microorganisms liberate from organic substrates. Microorganisms oxidize organic compounds, and the electrons from the intracellular electron transport chains are transferred to an external electron acceptor (i.e., an anode poised at a suitable potential) (3). One of the challenges facing MFC performanc...

Construction of an Electron Transfer Mediator Pathway for Bioelectrosynthesis by Escherichia coli

“…In contrast to E. coli BA102, a significant pair of redox peak was observed from the bioelectrochemical system inoculated with E. coli-phz. Figure 2A showed an oxidation peak in the range of 0.0 to −0.20 V and reduction peak between −0.30 and −0.50 V, which agreed with the broad PCA redox peak system determined for P. aeruginosa PA14 (Bosire et al, 2016). The results indicate that self-excreted PCA functioned as electron mediator in the bioelectrochemical system inoculated with E. coli-phz, which achieved the utilization of electrons and redox reaction in the bioelectrochemical system inoculated with E. coli-phz.…”

“…Phenazine-1-carboxylic acid (PCA) is a type of redox-active phenazine and is produced by species of Pseudomonas and Actinomycetes. PCA possesses a relatively low for redox potential (E = −0.24 V vs. Ag/AgClsat) and is primarily involved in reversible redox cycling under oxygen-limited conditions (Bosire et al, 2016;Bosire and Rosenbaum, 2017). Reportedly, PCA rather than pyocyanin may be responsible for electron transfer from the cathode to Pseudomonas aeruginosa PA14 (Bosire and Rosenbaum, 2017).…”

Electrochemical Potential Influences Phenazine Production, Electron Transfer and Consequently Electric Current Generation by Pseudomonas aeruginosa

“…The mean formal potential of PS1 was the same as the formal potential of PCA standards [-0.24 V; (Bosire et al, 2016)]. Indeed, PCA was detected via HPLC as the dominating phenazine species in all experiments.…”

Estimation of pathogenic potential of an environmental Pseudomonas aeruginosa isolate using comparative genomics

“…The P. aeruginosa KRP1 isolate was so far investigated only towards its ability to produce increased levels of current in bioelectrochemical systems [80] and to dominate such systems, when inoculated with a mixed community of microbes [62]. Thereby, its main success for function in bioelectrochemical systems and likely also a factor in its dominance of microbial communities, is its enhanced production of phenazines [80]. These redox active natural products mediate the electron transfer to a provided electrode and act as antimicrobials through the generation of reactive oxygen species.…”