Phenazines as model low-midpoint potential electron shuttles for photosynthetic bioelectrochemical systems

Clifford, Eleanor R.; Bradley, Robert W.; Wey, Laura T.; Lawrence, Joshua M.; Chen, Xiaolong; Howe, Christopher J.; Zhang, Jenny Z.

Abstract

Bioelectrochemical approaches for energy conversion rely on efficient wiring of natural electron transport chains to electrodes. However, state-of-the-art exogenous electron mediators give rise to significant energy losses and, in the case of living systems, long-term cytotoxicity. Here, we explored new selection criteria for exogenous electron mediation by examining phenazines as novel low-midpoint potential molecules for wiring the photosynthetic electron transport chain of the cyanobacteriumSynechocystissp. PCC 6803 to electrodes. We identified pyocyanin (PYO) as an effective cell-permeable phenazine that can harvest electrons from highly reducing points of photosynthesis. PYO-mediated photocurrents were observed to be 4-fold higher than mediator-free systems with an energetic gain of 200 mV compared to the common high-midpoint potential mediator 2,6-dichloro-1,4-benzoquinone (DCBQ). The low-midpoint potential of PYO led to O2reduction side-reactions, which competed significantly against photocurrent generation; the tuning of mediator concentration was important for outcompeting the side-reactions whilst avoiding acute cytotoxicity. DCBQ-mediated photocurrents were generally much higher but also decayed rapidly and were non-recoverable with fresh mediator addition. This suggests that the cells can acquire DCBQ-resistance over time. In contrast, PYO gave rise to steadier current enhancement despite the co-generation of undesirable reactive oxygen species, and PYO-exposed cells did not develop acquired resistance. Moreover, we demonstrated that the cyanobacteria can be genetically engineered to produce PYO endogenously to improve long-term prospects. Overall, this study established that energetic gains can be achievedviathe use of low-potential phenazines in photosynthetic bioelectrochemical systems, and quantifies the factors and trade-offs that determine efficacious mediation in living bioelectrochemical systems.

Citation

Clifford, E. R., Bradley, R. W., Wey, L. T., Lawrence, J. M., Chen, X., Howe, C. J., & Zhang, J. Z. (2021). Phenazines as model low-midpoint potential electron shuttles for photosynthetic bioelectrochemical systems. Chemical Science, 12(9), 3328-3338. https://doi.org/10.1039/d0sc05655c

• Journal Article Type: Article
• Acceptance Date: Jan 14, 2021
• Online Publication Date: Jan 15, 2021
• Publication Date: Mar 7, 2021
• Deposit Date: Aug 3, 2023
• Publicly Available Date: Aug 3, 2023
• Journal: Chemical Science
• Print ISSN: 2041-6520
• Electronic ISSN: 2041-6539
• Publisher: Royal Society of Chemistry
• Peer Reviewed: Peer Reviewed
• Volume: 12
• Issue: 9
• Pages: 3328-3338
• DOI: https://doi.org/10.1039/d0sc05655c
• Public URL: https://nottingham-repository.worktribe.com/output/23787283
• Publisher URL: https://pubs.rsc.org/en/content/articlelanding/2021/sc/d0sc05655c