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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.

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Authors

Eleanor R. Clifford

Robert W. Bradley

Laura T. Wey

Joshua M. Lawrence

XIAOLONG CHEN XIAOLONG.CHEN@NOTTINGHAM.AC.UK
Assistant Professor in Sustainable Engineering

Christopher J. Howe

Jenny Z. Zhang



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

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