Rational design of artificial redox-mediating systems toward upgrading photobioelectrocatalysis

Abstract

Photobioelectrocatalysis has recently attracted particular research interest owing to the possibility to achieve sunlight-driven biosynthesis, biosensing, power generation, and other niche applications. However, physiological incompatibilities between biohybrid components lead to poor electrical contact at the biotic-biotic and biotic-abiotic interfaces. Establishing an electrochemical communication between these different interfaces, particularly the biocatalyst-electrode interface, is critical for the performance of the photobioelectrocatalytic system. While different artificial redox mediating approaches spanning across interdisciplinary research fields have been developed in order to electrically wire biohybrid components during bioelectrocatalysis, a systematic understanding on physicochemical modulation of artificial redox mediators is further required. Herein, we review and discuss the use of diffusible redox mediators and redox polymer-based approaches in artificial redox-mediating systems, with a focus on photobioelectrocatalysis. The future possibilities of artificial redox mediator system designs are also discussed within the purview of present needs and existing research breadth.

Keywords: Biohybrid; Diffusible redox mediators; Electrical wiring; Photobioelectrochemical cells; Redox polymers.

Fig. 1

Schematic representation of the photobioelectrocatalytic mechanism; generation of charge separations in photosystems by harvesting light and the consequent conversion of that energy to a electrical energy or, b chemical energy, via redox catalysis

Fig. 2

Schematic representations of EET; a E-DET via membrane proteins, b E-DET via intrinsic conductive molecular wires (e.g., pili, filaments), c E-MET via endogenous or exogenous diffusible redox mediators, d E-MET via redox polymers/matrices, e electron exchange during E-MET

Fig. 3

Common diffusible redox mediators; a–g benzoquinone derivatives, h–k benzoquinone derivatives with fused aromatic centers, l–p redox dye species

Fig. 4

Schematic representation of a PSI-Au electrode biohybrid, where the PSI forms a monolayer on the Au surface by the bis-aniline cross-linkage. The crosslinks provide the electric contact at the biotic-abiotic interface, while ascorbic acid and DCPIP respectively function as electron donor and internal redox mediator. Adapted with permission from O. Yehezkeli, O. Wilner, R. Tel-Vered, D. Roizman-Sade, R. Nechushtai, and I. Willner. Generation of Photocurrents by Bis-aniline-Cross-Linked Pt Nanoparticle/Photosystem I Composites on Electrodes. J. Phys. Chem. B 2010, 114, 45, 14,383–14,388. Copyright (2010) American Chemical Society

Fig. 5

Bipyridinium diffusible redox mediators; a 4,4’-bipyridinium salts, b 2,2’-bipyridinium salts, c viologen-bound cationic porphyrins ZnP(C_nV)₄, d–f pyropheophorbide-a structures conjugated with viologen

Fig. 6

Schematic representation of the electron mediation at the MoFeP enzyme-CdS biotic abiotic interface; a oligophenylenes as mediators, b cobaltocene as mediator. Adapted with permission from A. Harris, S. Roy, S. Ganguly, A. Parameswar, F. Lucas, A. Holewinski, A. Goodwin and J. Cha. Investigating the use of conducting oligomers and redox molecules in CdS–MoFeP biohybrids. NanoscaleAdv.,2021,3,1392. Published by The Royal Society of Chemistry

Fig. 7

Schematic representation of redox mediation by pyocyanin biosynthesized by P. aeruginosa. Adapted with permission from G. Ren, Y. Sun, Y. Ding, A. Lu, Y. Li, C. Wang, and H. Ding, Enhancing extracellular electron transfer between Pseudomonas aeruginosa PAO1 and light-driven semiconducting birnessite. Bioelectrochemistry, 2018, 123, 233–240. Copyright (2018) Elsevier

Fig. 8

Redox polymers by a structural classification; a schematic representation of generalized electron transfer in a branched redox polymer, b–e examples of branched redox polymers, f schematic representation of generalized electron transfer in an unbranched redox polymer, g–j examples of unbranched redox polymers

Fig. 9

Schematic representation of electron transfer in the Z-scheme; a during natural photosynthesis, b semi-artificial Z-scheme, where PSII-PSI interface is redox mediated by Os-redox polymers. Adapted with permission from T. Kothe, N. Plumeré, A. Badura, M. Nowaczyk, D. Guschin, M. Rçgner, and W. Schuhmann, Combination of a Photosystem 1‐Based Photocathode and a Photosystem 2‐Based Photoanode to a Z‐Scheme Mimic for Biophotovoltaic Applications. Angew. Chem., Int. Ed., 2013, 52, 14,233–14,236. Copyright (2013) Wiley

Fig. 10

Schematic representation of electron transfer at the PSII-diketopyrrolopyrrole dye interface, where both biological entities harvest solar energy, en route to the hydrogenase enzyme. Adapted with permission from K.P. Sokol, W. E. Robinson, J. Warnan, N. Kornienko, M. M. Nowaczyk, A. Ruff, J. Z. Zhang and E. Reisner. Bias-free photoelectrochemical water splitting with photosystem II on a dye-sensitized photoanode wired to hydrogenase. Nat. Energy, 2018, 3, 944–951. Copyright (2018) Nature

Fig. 11

Schematic representation of the photobioelectrochemical enzymatic electrode incorporating a glucose oxidase-PSI interface electrically wired by an Os-based redox polymer, and the PSI-ITO electrode interface electrically wired by pyrroloquinolinequinone. Adapted with permission from A. Efratil, C. Lu, D. Michaeli, R. Nechushtai, S. Alsaoub, W. Schumann and I. Willner. Assembly of photo-bioelectrochemical cells using photosystem I-functionalized electrodes. Nat. Energy, 2016, 1, 15,021. Copyright (2016) Springer Nature

Fig. 12

Schematics of electron transfer; a at the PQQ glucose dehydrogenase-TiO₂ interface redox mediated by polymer PMSA1 represented in terms of energy levels. Adapted with permission from M. Riedel, F. Lisdat, Integration of Enzymes in Polyaniline-Sensitized 3D Inverse Opal TiO₂ Architectures for Light-Driven Biocatalysis and Light-to-Current Conversion, ACS Appl. Mater. Interfaces, 2018, 10, 267–277). Copyright (2018) American Chemical Society. b in a photobioelectrocatalytic fuel cell where the thylakoid-Au electrode interface and the bilirubin oxidase-Au electrode interface are respectively redox mediated by conductive poly 4-(4H-dithieno [3,2-b:2′,3′-d]pyrol-4-yl) aniline crosslinked to cytochrome C and poly[5-(4H-dithieno [3,2-b:2′,3′-d]pyrol-4-yl) naphtalene-1-amine]. Adapted with permission from E. Cevika, B. Carbas, M. Senel, H. Yildiz, Construction of conducting polymer/cytochrome C/thylakoid membrane-based photo-bioelectrochemical fuel cells generating high photocurrent via photosynthesis, Biosens. Bioelectron., 2018, 113, 25–31. Copyright (2018) Elsevier