In situ time-resolved spectroelectrochemistry reveals limitations of biohybrid photoelectrode performance

• Published in: Joule Vol. 7; no. 3; pp. 529 - 544
• Main Authors: Nawrocki, Wojciech J., Jones, Michael R., Frese, Raoul N., Croce, Roberta, Friebe, Vincent M.
• Format: Journal Article
• Language: English
• Published: Elsevier Inc 15.03.2023; Elsevier
• Subjects: Analytical chemistry; bioelectrochemistry; biohybrid; biophotoelectrochemistry; biosensing; Chemical Sciences; fluorescence; photosynthesis; pump-probe spectroscopy; reaction center; solar energy conversion; spectroelectrochemistry; solar energy conversion; bioelectrochemistry; biohybrid; photosynthesis; fluorescence; pump-probe spectroscopy; biophotoelectrochemistry; spectroelectrochemistry; biosensing; reaction center
• ISSN: 2542-4351; 2542-4351
• DOI: 10.1016/j.joule.2023.02.015

Photosynthetic reaction centers catalyze the majority of solar energy conversion on the Earth. Under low-intensity illumination, this is achieved with a near-unity quantum efficiency, almost every absorbed photon producing a photochemical charge separation. Biohybrid technologies seek to capture the high efficiency of natural photoproteins by combining them with man-made electrodes. However, the transfer of photoproteins from their membrane environment into an abiotic architecture invariably results in efficiency losses. Here, we combined spectroscopy and analytical electrochemistry to identify the loss processes in a reaction-center-based biophotoelectrode. While over 90% efficient under low-intensity illumination, the biophotoelectrode efficiency dropped to ∼11% under high-intensity illumination. This loss stemmed from bottlenecks in electron transfer that rendered 60% of reaction centers inactive, as well as a short-circuiting of 73% of the separated charge from active reaction centers. The quantitative insights into loss processes presented in this work will be instrumental in shaping future rational design of biophotoelectrode devices. [Display omitted] •A protein-photoelectrode was investigated with spectroscopy and electrochemistry•We resolved electron flow and energy loss channels during biohybrid operation•Continuous intense irradiation exacerbated loss channels and compromised efficiency•The knowledge will help drive the rational design of more efficient biohybrids Solar energy fuels life in two ways: through photosynthesis, providing food for virtually all organisms on the Earth; and by generating electricity in photovoltaic devices. Biohybrid photoelectrodes combine the best of both worlds, coupling natural-light-driven photoenzymes with complex artificial materials in a bid to achieve sustainable, low-power tools. These may be used in a wide range of applications, from the production of solar fuels and value-added chemicals to electricity. However, bridging nature and technology often proves challenging, as biohybrid devices remain inefficient and unstable due to the creation of harmful side reactions. Using combined spectroscopic and electrochemical tools, we discover the origin of productivity losses during the operation of a state-of-the-art biohybrid device. A comprehensive quantification of loss processes is provided together with a blueprint for removal of these hurdles, bringing us closer to a zero-carbon economy driven by sustainable photoenzymes. In this work, we combined electrochemistry and spectroscopy to analyze electron flow through a protein-based photoelectrode. Such biophotoelectrodes form a platform for biosolar cells, where the processes of solar energy capture and conversion take place within natural photosynthetic proteins. We show that both non-native electron transfer to/from the photoenzyme and a variety of short-circuit loops limit biohybrid performance under operating conditions. The findings are crucial for the development of strategies to block loss channels and enable efficient protein-based biotechnologies.