In situ Time-Resolved Spectroelectrochemistry Reveals Limitations of Biohybrid Photoelectrode Performance

Abstract

Photosynthetic reaction centres catalyse the majority of solar energy conversion on Earth. These pigment proteins achieve this goal with a near-unity quantum efficiency, transducing the energy of almost every absorbed photon into that of a charge separated state. Capturing the high efficiency of these natural proteins with man-made electrodes is the goal of biohybrid technologies such as biophotovoltaics, biofuel cells and biosensors. However, the removal of reaction centres from their natural cellular environment and their integration into an abiotic biohybrid architecture invariably introduces loss channels that compromise energy conversion efficiency. Here, we developed the combined use of spectroscopy and analytical electrochemistry to identify electron transfer bottlenecks, back-reactions and short-circuits that affect the performance of a bacterial reaction centre-based biophotoelectrode. We determined that the system was over 90% efficient under low intensity light but dropped to ~10% efficiency under intense continuous illumination. Limitations and loss processes included bottlenecks in electron transfer that rendered 62% of reaction centres inactive, as well as a short-circuiting of 73% of the photochemical product from active reaction centres. These findings will help shape rational design strategies for improving the performance of biohybrid devices and may be more broadly applied to other donor-acceptor type photocatalysts.

The Role of Electrostatic Binding Interfaces in the Performance of Bacterial Reaction Center Biophotoelectrodes

“…The biophotoelectrode activity was measured in an electrochemical cell containing 1.5 mM water-soluble ubiquinone-0 (Q 0 ) as an electron acceptor at an applied potential of +160 mV versus the standard hydrogen electrode (SHE). To exclude acceptor side (i.e., Q B /Q 0 ) limitations or short-circuits from controlling RC turnover, 4 the light intensity was lowered to 2.6 mW cm −2 such that peak photocurrents were in a linear regime with respect to the light intensity (Figure S2). To characterize dependence on its concentration, cyt c was titrated into the electrolyte, and, after equilibration, the photocurrent during 30 s of illumination was recorded (Figure 3a).…”

“…A principal challenge in the development of biohybrid RC photoelectrodes is achieving an efficient transfer of electrons from the electrode following photochemical charge separation within the RC. 4 The electrostatic interactions occurring between proteins and the electrode, 5 and between adjacent proteins, 6 form interfacial boundaries that may result in kinetic bottlenecks in the biohybrid electron transfer chain. 4 Improvement of the performance of biophotoelectrodes requires a better understanding of the impact of these interfaces on electron transfer from the electrode.…”

“…4 The electrostatic interactions occurring between proteins and the electrode, 5 and between adjacent proteins, 6 form interfacial boundaries that may result in kinetic bottlenecks in the biohybrid electron transfer chain. 4 Improvement of the performance of biophotoelectrodes requires a better understanding of the impact of these interfaces on electron transfer from the electrode.…”

“…21,24 These are only a fraction of the maximal RC TOF of up to 2300 e − s −1 that can be observed with purified proteins in solution. 20,27 A recent study using spectroelectrochemistry has shown that a limiting factor for RC turnover on an electrode is a kinetic bottleneck associated with cyt c-mediated electron transfer, 4 indicating a parameter that could be adjusted for better overall performance. In the present work, we characterized biophotoelectrode performance in response to modifications expected to impact the electrostatic interfaces between the RC and cyt c and cyt c and an electrode.…”