Sustaining Electron Transfer Pathways Extends Biohybrid Photoelectrode Stability to Years

Abstract

The exploitation of natural photosynthetic enzymes in semi-artificial devices constitutes an attractive and potentially sustainable route for the conversion of solar energy into electricity and solar fuels. However, the stability of photosynthetic proteins after incorporation in a biohybrid architecture typically limits the operational lifetime of biophotoelectrodes to a few hours. Here, we demonstrate ways to greatly enhance the stability of a mesoporous electrode coated with the RC-LH1 photoprotein from Rhodobacter sphaeroides. By preserving electron transfer pathways, we extended operation under continuous high-light to 33 days, and operation after storage to over two years. Coupled with large photocurrents that reached peak values of 4.6 mA cm À 2 , the optimized biophotoelectrode produced a cumulative output of 86 C cm À 2 , the largest reported performance to date. Our results demonstrate that the factor limiting stability is the architecture surrounding the photoprotein, and that biohybrid sensors and photovoltaic devices with operational lifetimes of years are feasible.

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

“…Investigations in situ and in operandum are crucial for the rational design of high-performing biohybrids, particularly in the context of recent and more complex benchmark architectures that drive large photocurrent densities but encounter multiple loss channels from short circuits, electron transfer bottlenecks, and excitation quenching. 4,[22][23][24][25] In this work, we utilized a combined spectroelectrochemical instrument, based on a ms/ms pump-probe Joliot-type spectrophotometer, to measure the redox states of Rba sphaeroides RC-LH1 complexes adsorbed on a semi-transparent mesoporous indium tin oxide electrode (mITO -Figure 1D). By simultaneously recording photocurrents and spectrally derived functional bRC oxidation states, kinetic bottlenecks and loss processes were identified at various stages of excitation and electron transfer in this mITO|cyt c|RC-LH1 electrode.…”

“…An applied potential of +160 mV vs. SHE was used to optimally drive a photocathodic current, as described previously for cyt c mediated bRC photocathodes. 4,26 Excitation was provided either by an LED peaking at 590 nm, or by 5 ns laser flashes at 532 nm (Figures 2A and 2B). Photooxidation of the bRC primary electron donor was monitored at 865 nm (e 865 = 112 G 6 mM À1 cm À1 , see Straley et al 27 ), with simultaneous recording of photoinduced electron transfer at the electrode interface using chronoamperometry.…”

“…1 This innate efficiency has driven interest in the direct utilization of natural and engineered pigment-protein complexes in biohybrid devices. [2][3][4] A challenge of using a photosynthetic RC as a primary photovoltaic component is the retention of the mechanisms that underpin a high quantum efficiency of charge separation when the RC is incorporated into a device.…”

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

“…Second, to support a photocurrent over multiple RC turnovers, cyt c molecules have to remain largely confined to the plane of the electrode surface during fabrication and operation. That this occurs is supported by studies that have shown that the photocurrents remain stable for hours after free cyt c is removed from the electrolyte. − Third, the orientation of the RC on the electrode may occlude cyt c access, restricting the rate of P870 + reduction . These differences result in RC electron transfer turnover frequencies (TOF) that are typically on the order of 10 to 150 e – s –1 . , 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. , …”

“…That this occurs is supported by studies that have shown that the photocurrents remain stable for hours after free cyt c is removed from the electrolyte. 23 − 25 Third, the orientation of the RC on the electrode may occlude cyt c access, restricting the rate of P870 + reduction. 26 These differences result in RC electron transfer turnover frequencies (TOF) that are typically on the order of 10 to 150 e – s –1 .…”