Covalent attachment of photosynthetic reaction centers to hydrogen-bonded organic semiconductors for bio-optoelectronic applications

Hydrogen-bonded pigments are a class of organic colorants, which features many natural-origin molecules that have been used for centuries, as well as numerous mass-produced industrial synthetic compounds used in applications as various as out- door paints, cosmetics, and printing inks. Their widespread use in the dye and pigment industry is motivated by three favorable properties: low-cost production, excellent stability, and low toxicity, with some of them considered less hazardous than even water-soluble food dyes. Recently, H-bonded pigments have emerged also as promising organic semiconductors, with epindolidione (EPI) and quinacridone (QNC) demonstrating hole mobility in the range of 0.1-1 cm2 V-1 s-1 and outstanding operational stability in both air and in aqueous environments with pH 3-10 [1]. This latter finding is motivating for deploying these materials in applications requiring direct interfacing with biological ''wet'' environments. Their N-H and C=O functional groups are the "chemical handles" that are in principle amenable for direct bioconjugation. A proper combination of the photosynthetic reaction center (RC), the pivotal protein in photosynthesis, with engineered materials such as metals or inorganic semiconductor electrodes, has attracted great attention for the building of new versatile hybrid devices for solar energy conversion. Here we propose a covalent approach able to stably anchor RCs onto evaporated thin films of EPI and QNC. The N-H functional group of these molecules in thin film reacts spontaneously with N-hydroxysuccinimide functionalized linkers as disuccinimidyl suberate. The protruding linkers are then used to covalently bind the lysines residues of the Rb. sphaeroides RC, by forming an amide linkage (right panel in the figure). Our protocol is shown to preserve the semiconducting properties of the pigments while maintaining the protein's photoactivity. Multiple reflection IR spectroscopy and AFM demonstrated the effective covalent binding and the robustness of the protein anchoring even after buffer washing. Furthermore, RC charge recombination kinetic measurements confirmed the full functionality of bioconjugated proteins ruling out any possible hindering effect from the organic films. As key results of our work, we show that semiconductors preserve their favorable electrical properties and the proposed photoconductor device operates under water, before and after RCs anchoring. These are enabling steps for using H-bonded pigments as a platform for multifunctional bioelectronics devices.