Gold nanoclusters cause selective light-driven biochemical catalysis in living nano-biohybrid organisms

Living nano-biohybrid organisms or nanorgs combine the specificity and well-designed surface chemistry of an enzyme catalyst site, with the strong light absorption and efficient charge injection (for biocatalytic reaction) from inorganic materials. Previous efforts in harvesting sunlight for renewable and sustainable photochemical conversion of inexpensive feedstocks to biochemicals using nanorgs focused on the design of semiconductor nanoparticles or quantum dots (QDs). However, metal nanoparticles and nanoclusters (NCs), such as gold (Au), offer strong light absorption properties and biocompatibility for potential application in living nanorgs. Here we show that optimized, sub-1 nanometer Au NCs-nanorgs can carry out selective biochemical catalysis with high turnover number (10⁸ mol mol^-1 of cells) and turnover frequency (>2 × 10⁷ h^-1). While the differences of size, light absorption, and electrochemical properties between these NCs (with 18, 22, and 25 atoms) are small, large differences in their light-activated properties dictate that 22 atom Au NCs are best suited for forming living nanorgs to drive photocatalytic ammonia production from air. Based on our experiments, these Au₂₂ NC-nanorgs demonstrate 29.3% quantum efficiency of converting absorbed photons to the desired chemical, and 12.9% efficiency of photon-to-fuel conversion based on energy input-output. Further, by comparing the light-driven ammonia production yield between strains producing Mo-Fe nitrogenase with and without histidine tags, we demonstrate that preferential coupling of Au NCs to the nitrogenase through Au-histidine interactions is crucial for effective electron transfer and subsequent product generation. Together, these results provide the design rules for forming Au NCs-nanorgs and can have important implications for carrying out light-driven biochemical catalysis for renewable solar fuel generation.