Z-scheme solar water splitting via self-assembly of photosystem I-catalyst hybrids in thylakoid membranes

Nature's solar energy converters, the Photosystem I (PSI) and Photosystem II (PSII) reaction center proteins, flawlessly manage photon capture and conversion processes in plants, algae, and cyanobacteria to drive oxygenic water-splitting and carbon fixation. Herein, we utilize the native photosynthetic Z-scheme electron transport chain to drive hydrogen production from thylakoid membranes by directional electron transport to abiotic catalysts bound at the stromal end of PSI. Pt-nanoparticles readily self-assemble with PSI in spinach and cyanobacterial membranes as evidenced by light-driven H2 production in the presence of a mediating electron shuttle protein and the sacrificial electron donor sodium ascorbate. EPR characterization confirms placement of the Pt-nanoparticles on the acceptor end of PSI. In the absence of sacrificial reductant, H2 production at PSI occurs via coupling to light-induced PSII O2 evolution as confirmed by correlation of catalytic activity to the presence or absence of the PSII inhibitor DCMU. To create a more sustainable system, first-row transition metal molecular cobaloxime and nickel diphosphine catalysts were found to perform photocatalysis when bound in situ to cyanobacterial thylakoid membranes. Thus, the self-assembly of abiotic catalysts with photosynthetic membranes demonstrates a tenable method for accomplishing solar overall water splitting to generate H2, a renewable and clean fuel. This work benchmarks a significant advance toward improving photosynthetic efficiency for solar fuel production.