Semiartificial Photosynthetic Nanoreactors for H₂ Generation

A relatively unexplored energy source in synthetic cells is transmembrane electron transport, which like proton and ion transport can be light driven. Here, synthetic cells, called nanoreactors, are engineered for compartmentalized, semiartificial photosynthetic H₂ production by a Clostridium beijerinckii [FeFe]-hydrogenase (H₂ase). Transmembrane electron transfer into the nanoreactor was enabled by MtrCAB, a multiheme transmembrane protein from Shewanella oneidensis MR-1. On illumination, graphitic nitrogen-doped carbon dots (g-N-CDs) outside the nanoreactor generated and delivered photoenergized electrons to MtrCAB, which transferred these electrons to encapsulated H₂ase without requiring redox mediators. Compartmentalized, light-driven H₂ production was observed with a turnover frequency (TOF_H2ase) of 467 ± 64 h^-1 determined in the first 2 h. Addition of the redox mediator methyl viologen (MV) increased TOF_H2ase to 880 ± 154 h^-1. We hypothesize that the energetically "uphill" electron transfer step from MtrCAB to H₂ase ultimately limits the catalytic rate. These nanoreactors provide a scaffold to compartmentalize redox half reactions in semiartificial photosynthesis and inform on the engineering of nanoparticle-microbe hybrid systems for solar-to-chemical conversion.