Semiartificial Photosynthetic Nanoreactors for H2 Generation

• Published in: Journal of the American Chemical Society 2024-12
• Main Authors: Zhang, Huijie, Jaenecke, Jan, Bishara-Robertson, Imogen L, Casadevall, Carla, Redman, Holly J, Winkler, Martin, Berggren, Gustav, Plumeré, Nicolas, Butt, Julea N, Reisner, Erwin, Jeuken, Lars J C
• Format: Article
• Language: English
• ISSN: 1520-5126; 1520-5126
• DOI: 10.1021/jacs.4c12311

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 (TOFH2ase) of 467 ± 64 h-1 determined in the first 2 h. Addition of the redox mediator methyl viologen (MV) increased TOFH2ase 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.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 (TOFH2ase) of 467 ± 64 h-1 determined in the first 2 h. Addition of the redox mediator methyl viologen (MV) increased TOFH2ase 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 engi