Solar hydrogen-producing bionanodevice outperforms natural photosynthesis

Abstract

Although a number of solar biohydrogen systems employing photosystem I (PSI) have been developed, few attain the electron transfer throughput of oxygenic photosynthesis. We have optimized a biological/organic nanoconstruct that directly tethers F(B), the terminal [4Fe-4S] cluster of PSI from Synechococcus sp. PCC 7002, to the distal [4Fe-4S] cluster of the [FeFe]-hydrogenase (H(2)ase) from Clostridium acetobutylicum. On illumination, the PSI-[FeFe]-H(2)ase nanoconstruct evolves H(2) at a rate of 2,200 ± 460 μmol mg chlorophyll(-1) h(-1), which is equivalent to 105 ± 22 e(-)PSI(-1) s(-1). Cyanobacteria evolve O(2) at a rate of approximately 400 μmol mg chlorophyll(-1) h(-1), which is equivalent to 47 e(-)PSI(-1) s(-1), given a PSI to photosystem II ratio of 1.8. The greater than twofold electron throughput by this hybrid biological/organic nanoconstruct over in vivo oxygenic photosynthesis validates the concept of tethering proteins through their redox cofactors to overcome diffusion-based rate limitations on electron transfer.

Fig. 1.

Schematic comparison of electron flow in (A) in vivo photosynthesis and (B) the photosynthetic nanoconstructs described here. Rates given indicate the electron throughput through each of the photosynthetic reaction centers in each scenario. Electron transfer is primarily diffusionally governed in A and through bonds in B. Direct electron transfer reactions are indicated as black solid arrows, diffusion-based steps as black dashed arrows. Protein complexes are shown as crystal structures. Cross-linking in B is indicated as a red arrow. The molecular wire structure is shown in red. (Cyt c₆: cytochrome c₆, Cb₆f: cytochrome b₆f complex, Fd: ferredoxin, FNR: ferredoxin:NADP⁺ oxido reductase, HydA: hydrogenase, PQ: plastoquinone pool).