A Clean Energy Future 

Solar energy is an important source of clean energy that can help meet the ever-increasing global demands for energy.  Solar-to-fuels research involves developing new materials that can efficiently capture sunlight and convert it into a storable fuel so that the energy from the sun can be used when needed.  An efficient way to store the sun’s energy is in the chemical bonds of molecules such as hydrogen gas (H₂).  Unlike carbon-based fossil fuels that produce environmentally harmful carbon dioxide (CO₂), H₂ is a clean fuel because, upon burning to release the energy in its chemical bond, water is produced.

Nature’s Solar Energy Converters

We can learn from Nature how to do this.  Nature uses specialized proteins called Reaction Centers (RCs) to convert light energy into chemical energy.  This occurs via light-induced rapid sequential electron transfers between cofactors bound within the core of the RC proteins, resulting in the formation of a long-lived charge separated state that can be utilized to drive chemical reactions.  RCs are extremely efficient solar energy converters, producing nearly one electron for every photon absorbed. To date, no artificial photosynthetic system can replicate the charge-separation efficiencies of Nature’s RCs.  One type of RC, called Photosystem I (PSI), generates an electron that has enough of an electrochemical potential to drive H₂ production.  All that is needed is a catalyst to capture the light-generated electrons of PSI. 

Photosynthetic Biohybrids 

To do this, we study what are called biohybrids: complexes between proteins and synthetic molecules.  Photosynthetic biohybrids combine the function of a synthetic catalyst with the optimized light capture and conversion capabilities of the PSI RC.  The question is how to make a protein-catalyst complex such that efficient electron transfer between them occurs?  Over the years, many different types of PSI biohybrids have been reported, inspiring us to try our hand at it.  In building our biohybrid, we looked to Nature for inspiration.  PSI has two small, soluble acceptor proteins that shuttle the electrons generated by PSI to other metabolic pathways.  The interaction between PSI and these acceptor proteins is electrostatically driven with the negatively charged surfaces of the proteins binding to a positively charged docking site on PSI.  By using platinum nanoparticles (PtNPs, good H₂ catalysts!) of a similar size to the acceptor proteins and coated with negatively charged ligands, we found that we could readily bind the PtNPs to PSI.  Electron paramagnetic resonance (EPR) spectroscopic studies, which can observe the unpaired electron spins as they move through the RC following light-excitation, showed very efficient electron transfer from PSI to the PtNP in the biohybrid and confirmed the location of the PtNPs on the acceptor end (stromal side) of PSI.  Importantly, we observed very high rates of light-driven H₂ production for our electrostatically assembled PSI-PtNP biohybrid in photocatalysis experiments.  Thus, by simply using sunlight, water, and the biohybrid (in very small amounts, nanomolar concentrations), we generate the solar fuel H₂!!  To date, this remains one of the best PSI-generating H₂ systems.

Revealing the Molecular Structure of a Photosynthetic Biohybrid

 Where does the PtNP bind to the protein?  What interactions does the PtNP have with the protein surface?  How does the PtNP-protein interface mediate electron transfer?   We addressed these questions by using cryo-electron microscopy (cryo-EM), a technique that uses a transmission electron microscope to image proteins at cryogenic temperatures.   In this Nature Communications article, we report the 2.27 Å global resolution cryo-EM structure of our PSI-PtNP biohybrid.  The cryo-EM map revealed a trimeric PSI structure consistent with most other cyanobacterial PSI structures.  Two high-signal ellipsoidal map regions were identified per PSI monomer and assigned to PtNP binding sites.  This was a surprise!  We had always thought that only one PtNP bound to each PSI monomer.   Both PtNPs bind to the stromal side of PSI.  One of the PtNP sites is within 14 Å of the terminal electron acceptor cofactor of PSI, an iron-sulfur cluster.  We believe this to be the site of photocatalysis.  This site overlaps the native acceptor protein sites, although the PtNP is in a slightly different location.  Furthermore, we were able to determine the protein subunits and specific amino acid residues that likely interact with the PtNPs.

Looking Ahead

This first direct structural look at a protein-nanomaterial interface is important, as it reveals features that can be experimentally explored and optimized for solar-driven H₂ production.  For instance, now we know where to genetically alter the protein’s amino acids involved in catalyst binding, such as mutating individual amino acids to probe their specific role in catalyst interactions or adding positively charged side chains to increase binding specificity.  On the flip side, we can chemically tune the NP size, composition, and charge to enhance protein-catalyst interactions and catalytic efficiencies. 

Concomitantly, we hope this structure will inspire scientific discovery in the wider community.  There are many light-active nanomaterials (instead of PSI) linked to enzyme-driven catalysis to generate solar fuels, yet none of these systems have been structurally characterized.  Our hope is that this PSI-PtNP structure will inform on these other systems and increase  fundamental understanding of structure-function relationships instrumental to bioenergy.