Exploiting Chromophore–Protein Interactions through Linker Engineering To Tune Photoinduced Dynamics in a Biomimetic Light-Harvesting Platform

Abstract

Creating artificial systems that mimic and surpass those found in nature is one of the great challenges of modern science. In the context of photosynthetic light harvesting, the difficulty lies in attaining utmost control over the energetics, positions and relative orientations of chromophores in densely packed arrays to transfer electronic excitation energy to desired locations with high efficiency. Toward achieving this goal, we use a highly versatile biomimetic protein scaffold from the tobacco mosaic virus coat protein on which chromophores can be attached at precise locations via linkers of differing lengths and rigidities. We show that minor linker modifications, including switching chiral configurations and alkyl chain shortening, lead to significant lengthening of the ultrafast excited state dynamics of the system as the linkers are shortened and rigidified. Molecular dynamics simulations provide molecular-level detail over how the chromophore attachment orientations, positions, and distances from the protein surface lead to the observed trends in system dynamics. In particular, we find that short and rigid linkers are able to sandwich water molecules between chromophore and protein, leading to chromophore-water-protein supracomplexes with intricately coupled dynamics that are highly dependent on their local protein environment. In addition, cyclohexyl-based linkers are identified as ideal candidates to retain rotational correlations over several nanoseconds and thus lock relative chromophore orientations throughout the lifetime of an exciton. Combining linker engineering with judicious placement of chromophores on the hydrated protein scaffold to exploit different chromophore-bath couplings provides a clear and effective path to producing highly controllable artificial light-harvesting systems that can increasingly mimic their natural counterparts, thus aiding to elucidate natural photosynthetic mechanisms.

Engineering couplings for exciton transport using synthetic DNA scaffolds

“…Nanoscale control over chromophore position is challenging in proteins due to their structural complexity and limitations in mutagenesis. [20][21][22] Instead, synthetic model systems that position chromophores have been developed, including metal-organic frameworks, 8,23 viral proteins, [24][25][26] self-assembled molecular aggregates, [27][28][29][30] and conjugated polymers. 31 However, these systems lack a synthetic handle for electronic coupling.…”

“…While the impact of the bath on exciton dynamics had been well established theoretically, [97][98][99] previous experiments were limited to the impact of the bath on individual excitonic states. 24 Chromophore-DNA constructs open the door to varying the system-bath coupling for chromophore aggregates, and thus achieving the full nanoscale control required to direct exciton dynamics.…”

Hierarchical Self-Assembly of Proteins Through Rationally Designed Supramolecular Interfaces

“…Scientists usually used chemical modification or biological genetic recombination to construct functional protein nanomaterials. Francis et al site-specifically modified TMV coat proteins with chromophore pairs, and found TMV disks could not only prevent the aggregation-induced quench of chromophores but also greatly improved FRET transfer efficacy (Delor et al, 2018). If introducing GPx catalytic centers on TMV via site-directed gene mutagenesis, the reengineered nanostructures showed ultrahigh catalytic activity and stability (Hou et al, 2012).…”

Examination of abiotic cofactor assembly in photosynthetic biomimetics: site-specific stereoselectivity in the conjugation of a ruthenium(II) tris(bipyridine) photosensitizer to a multi-heme protein

“…These studies demonstrate that complementary geometric shapes and non-covalent interactions within a protein binding pocket can be used to create a conformationally determined, lock-and-key specificity for photosensitizer integration within protein host matrices. Further, investigations of photosynthetic biohybrid designs for light-harvesting have demonstrated that chiral linkages can be used to create sterically-constrained, chromophore-protein couplings that function to enhance light-harvesting by modulating nuclear relaxation dynamics, extending excited-state lifetimes, and controlling Stokes shift energy losses (Delor et al 2018). These designed protein-chromophore interactions are anticipated to mimic those functioning in native photosynthetic light-harvesting proteins.…”