Efficient photosynthetic energy conversion requires quantitative, light-driven formation of high-energy, charge-separated states. However, energies of high-lying excited states are rarely extracted, in part because the congested density of states in the excited-state manifold leads to rapid deactivation. Conventional photosystem designs promote electron transfer (ET) by polarizing excited donor electron density toward the acceptor (“one-way” ET), a form of positive design. Curiously, negative design strategies that explicitly avoid unwanted side reactions have been underexplored. We report here that electronic polarization of a molecular chromophore can be used as both a positive and negative design element in a light-driven reaction. Intriguingly, prudent engineering of polarized excited states can steer a “U-turn” ET—where the excited electron density of the donor is initially pushed away from the acceptor—to outcompete a conventional one-way ET scheme. We directly compare one-way vs. U-turn ET strategies via a linked donor–acceptor (DA) assembly in which selective optical excitation produces donor excited states polarized either toward or away from the acceptor. Ultrafast spectroscopy of DA pinpoints the importance of realizing donor singlet and triplet excited states that have opposite electronic polarizations to shut down intersystem crossing. These results demonstrate that oppositely polarized electronically excited states can be employed to steer photoexcited states toward useful, high-energy products by routing these excited states away from states that are photosynthetic dead ends.
more »
« less
Mimicking Natural Photosynthesis: Designing Ultrafast Photosensitized Electron Transfer into Multiheme Cytochrome Protein Nanowires
Efficient nanomaterials for artificial photosynthesis require fast and robust unidirectional electron transfer (ET) from photosensitizers through charge-separation and accumulation units to redox-active catalytic sites. We explored the ultrafast time-scale limits of photo-induced charge transfer between a Ru(II)tris(bipyridine) derivative photosensitizer and PpcA, a 3-heme c-type cytochrome serving as a nanoscale biological wire. Four covalent attachment sites (K28C, K29C, K52C, and G53C) were engineered in PpcA enabling site-specific covalent labeling with expected donor-acceptor (DA) distances of 4–8 Å. X-ray scattering results demonstrated that mutations and chemical labeling did not disrupt the structure of the proteins. Time-resolved spectroscopy revealed three orders of magnitude difference in charge transfer rates for the systems with otherwise similar DA distances and the same number of covalent bonds separating donors and acceptors. All-atom molecular dynamics simulations provided additional insight into the structure-function requirements for ultrafast charge transfer and the requirement of van der Waals contact between aromatic atoms of photosensitizers and hemes in order to observe sub-nanosecond ET. This work demonstrates opportunities to utilize multi-heme c-cytochromes as frameworks for designing ultrafast light-driven ET into charge-accumulating biohybrid model systems, and ultimately for mimicking the photosynthetic paradigm of efficiently coupling ultrafast, light-driven electron transfer chemistry to multi-step catalysis within small, experimentally versatile photosynthetic biohybrid assemblies.
more »
« less
- NSF-PAR ID:
- 10199707
- Date Published:
- Journal Name:
- Nanomaterials
- Volume:
- 10
- Issue:
- 11
- ISSN:
- 2079-4991
- Page Range / eLocation ID:
- 2143
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
H. J. M. Hou and S. I. Allakhverdiev (Ed.)Photosynthetic Reaction Centers (RCs) can be considered blueprints for highly efficient energy transfer. Embedded with an array of cofactors, including (bacterio)chlorophyll ((B)Chl) and (B)pheophytin ((B)Pheo) molecules, RCs function with a high quantum yield that spans a wide spectral range. Understanding the principles that underlie their function can influence the design of the next generation of artificial photosynthetic devices. We are particularly interested in the factors that influence the early stages of light-driven charge separation in RCs. With the recent publication of several highly anticipated RC structures and advanced computational methods available, it is possible to probe both the geometric and electronic structures of an array of RCs. In this chapter, we review the electronic and geometric structures of the (B)Chl and (B)Pheo primary electron acceptors from five RCs, comprising both Type I and Type II RCs and representing both heterodimeric and homodimeric systems. We showcase the dimeric A0●– state of Type I RCs, whereby the unpaired electron is delocalized, to various extents, over two (B)Chl molecules, (B)Chl2 and (B)Chl3. This delocalization is controlled by several factors, including the structure of the (B)Chls, interactions with the surrounding protein matrix, and the orientation and distances of the cofactors themselves. In contrast, the primary acceptors of Type II RCs are entirely monomeric, with electron density residing solely on the (B)Pheo. We compare the natural design of the primary acceptors of the Type I and Type II RCs from both an evolutionary and application based perspective.more » « less
-
In recent years, organic dye molecules as photosensitizers have played a significant role in the field of dye-sensitized solar cells. In this context, two primary dihydroindolocarbazole-based organic dyes (sk201 and sk202), which were synthesized recently by Song et al., and three further designed dyes (DMZ1-3) were theoretically investigated based on density functional theory and time-dependent density functional theory. Molecular geometries, absorption spectra, charge transfer, molecular electrostatic potential and nonlinear optical properties were quantificationally studied and visually presented to reveal the relationships between the molecular structures and performances of dyes. The effects of joining the isolated dyes and TiO2 on the molecular absorption spectra and energy levels were analyzed. Moreover, several parameters, such as efficiency of light-harvesting, driving forces of electron regeneration and injection, excited-state lifetime and vertical dipole moment, were calculated to give the multi-angle demonstrations of the photovoltaic performances for these dyes.more » « less
-
Statement of Purpose Hybrid nanoparticles in which a polymer is used to stabilize the secondary structure of enzyme provide a means to preserve its activity in non-native environments. This approach is illustrated here with horseradish peroxidase (HRP), an important heme enzyme used in medical diagnostic, biosensing, and biotechnological applications. Polymer chaperones in these polymer-enzyme complex (PEC) nanoparticles can enhance the utility of enzymes in unfavorable environments. Structural analysis of the PECs is a crucial link in the machine-learning driven iterative optimization cycle of polymer synthesis and testing. Here, we discuss the utility of small-angle X-ray scattering (SAXS) and quartz crystal microbalance with dissipation (QCMD) for evaluating PECs. Materials and Methods Six polymers were synthesized by automated photoinduced electron/energy transfer-reversible addition-fragmentation chain-transfer (PET-RAFT) polymerization directly in 96-well plates.1 Multiple molar ratios of enzyme:polymer (1:1, 1:5, 1:10, and 1:50) were characterized. HRP was mixed with the polymer and heated to 65 °C for 1 hr to form PECs. Enzyme assay and circular dichroism measurements were performed along with SAXS and QCMD to understand polymer-protein interactions. SAXS data were obtained at NSLS-II beamline 16-ID. Results and Discussion SAXS data were analyzed to determine the radius of gyration (Rg), Porod exponent and pair distance distribution functions (P(r)) (Figure 1). Rg, which corresponds to the size of the PEC nanoparticles, is sensitive to the polydispersity of the solution and does not change significantly in the presence of the polymer GEP1. Notably, the maximal dimension does not change as significantly upon heating to denaturation in the case of the PEC as it does with HRP alone. The effect of denaturation induced by heating seems to depend on the molar ratio of the polymer to enzyme. The Porod exponent, which is related to roughness, decreased from about 4 to 3 upon complexation indicating polymer binding to the enzyme’s surface. These were confirmed by modeling the structures of the HRP, the polymer and the PEC were modeled using DAMMIF/DAMMIN and MONSA (ATSAS software). The changes observed in the structure could be correlated to the measured enzymatic activity. Figure 2 shows the evolution of the PEC when the polymer is deposited onto the enzyme immobilized on Figure 1. P(r) plots for PEC vs. HRP before and after heating, illustrating the increased enzymatic stability due to polymer additives. gold-coated QCM sensors. The plots show the changes in frequency (f) and dissipation (D) with time as HRP is first deposited and is followed by the adsorption of the polymer. Large f and D show that the polymer forms a complex with HRP. Such changes were not observed with negative controls, Pluronics and poly(ethylene glycol). Comparison of the data from free particles in solution with QCM data from immobilized enzymes, shows that the conformation of the complexes in solution and surface-bound HRP could be different. This way, we were able to explore the various states of complex formation under different conditions with different polymers. Figure 2. QCMD data showing the interaction between the immobilized HRP and the polymer. 3rd and 5th harmonics are plotted (blue -f; red-D). Conclusion SAXS and QCMD data show that stabilization of the enzyme activity by inhibiting the unraveling of the secondary structure as seen in size, surface roughness, pair distribution function and percent helicity. Acknowledgment This work was supported by NSF grant 2009942. References [1] Tamasi, M, et al. Adv Intell Syst 2020, 2(2): 1900126.more » « less
-
Strong excitonic coupling in photosynthetic systems is believed to enable efficient light absorption and quantitative charge separation, motivating the development of artificial multi-chromophore arrays with equally strong or even stronger excitonic coupling. However, large excitonic coupling strengths have typically been accompanied by fast non-radiative recombination, limiting the potential of the arrays for solar energy conversion as well as other applications such as fluorescent labeling. Here, we report giant excitonic coupling leading to broad optical absorption in bioinspired BODIPY dyads that have high photostability, excited-state lifetimes at the nanosecond scale, and fluorescence quantum yields of nearly 50%. Through the synthesis, spectroscopic characterization, and computational modeling of a series of dyads with different linking moieties, we show that the strongest coupling is obtained with diethynylmaleimide linkers, for which the coupling occurs through space between BODIPY units with small separations and slipped co-facial orientations. Other linkers allow for broad tuning of both the relative through-bond and through-space coupling contributions and the overall strength of interpigment coupling, with a tradeoff observed in general between the strength of the two coupling mechanisms. These findings open the door to the synthesis of molecular systems that function effectively as light-harvesting antennas and as electron donors or acceptors for solar energy conversion.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.3390/nano10112143
