Periodic Reporting for period 4 - BioInspired_SolarH2 (Engineering Bio-Inspired Systems for the Conversion of Solar Energy to Hydrogen)
Reporting period: 2023-10-01 to 2024-09-30
The current energy approach is not sustainable. Our reliance on fossil fuels produces the dangerous accumulation of carbon dioxide in the atmosphere which has disastrous consequences for the environment and our health. Therefore, a change of paradigm is required. The solution resides in nature, more specifically in photosynthesis, the fundamental biological process by which solar energy, water and carbon dioxide are converted into oxygen and biomass.
Here, I have proposed to apply the detailed knowledge that we have gather over the years about the design principles that lead to efficient solar-energy collection, transfer and conversion in photosynthesis to engineer bio-inspired molecular machines able to convert solar energy to a separation of charges, that once coupled to catalysts, will drive water splitting and produce hydrogen, a carbon-neutral solar fuel.
The Design Principles of Photosynthetic Charge Separation are: i) collective excited states (excitons), ii) multiple charge-separation pathways, iii) coherent mixing between excitons and charge-transfer (CT) states promoted by resonant vibrations, iv) the smart protein matrix that controls the selection of the charge-separation pathways and the presence of coherence.
These Design Principles (i and iii) have been implemented into bio-inspired chromophore-protein assemblies and have been studied by a series of state-of-the-art spectroscopic techniques.
Therefore, we have paved the way to achieve the overall objective of generating solar fuels with a system composed by renewable and abundant materials, utilizing water as starting material and solar energy as driving force.
Here, I have proposed to apply the detailed knowledge that we have gather over the years about the design principles that lead to efficient solar-energy collection, transfer and conversion in photosynthesis to engineer bio-inspired molecular machines able to convert solar energy to a separation of charges, that once coupled to catalysts, will drive water splitting and produce hydrogen, a carbon-neutral solar fuel.
The Design Principles of Photosynthetic Charge Separation are: i) collective excited states (excitons), ii) multiple charge-separation pathways, iii) coherent mixing between excitons and charge-transfer (CT) states promoted by resonant vibrations, iv) the smart protein matrix that controls the selection of the charge-separation pathways and the presence of coherence.
These Design Principles (i and iii) have been implemented into bio-inspired chromophore-protein assemblies and have been studied by a series of state-of-the-art spectroscopic techniques.
Therefore, we have paved the way to achieve the overall objective of generating solar fuels with a system composed by renewable and abundant materials, utilizing water as starting material and solar energy as driving force.
For Aim I, after successfully constructing several chromophore-protein assemblies via a novel protocol we have investigated their thermodynamic and electronic properties by a collection of steady-state spectroscopic techniques: Absorption, Fluorescence, Circular Dichroism, Resonance Raman, and Stark; by which we have reached a high level of understanding about our systems. Among other, the main results for our four-helix protein bundles are: i) several protein designs can accommodate four chromophores, ii) these chromophores interact forming two excitonically coupled dimers, iii) the thermal stability of the proteins increase upon chromophore binding, iv) upon protein denaturalization the chromophore remains bound to the protein and upon refolding the assembly folds back to its initial conformation, v) the lowest exciton state has charge-transfer character. These results demonstrate the robustness of our platform and our capacity to implement the design principles of photosynthesis (i and iii) in our quest to design and construct bio-inspired chromophore-protein assemblies for their future implementation into devices for solar-to-electricity and solar-to-fuel conversion. To improve the charge-transfer character, and thus the charge-separation capacity of our systems, we have designed new protein sequences with charged amino acids and with extra helices (designs currently under study). To investigate the photoinduced energy and electron transfer dynamics and the presence of coherence in our systems we have performed ultrafast Broad-Band Transient Absorption (BBTAS) and Two-Dimensional Electronic Spectroscopy (2DES) experiments. The results show that in the excitonically coupled dimers a short-lived (150 picoseconds) charge-transfer state is formed, which possibly yields a charge-separated state. Even though this possibility requires further investigation, it is worth noting that this observation indicates that we have managed to produce a photoinduced charge separation, which is the main objective of Aim I. This work has been presented in international conferences, and we are working on five manuscripts to be submitted for publication in the following months.
In parallel, we have performed a combined experimental/theoretical work to optimize the chromophore binding capacity of a protein via molecular dynamics simulations, which opens new avenues for the rational design of chromophore–protein complexes with advanced functionalities (higher chromophore loading, enhanced coupling, strong charge-separation efficiency). This work was presented in conferences and was published in Protein Science in 2023).
Aim II which focuses on the implementation of our assemblies in devices for solar-energy conversion, has not been started yet since it requires Aim I to be completed. However, in light of the new insights obtained by ultrafast spectroscopy, we consider that we are ready to start building such devices.
Aim III intends to advance the understanding of the role of coherence in enhancing function in photosynthesis. We have performed BBTAS and 2DES on light-harvesting and in core complexes (containing both light-harvesting and reaction centers). In isolated light-harvesting complexes, we have demonstrated coherent energy transfer, and we have studied the role of coherence in the photoprotection mechanism active in plants. In the more intact core complexes, we have investigated the understudied role of coherence in the energy transfer process from complex to complex, and the coherent effects in electron transfer in their reaction centers. Some of these outcomes have been presented in conferences, and four manuscripts are currently being prepared based on these results.
In parallel, we have performed a combined experimental/theoretical work to optimize the chromophore binding capacity of a protein via molecular dynamics simulations, which opens new avenues for the rational design of chromophore–protein complexes with advanced functionalities (higher chromophore loading, enhanced coupling, strong charge-separation efficiency). This work was presented in conferences and was published in Protein Science in 2023).
Aim II which focuses on the implementation of our assemblies in devices for solar-energy conversion, has not been started yet since it requires Aim I to be completed. However, in light of the new insights obtained by ultrafast spectroscopy, we consider that we are ready to start building such devices.
Aim III intends to advance the understanding of the role of coherence in enhancing function in photosynthesis. We have performed BBTAS and 2DES on light-harvesting and in core complexes (containing both light-harvesting and reaction centers). In isolated light-harvesting complexes, we have demonstrated coherent energy transfer, and we have studied the role of coherence in the photoprotection mechanism active in plants. In the more intact core complexes, we have investigated the understudied role of coherence in the energy transfer process from complex to complex, and the coherent effects in electron transfer in their reaction centers. Some of these outcomes have been presented in conferences, and four manuscripts are currently being prepared based on these results.
On the Artificial Photosynthesis field (Aim I), the implementation of excitons with charge-transfer character into our chromophore-protein assemblies, our ability to control the chromophore-chromophore and the chromophore-protein interactions and our capacity to investigate their thermodynamic, electronic, and vibrational properties as well as their charge-separation capacity and ultrafast dynamics, are breakthroughs beyond the state of the art which places us in an advantageous position in the exciting research field of de novo protein design (with the Nobel in Chemistry in 2024 awarded to pioneers in this field). Our results demonstrate that our approach towards the construction of robust and efficient light-harvesting and charge-separation units as it was described in my BioInspired_SolarH2 proposal is unique because of the combination of: first-hand knowledge about the design principles of photosynthesis; a controllable, robust and flexible system (with the potential to be gradually optimized); theoretical tools; and a collection of complementary spectroscopic methods both steady-state and time-resolved that provide a complete physical picture of our systems under study. Consequently, our efforts have resulted in progress beyond the state of the art to be materialized in several articles published (likely) in high impact journals. On the Natural Photosynthesis research line (Aim III), our experiments on isolated as well as on large and intact complexes provide information on the presence and role of coherence in the intra- and inter-complex energy transfer process, in the photoprotection mechanism in plants, and in the electron transfer in reaction centers in their native environment. These investigations advance the field beyond the state of the art since most of the work performed on the role of coherence in Photosynthesis deals with intra-complex energy and electron transfer in isolated reaction center complexes. We are preparing four manuscripts based on these results to be submitted to high impact journals.