Local Phonon Environment as a Design Element for Long-lived Excitonic Coherence: Dithia-anthracenophane Revisited

Excitonic energy transfer in light harvesting complexes, the primary process of photosynthesis, operates with near-unity efficiency. Experimental and theoretical studies suggest that quantum mechanical wave-like motion of excitons in the pigment-protein complex may be responsible for this quantum efficiency. Observed coherent exciton dynamics can be modelled completely only if we consider the interaction of the exciton with its complex environment. While it is known that the relative orientation of the chromophore units and reorganisation energy are important design elements, the role of a structured phonon environment is often not considered. The purpose of this study is to investigate the role of a structured immediate phonon environment in determining the exciton dynamics and the possibility of using it as an optimal design element. Through the case study of dithia-anthracenophane, a bichromophore using the Hierarchical Equations Of Motion formalism, we show that the experimentally observed coherent exciton dynamics can be reproduced only by considering the actual structure of the phonon environment. While the slow dephasing of quantum coherence in dithia-anthracenophane can be attributed to strong vibronic coupling to high-frequency modes, vibronic quenching is the source of long oscillation periods in population transfer. This study sheds light on the crucial role of the structure of the immediate phonon environment in determining the exciton dynamics. We conclude by proposing some design principles for sustaining long-lived coherence in molecular systems.

Plant Photochemistry, Reactive Oxygen Species, and Photoprotection

Light energy, absorbed as photons by chlorophylls and other pigment molecules consisting of light-harvesting complexes (LHCs), is transferred to the reaction centres (RCs), where, through charge separation, electrons flow from photosystem II (PSII) through cytochrome b6f and diffusible electron carriers to photosystem I (PSI) [...]

Environmental Tuning of Homologs of the Orange Carotenoid Protein-Encoding Gene in the Cyanobacterium Fremyella diplosiphon

The orange carotenoid protein (OCP) family of proteins are light-activated proteins that function in dissipating excess energy absorbed by accessory light-harvesting complexes, i.e., phycobilisomes (PBSs), in cyanobacteria. Some cyanobacteria contain multiple homologs of the OCP-encoding gene (ocp). Fremyella diplosiphon, a cyanobacterium studied for light-dependent regulation of PBSs during complementary chromatic acclimation (CCA), contains several OCP homologs – two full-length OCPs, three Helical Carotenoid Proteins (HCPs) with homology to the N-terminus of OCP, and one C-terminal domain-like carotenoid protein (CCP) with homology to the C-terminus of OCP. We examined whether these homologs are distinctly regulated in response to different environmental factors, which could indicate distinct functions. We observed distinct patterns of expression for some OCP, HCP, and CCP encoding genes, and have evidence that light-dependent aspects of ocp homolog expression are regulated by photoreceptor RcaE which controls CCA. RcaE-dependent transcriptional regulator RcaC is also involved in the photoregulation of some hcp genes. Apart from light, additional environmental factors associated with cellular redox regulation impact the mRNA levels of ocp homologs, including salt, cold, and disruption of electron transport. Analyses of conserved sequences in the promoters of ocp homologs were conducted to gain additional insight into regulation of these genes. Several conserved regulatory elements were found across multiple ocp homolog promoters that potentially control differential transcriptional regulation in response to a range of environmental cues. The impact of distinct environmental cues on differential accumulation of ocp homolog transcripts indicates potential functional diversification of this gene family in cyanobacteria. These genes likely enable dynamic cellular protection in response to diverse environmental stress conditions in F. diplosiphon.

Photosynthetic light harvesting and thylakoid organization in a CRISPR/Cas9 Arabidopsis thaliana LHCB1 knockout mutant.

Light absorbed by chlorophylls of photosystem II and I drives oxygenic photosynthesis. Light-harvesting complexes increase the absorption cross-section of these photosystems. Furthermore, these complexes play a central role in photoprotection by dissipating the excess of absorbed light energy in an inducible and regulated fashion. In higher plants, the main light-harvesting complex is the trimeric LHCII. In this work, we used CRISPR/Cas9 to knockout the five genes encoding LHCB1, which is the major component of the trimeric LHCII. In absence of LHCB1 the accumulation of the other LHCII isoforms was only slightly increased, thereby resulting in chlorophyll loss leading to a pale green phenotype and growth delay. Photosystem II absorption cross-section was smaller while photosystem I absorption cross-section was unaffected. This altered the chlorophyll repartition between the two photosystems, favoring photosystem I excitation. The equilibrium of the photosynthetic electron transport was partially maintained by a lower photosystem I over photosystem II reaction center ratio and by the dephosphorylation of LHCII and photosystem II. Loss of LHCB1 altered the thylakoid structure, with less membrane layers per grana stack and reduced grana width. Stable LHCB1 knock out lines allow characterizing the role of this protein in light harvesting and acclimation and pave the way for future in vivo mutational analyses of LHCII.

Artificial quantum photosynthetic materials

Photosynthesis has been shown to be a highly efficient process for energy transfer in plants and bacteria. It has been proposed that quantum mechanics plays a key role in this energy transfer process. There has been evidence that photosynthetic systems may exhibit quantum coherence. As artificial light-harvesting complexes have been proposed to mimic photosynthesis, it is prudent that artificial photosynthetic materials should also be tested for quantum coherence. To date, such studies have not been reported. In this work, we examine one such system, the BODIPY light harvesting complex (LHC), which has been shown to exhibit classical energy transfer via Förster resonance energy transfer. We compare the photon absorption of the LHC with the BODIPY chromophore by performing UV-visible, transient absorption, broadband pump-probe (BBPP) and two-dimensional electronic (2DES) spectroscopy. The 2DES and BBPP show evidence for quantum coherence, with oscillation frequencies of 100 cm-1 and 600 cm-1, which are attributable to vibronic, or exciton-phonon type coupling. Further computational analysis suggests strong couplings of the molecular orbitals of the LHC resulting from the stacking of neighbouring BODIPY chromophore units may contribute to undesirable hypochromic effects .

A different perspective for nonphotochemical quenching in plant antenna complexes

Light-harvesting complexes of plants exert a dual function of light-harvesting (LH) and photoprotection through processes collectively called nonphotochemical quenching (NPQ). While LH processes are relatively well characterized, those involved in NPQ are less understood. Here, we characterize the quenching mechanisms of CP29, a minor LHC of plants, through the integration of two complementary enhanced-sampling techniques, dimensionality reduction schemes, electronic calculations and the analysis of cryo-EM data in the light of the predicted conformational ensemble. Our study reveals that the switch between LH and quenching state is more complex than previously thought. Several conformations of the lumenal side of the protein occur and differently affect the pigments’ relative geometries and interactions. Moreover, we show that a quenching mechanism localized on a single chlorophyll-carotenoid pair is not sufficient but many chlorophylls are simultaneously involved. In such a diffuse mechanism, short-range interactions between each carotenoid and different chlorophylls combined with a protein-mediated tuning of the carotenoid excitation energies have to be considered in addition to the commonly suggested Coulomb interactions.

Dimeric and high-resolution structures of Chlamydomonas Photosystem I from a temperature-sensitive Photosystem II mutant

Water molecules play a pivotal functional role in photosynthesis, primarily as the substrate for Photosystem II (PSII). However, their importance and contribution to Photosystem I (PSI) activity remains obscure. Using a high-resolution cryogenic electron microscopy (cryo-EM) PSI structure from a Chlamydomonas reinhardtii temperature-sensitive photoautotrophic PSII mutant (TSP4), a conserved network of water molecules - dating back to cyanobacteria - was uncovered, mainly in the vicinity of the electron transport chain (ETC). The high-resolution structure illustrated that the water molecules served as a ligand in every chlorophyll that was missing a fifth magnesium coordination in the PSI core and in the light-harvesting complexes (LHC). The asymmetric distribution of the water molecules near the ETC branches modulated their electrostatic landscape, distinctly in the space between the quinones and FX. The data also disclosed the first observation of eukaryotic PSI oligomerisation through a low-resolution PSI dimer that was comprised of PSI-10LHC and PSI-8LHC.

Structural Diversity of Photosystem I and Its Light-Harvesting System in Eukaryotic Algae and Plants

Photosystem I (PSI) is one of the most efficient photoelectric apparatus in nature, converting solar energy into condensed chemical energy with almost 100% quantum efficiency. The ability of PSI to attain such high conversion efficiency depends on the precise spatial arrangement of its protein subunits and binding cofactors. The PSI structures of oxygenic photosynthetic organisms, namely cyanobacteria, eukaryotic algae, and plants, have undergone great variation during their evolution, especially in eukaryotic algae and vascular plants for which light-harvesting complexes (LHCI) developed that surround the PSI core complex. A detailed understanding of the functional and structural properties of this PSI-LHCI is not only an important foundation for understanding the evolution of photosynthetic organisms but is also useful for designing future artificial photochemical devices. Recently, the structures of such PSI-LHCI supercomplexes from red alga, green alga, diatoms, and plants were determined by X-ray crystallography and single-particle cryo-electron microscopy (cryo-EM). These findings provide new insights into the various structural adjustments of PSI, especially with respect to the diversity of peripheral antenna systems arising via evolutionary processes. Here, we review the structural details of the PSI tetramer in cyanobacteria and the PSI-LHCI and PSI-LHCI-LHCII supercomplexes from different algae and plants, and then discuss the diversity of PSI-LHCI in oxygenic photosynthesis organisms.

Predicting the future of excitation energy transfer in light-harvesting complex with artificial intelligence-based quantum dynamics

Exploring excitation energy transfer (EET) in light-harvesting complexes (LHCs) is essential for understanding the natural processes and design of highly-efficient photovoltaic devices. LHCs are open systems, where quantum effects may play a crucial role for almost perfect utilization of solar energy. Simulation of energy transfer with inclusion of quantum effects can be done within the framework of dissipative quantum dynamics (QD), which are computationally expensive. Thus, artificial intelligence (AI) offers itself as a tool for reducing the computational cost. We suggest AI-QD approach using AI to directly predict QD as a function of time and other parameters such as temperature, reorganization energy, etc., completely circumventing the need of recursive step-wise dynamics propagation in contrast to the traditional QD and alternative, recursive AI-based QD approaches. Our trajectory-learning AI-QD approach is able to predict the correct asymptotic behavior of QD at infinite time. We demonstrate AI-QD on seven-sites Fenna–Matthews–Olson (FMO) complex.