From antenna to reaction center: Pathways of ultrafast energy and charge transfer in photosystem II

Abstract

The photosystem II core complex (PSII-CC) is the smallest subunit of the oxygenic photosynthetic apparatus that contains core antennas and a reaction center, which together allow for rapid energy transfer and charge separation, ultimately leading to efficient solar energy conversion. However, there is a lack of consensus on the interplay between the energy transfer and charge separation dynamics of the core complex. Here, we report the application of two-dimensional electronic-vibrational (2DEV) spectroscopy to the spinach PSII-CC at 77 K. The simultaneous temporal and spectral resolution afforded by 2DEV spectroscopy facilitates the separation and direct assignment of coexisting dynamical processes. Our results show that the dominant dynamics of the PSII-CC are distinct in different excitation energy regions. By separating the excitation regions, we are able to distinguish the intraprotein dynamics and interprotein energy transfer. Additionally, with the improved resolution, we are able to identify the key pigments involved in the pathways, allowing for a direct connection between dynamical and structural information. Specifically, we show that C505 in CP43 and the peripheral chlorophyll Chlz D1 in the reaction center are most likely responsible for energy transfer from CP43 to the reaction center.

Expression of the far‐red D1 protein or introduction of conserved far‐red D1 residues into Synechocystis sp. PCC 6803 impairs Photosystem II

“…In the FRL‐PS II centres, the ChlZ D1 is a chlorophyll a molecule (Gisriel et al, 2023). This chlorophyll has been indicated to be responsible for energy transfer from CP43 to the reaction centre (Yang et al, 2022).…”

“…In the FRL‐PS II centres, the ChlZ D1 is a chlorophyll a molecule (Gisriel et al, 2023). This chlorophyll is responsible for energy transfer from CP43 to the reaction centre (Diner & Rappaport, 2002; Yang et al, 2022). The PsbC‐508 chlorophyll, a chlorophyll f in FRL‐PS II centres, is the closest non‐reaction centre chlorophyll to Chl D1 and has been suggested to be involved in bridging energy transfer from CP43 to D1 (Nürnberg et al, 2018).…”

“…In the FRL-PS II centres, the ChlZ D1 is a chlorophyll a molecule (Gisriel et al, 2023). This chlorophyll has been indicated to be responsible for energy transfer from CP43 to the reaction centre (Yang et al, 2022). Amino acid changes in helix A of D1 were introduced into Synechocystis 6803 by mutating the psbA2 gene in a strain lacking psbA1 and psbA3.…”

Infrared Signatures of Phycobilins within the Phycocyanin 645 Complex

“…Despite the wide energy gaps between each excitonic state, their bandwidths lead to spectral overlap which makes the assignment of infrared signatures to specific pigments difficult via pump-probe data. We, therefore, take advantage of the excitation-energy-dependent infrared signatures of 2DEV spectroscopy, which, combined with the enhanced spectral resolution of this technique, − allows us to identify the infrared features specific to each pigment in the PC645 complex. 2DEV spectroscopy ultimately provides a detailed picture of the spatiotemporal flow of the excitation energy between each pigment pair in PC645 due to the influence of the local protein environment on the IR signatures of each pigment.…”

Stabilization of Charge-Transfer Excited States in Biological Systems: A Computational Focus on the Special Pair in Photosystem II Reaction Centers

“…Recently, nonlinear pump–probe spectroscopy has been used as it allows for the monitoring of dynamical processes on a picosecond time scale. Specifically, 2D spectroscopy of a UV–Vis pump and an infrared probe pulse can track infrared vibrational modes, which become sensitized/perturbed due to the presence of photoelectrons or holes. , Crystallography and large-scale computational modeling using molecular mechanics force fields have worked together in tandem as experimentally determined structures, e.g., of the PSII complexes have allowed computational chemistry methods to simulate photophysical processes. At the same time, molecular dynamics (MD) simulations have been able to refine crystallographic structures with, e.g., water distributions and electron density maps by correcting known issues of the protein environments at cryogenic temperatures .…”