Charge transfer as a mechanism for chlorophyll fluorescence concentration quenching

Bourne-Worster, Susannah; Feighan, Oliver; Manby, Frederick R.

Abstract

Significance
The light-absorbing molecules (chlorophyll) in photosynthetic organisms must be held close together to achieve efficient energy transport but in solution, such close proximity leads to rapid energy loss (quenching). The hypothesized quenching mechanism is photoinduced charge separation followed by rapid charge recombination but this has never been proven. We confirm the feasibility of this mechanism using detailed calculations to show that charge separation outcompetes fluorescence (i.e., induces quenching) at chlorophyll separations compatible with the concentrations at which quenching is observed. Moreover, we reveal that the stiff photosynthetic protein environment inhibits quenching by preventing chlorophyll pairs from adopting a suitable shape for charge transfer. This insight into the protein function identifies a crucial design feature for efficient future artificial light-harvesting devices.
Abstract
Highly concentrated solutions of chlorophyll display rapid fluorescence quenching. The same devastating energy loss is not seen in photosynthetic light-harvesting antenna complexes, despite the need for chromophores to be in close proximity to facilitate energy transfer. A promising, though unconfirmed mechanism for the observed quenching is energy transfer from an excited chlorophyll monomer to a closely associated chlorophyll pair that subsequently undergoes rapid nonradiative decay to the ground state via a short-lived intermediate charge-transfer state. In this work, we make use of newly emerging fast methods in quantum chemistry to assess the feasibility of this proposed mechanism. We calculate rate constants for the initial charge separation, based on Marcus free-energy surfaces extracted from molecular dynamics simulations of solvated chlorophyll pairs, demonstrating that this pathway will compete with fluorescence (i.e., drive quenching) at experimentally measured quenching concentrations. We show that the rate of charge separation is highly sensitive to interchlorophyll distance and the relative orientations of chromophores within a quenching pair. We discuss possible solvent effects on the rate of charge separation (and consequently the degree of quenching), using the light-harvesting complex II (LH2) protein from rps. acidophila as a specific example of how this process might be controlled in a protein environment. Crucially, we reveal that the LH2 antenna protein prevents quenching, even at the high chlorophyll concentrations required for efficient energy transfer, by restricting the range of orientations that neighboring chlorophyll pairs can adopt.

Citation

Bourne-Worster, S., Feighan, O., & Manby, F. R. (2023). Charge transfer as a mechanism for chlorophyll fluorescence concentration quenching. Proceedings of the National Academy of Sciences, 120(5), https://doi.org/10.1073/pnas.2210811120

• Journal Article Type: Article
• Acceptance Date: Dec 15, 2022
• Online Publication Date: Jan 23, 2023
• Publication Date: Jan 31, 2023
• Deposit Date: Jan 27, 2025
• Journal: Proceedings of the National Academy of Sciences
• Print ISSN: 0027-8424
• Electronic ISSN: 1091-6490
• Publisher: National Academy of Sciences
• Peer Reviewed: Peer Reviewed
• Volume: 120
• Issue: 5
• DOI: https://doi.org/10.1073/pnas.2210811120
• Public URL: https://durham-repository.worktribe.com/output/3353426
• Additional Information: Received: 2022-06-28; Accepted: 2022-12-15; Published: 2023-01-23