Issue 12, 2021

Chlorophyll excitation energies and structural stability of the CP47 antenna of photosystem II: a case study in the first-principles simulation of light-harvesting complexes

Abstract

Natural photosynthesis relies on light harvesting and excitation energy transfer by specialized pigment–protein complexes. Their structure and the electronic properties of the embedded chromophores define the mechanisms of energy transfer. An important example of a pigment–protein complex is CP47, one of the integral antennae of the oxygen-evolving photosystem II (PSII) that is responsible for efficient excitation energy transfer to the PSII reaction center. The charge-transfer excitation induced among coupled reaction center chromophores resolves into charge separation that initiates the electron transfer cascade driving oxygenic photosynthesis. Mapping the distribution of site energies among the 16 chlorophyll molecules of CP47 is essential for understanding excitation energy transfer and overall antenna function. In this work, we demonstrate a multiscale quantum mechanics/molecular mechanics (QM/MM) approach utilizing full time-dependent density functional theory with modern range-separated functionals to compute for the first time the excitation energies of all CP47 chlorophylls in a complete membrane-embedded cyanobacterial PSII dimer. The results quantify the electrostatic effect of the protein on the site energies of CP47 chlorophylls, providing a high-level quantum chemical excitation profile of CP47 within a complete computational model of “near-native” cyanobacterial PSII. The ranking of site energies and the identity of the most red-shifted chlorophylls (B3, followed by B1) differ from previous hypotheses in the literature and provide an alternative basis for evaluating past approaches and semiempirically fitted sets. Given that a lot of experimental studies on CP47 and other light-harvesting complexes utilize extracted samples, we employ molecular dynamics simulations of isolated CP47 to identify which parts of the polypeptide are most destabilized and which pigments are most perturbed when the antenna complex is extracted from PSII. We demonstrate that large parts of the isolated complex rapidly refold to non-native conformations and that certain pigments (such as chlorophyll B1 and β-carotene h1) are so destabilized that they are probably lost upon extraction of CP47 from PSII. The results suggest that the properties of isolated CP47 are not representative of the native complexed antenna. The insights obtained from CP47 are generalizable, with important implications for the information content of experimental studies on biological light-harvesting antenna systems.

Graphical abstract: Chlorophyll excitation energies and structural stability of the CP47 antenna of photosystem II: a case study in the first-principles simulation of light-harvesting complexes

Supplementary files

Article information

Article type
Edge Article
Submitted
03 Dec 2020
Accepted
08 Feb 2021
First published
12 Feb 2021
This article is Open Access

All publication charges for this article have been paid for by the Royal Society of Chemistry
Creative Commons BY license

Chem. Sci., 2021,12, 4463-4476

Chlorophyll excitation energies and structural stability of the CP47 antenna of photosystem II: a case study in the first-principles simulation of light-harvesting complexes

A. Sirohiwal, F. Neese and D. A. Pantazis, Chem. Sci., 2021, 12, 4463 DOI: 10.1039/D0SC06616H

This article is licensed under a Creative Commons Attribution 3.0 Unported Licence. You can use material from this article in other publications without requesting further permissions from the RSC, provided that the correct acknowledgement is given.

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