Simulations of Excitonic Couplings in Spinach Light-Harvesting Complex II Using a More Realistic Model in the Presence of Photosystem II Core

Abstract

In this study, we employed a method for evaluating dynamic exciton couplings by using atomic transition density moments and molecular dynamics (MD) coordinates. We then applied this computational approach to investigate protein-regulated exciton couplings in spinach light-harvesting complex II (LHCII). Our findings, based on a more realistic all-atom computational model in the presence of the photosystem II (PSII) core and minor antennas, reveal distinct coupling strength patterns for the monomers in LHCII. The probability distributions of excitonic couplings in isolated LHCII always exhibit a single peak, whereas those in the LHCII-PSII complex display a bimodal nature. Such reductions in the excitonic coupling strengths of the main pigments, especially for some chlorophyll-lutein pairs, suggest that the peripheral proteins could modulate energy transfer processes in LHCII-PSII. A closer examination of the key structural parameters reveals that the angles between helices A and B and the distance between CLA612 and LUT620 increase in LHCII-PSII, which are closely associated with the reductions in excitonic couplings.

1

Overall structure of the spinach LHCII-PSII supercomplex (PDB ID: 3JCU) and LHCII viewed along the membrane plane (a, b) or from the stromal side along the thylakoid membrane (c, d). M1, M2, and M3 in (c) and (d) represent three monomers in LHCII.

2

Pigments distributed in a monomer of LHCII are depicted in panel (a), with schematic diagrams in panel (b) for CLA611-CLA612 and panel (c) for CLA612-LUT620, illustrating key structural parameters of distance, dislocation angle, rotation angle, and dihedral angle. Different colors represent different pigments: lutein (LUT) in orange, chlorophyll a (CLA) in green, chlorophyll b (CHL) in cyan, neoxanthin (NEX) and violaxanthin (XAT) in violet, and the secondary structure of the protein scaffold in light gray.

3

Absolute interpigment excitonic couplings (in cm^–1) of monomer 1 in LHCII using different computational models (a). Differences between our computed values and those calculated by Duffy (lower-left triangle) and Müh (upper-right triangle) are shown in (b).

4

Absolute interpigment excitonic couplings (in cm^–1) of monomers 1 (M1), 2 (M2), and 3 (M3) in LHCII.

5

Probability distributions of absolute excitonic couplings (in cm^–1) of representative pigment pairs in LHCII: excitonic couplings for CLA611–CLA612 (a, b, c), CLA603–LUT621 (d, e, f), and CLA612–LUT620 (g, h, i), along with averaged values (indicated by blue lines).

6

Time evolution of excitonic couplings and key structural parameters of CLA611–CLA612 in monomers 1 (a), 2 (b), and 3 (c), along with representative snapshots in monomer 3 (d) (indicated by green stars).

7

Time evolution of excitonic couplings and key structural parameters of CLA612–LUT620 in monomers 1 (a), 2 (b), and 3 (c), along with representative snapshots in monomer 3 (d) (indicated by green stars).

8

Probability distributions of absolute excitonic couplings (in cm^–1) of representative pigment pairs in LHCII–PSII: excitonic couplings for CLA611–CLA612 (a, b, c), CLA603–LUT621 (d, e, f), and CLA612–LUT620 (g, h, i), along with averaged values of peaks (indicated by blue lines).

9

Probability distributions of absolute excitonic couplings (in cm^–1) for CLA611–CLA612 (a), CLA603–LUT621 (b), and CLA612–LUT620 pairs (c) in all three monomers in LHCII (in blue) and LHCII–PSII (in green), along with averaged values of peaks (indicated by blue and green lines).

10

Representative structures of monomers 1 (a), 2 (b), and 3 (c) extracted from production NPT MD simulations of LHCII–PSII. Different colors represent averaged values of different structural parameters: angle of LUT620–LUT621 in orange, angle of helices A and B in black, distance between CLA612–LUT620 in purple.

11

Representative structures of monomers 1 (a), 2 (b), and 3 (c) extracted from production NPT MD simulations of isolated LHCII. Different colors represent averaged values of different structural parameters: angle of LUT620–LUT621 in orange, angle of helices A and B in black, distance between CLA612–LUT620 in purple.