Tunneling Mechanisms of Quinones in Photosynthetic Reaction Center-Light Harvesting 1 Supercomplexes

Abstract

In photosynthesis, light energy is absorbed and transferred to the reaction center, ultimately leading to the reduction of quinone molecules through the electron transfer chain. The oxidation and reduction of quinones generate an electrochemical potential difference used for adenosine triphosphate synthesis. The trafficking of quinone/quinol molecules between electron transport components has been a long-standing question. Here, an atomic-level investigation into the molecular mechanism of quinol dissociation in the photosynthetic reaction center-light-harvesting complex 1 (RC-LH1) supercomplexes from Rhodopseudomonas palustris, using classical molecular dynamics (MD) simulations combined with self-random acceleration MD-MD simulations and umbrella sampling methods, is conducted. Results reveal a significant increase in the mobility of quinone molecules upon reduction within RC-LH1, which is accompanied by conformational modifications in the local protein environment. Quinol molecules have a tendency to escape from RC-LH1 in a tail-first mode, exhibiting channel selectivity, with distinct preferred dissociation pathways in the closed and open LH1 rings. Furthermore, comparative analysis of free energy profiles indicates that alternations in the protein environment accelerate the dissociation of quinol molecules through the open LH1 ring. In particular, aromatic amino acids form π-stacking interactions with the quinol headgroup, resembling the key components in a conveyor belt system. This study provides insights into the molecular mechanisms that govern quinone/quinol exchange in bacterial photosynthesis and lays the framework for tuning electron flow and energy conversion to improve metabolic performance.

Keywords: electron transport; enhanced sampling; molecular dynamics simulations; photosynthesis; quinone/quinol.

Figure 1

Schematic models of the simulations of RC–LH1. A,B) Schematic diagrams of the closed RC–LH1 model. C,D) Schematic diagrams of the open RC–LH1 model. All quinone molecules are shown in orange, except for the quinone molecule at the Q_B site, which is highlighted in yellow licorice. Protein chains are presented as gray cartoon models, with the protein‐W in the open ring model displayed in blue. The porphyrin rings of bacteriochlorophylls are shown in green, and carotenoids are depicted in purple.

Figure 2

Principle of S‐RaMD‐MD simulation. The blue ellipse signifies the force application area, labeled as C; the gray ellipse represents the reference position, denoted as R. The straight arrow symbolizes a “reckless” forward movement, while the curved arrow signifies a “roundabout” forward movement. The green cylinder illustrates permissible range of movement for quinol molecules.

Figure 3

Differences in the mobility of quinones before and after reduction. A,B) The positional changes of quinone molecules before (Q_A/Q_B) and after (Q_A/Q_BH₂) reduction, respectively. The protein is represented by gray cartoon model, Q_A is shown in orange, Q_B in yellow, the iron ion in purple, and its coordinating residues in green. C) and D) The distance changes between the six‐carbon ring of the quinone head groups and the nonheme iron before (Q_A/Q_B) and after (Q_A/Q_BH₂) reduction, respectively.

Figure 4

Interactions between the Q_B/Q_BH₂ molecule and protein residues. A,B) The evolving interactions between the headgroups of Q_B/Q_BH₂ and protein residues, respectively. C) The interactions between Q_B and protein residues. D–F) The evolving interactions between Q_BH₂ and protein residues. Hydrogen bonds and water bridges are respectively represented by yellow and purple dashed lines, while π‐stacking is indicated by black dashed lines. The Q_B/Q_BH₂ molecule is shown in yellow, and the amino acid residues E213, G226, H191, I225, F217, Y223, and A187 on the L‐subunit are shown in green licorice. The iron ion is displayed in purple VDW models, and its coordinating residues are shown in green lines. The water molecules involved in forming water bridges are denoted as W1 and W2. O_prox represents the proximal oxygen atom, O_dist represents the distal oxygen atom, O_prox‐m represents the oxygen atom on the proximal methoxy group, and O_dist‐m represents the oxygen atom on the distal methoxy group.

Figure 5

Schematic representation of the dissociation probabilities of quinol from different channels in closed RC–LH1. A) Dissociation with the head‐first mode. B) Dissociation with the tail‐first mode. The thickness of the yellow arrow represents the probability of dissociation, and the molecule presentation scheme is consistent with Figure 1.

Figure 6

Free energy changes during the dissociation process of quinol. A,B) depict schematics of dissociation with the head‐first and tail‐first modes, respectively. As the reaction coordinate increases, the color of the six‐carbon ring of the quinol head groups gradually changes from blue to red. The yellow dots represent reference points for the reaction coordinates. C) Comparison of the free energy changes between the head‐first and tail‐first dissociation modes.

Figure 7

Interaction and free energy changes during the quinol dissociation process in closed and open systems. A,B) The reaction coordinates and interaction changes for quinol dissociation in closed and open RC–LH1 systems, respectively. π‐stacking is indicated by green font, while hydrogen bonding is marked with blue‐gray font. As the reaction coordinate increases, the color of the six‐carbon ring of the quinol head groups gradually changes from blue to red. The yellow dots represent reference points of the reaction coordinates, with both systems using M‐W129's Cα atom. C,D) The free energy changes for the closed and open RC–LH1 systems, respectively. Key reaction coordinate sites are marked with four red dots labeled as a, b, c, and d.

Figure 8

Schematic representation of the dissociation probabilities of quinol from different channels in open RC–LH1. The thickness of the yellow arrow represents the probability of dissociation, and the molecule presentation scheme is consistent with Figure 1.