Molecular Level Design Principle behind Optimal Sizes of Photosynthetic LH2 Complex: Taming Disorder through Cooperation of Hydrogen Bonding and Quantum Delocalization

Abstract

The light harvesting 2 (LH2) antenna complex from purple photosynthetic bacteria is an efficient natural excitation energy carrier with well-known symmetric structure, but the molecular level design principle governing its structure-function relationship is unknown. Our all-atomistic simulations of nonnatural analogues of LH2 as well as those of a natural LH2 suggest that nonnatural sizes of LH2-like complexes could be built. However, stable and consistent hydrogen bonding (HB) between bacteriochlorophyll and the protein is shown to be possible only near naturally occurring sizes, leading to significantly smaller disorder than for nonnatural ones. Extensive quantum calculations of intercomplex exciton transfer dynamics, sampled for a large set of disorder, reveal that taming the negative effect of disorder through a reliable HB as well as quantum delocalization of the exciton is a critical mechanism that makes LH2 highly functional, which also explains why the natural sizes of LH2 are indeed optimal.

The role of charge-transfer states in the spectral tuning of antenna complexes of purple bacteria

“…The most important residues contributing to the solvatochromic shift of α-BChl are the hydrogen-bonding residue (Trp(W)45 in B800-850 and Tyr(Y)41 in B800-820), and the close residues of the neighboring β-apoprotein, Ala(A)29 and His(H)30 for both complexes [39,40,41]. However, also the neighboring β-BChl on the same unit has a non-negligible contribution.…”

Delocalized excitons in natural light-harvesting complexes

“…Strümpfer and K. Schulten, 2012). Application of the GME-MED approach (Jang et al, 2014(Jang et al, , 2015 showed that the rate can change significantly depending on the realization of the disorder and the inter-LH2 distances that are consistent with AFM images. Figure 15 shows the distribution of rates at 300 K between two LH2 complexes separated by a center-tocenter distance of 7.5 nm.…”

“…The outcomes of these calculations, in combination with empirical correction factors to complement numerical errors, laid the foundation for many exciton models that followed. In addition, already in 2002, all atomistic MD simulation of LH2 complex was shown to be feasible (Damjanović et al, 2002), providing the basis for more recent advances (Cupellini et al, 2016;Jang et al, 2015;Montemayor et al, 2018;Olbrich and Kleinekathöfer, 2010;Sisto et al, 2017). In this section, some of the outcomes of these recent computational studies for the LH2 antenna complex of Rps.…”

“…In this result, the distribution of rates is purely due to the Gaussian disorder in the excitation energy of each BChl with standard deviation of 200 cm −1 . Consideration of the distribution of inter-LH2 distances will result in wider distribution of rates (Jang et al, 2015).…”

“…15 Distribution of LH2-LH2 rates (left panel) and average population decay (right panel) of exciton on the initial LH2. More details can be found in (Jang et al, 2015).…”