Electronic Structure Effects Related to the Origin of the Remarkable Near-Infrared Absorption of ' Light Harvesting 1-Reaction Center Complex.

Various photosynthetic organisms have evolved to absorb light in different regions of the visible light spectrum, thus adapting to the various lighting conditions available on Earth. While most of these autotrophic organisms absorb wavelengths around the 700-800 nm region, some are capable of red-shifted absorptions above this range, but none as remarkably as whose main absorption is observed at 1015 nm, approximately 220 nm (0.34 eV) lower in energy than their main constituent pigments, BChl-, whose main absorption is observed at 795 nm. The structure of its light harvesting 1-reaction center was recently elucidated by cryo-EM; however, the electronic structure details behind this red-shifted absorption remain unattended. We used hybrid quantum mechanics/molecular mechanics (QM/MM) calculations to optimize one of the active centers and performed classical molecular dynamics (MD) simulations to sample conformations beyond the optimized structure. We did excited state calculations with the time-dependent density functional theory method at the CAM-B3LYP/cc-pVDZ level of theory. We reproduced the near IR absorption by sequentially modifying the number of components involved in our systems using representative structures from the calculated MD ensemble. Natural transition orbital analysis reveals the participation of the BChl- fragments to the main transition in the native structure and the structures obtained from the QM/MM and MD simulations. H-bonding pigment-protein interactions play a role on the conformation stabilization and orientation; however, the bacteriochlorin ring conformations and the exciton delocalization are the most relevant factors to explain the red-shifting phenomenon.