Elucidating the Role of Zinc-Bacteriochlorophyll A' in the Primary Photochemistry of Chloroacidobacterium thermophilum Reaction Centers

Abstract

Chloracidobacterium (Cab.) thermophilum is a microaerophilic, chlorophototrophic species in the phylum of Acidobacteria that contains homodimeric Type I reaction centers (RC). Photosynthetic RCs in bacteria convert light energy into chemical energy using (bacterio)chlorophyll ((B)Chl) cofactors. In addition to participating in energy transfer in the light-harvesting complexes, the (B)Chl molecules also act as the primary electron donor and primary electron acceptor in Type I RCs. Previously, reversed-phase high-performance liquid chromatography of Cab. thermophilum RCs revealed the presence of (B)Chl a, Chl a, and Zn2+-(B)Chl a' in a ratio of about 12.8:8.0:2.0. Moreover, it was shown that Cab. thermophilum uses chlorosomes and FMO for light harvesting, and synthesizes (B)Chl c in addition to (B)Chl a, Chl a, and Zn2+-(B)Chl a'. It has been demonstrated that Chl a is the primary electron acceptor in Cab. thermophilum RC and since Zn2+-(B)Chl a' is only present in the RC, it was suggested that it could function as the primary electron donor. In this study, we utilize high-resolution, two-dimensional (2D) 14N and 67Zn hyperfine sublevel correlation (HYSCORE) spectroscopy to determine the electronic and geometric structure of the primary donor cation, P840+, in the Cab. thermophilum RC. Additionally, we perform density functional theory (DFT) calculations to determine the electron spin-density distribution and electron-nuclear hyperfine coupling parameters of P840+ for comparison with the parameters that are obtained from the experimental 2D HYSCORE measurements. Our studies indicate that that the primary donor, P840, of the Cab. RC is comprised of Zn2+-sBChl a' molecules.