Electronic structure and energetics of a heterodimeric BChl g '/Chl a ' special pair generated by exposure of Heliomicrobium modesticaldum to dioxygen.

Heliobacteria are anoxygenic phototrophs that have a Type I homodimeric reaction center containing bacteriochlorophyll g (BChl g ). Previous experimental studies have shown that in the presence of light and dioxygen, BChl g is converted into 8 1 -OH-chlorophyll a F (hereafter Chl a F ), with an accompanying loss of light-driven charge separation. These studies suggest that the reaction center only loses the ability to transfer electrons once both BChl g ' molecules of the P 800 special pair have been converted to Chl a F '. The present work confirms that the partially converted BChl g '/Chl a F ' special pair remains functional in samples exposed to dioxygen by demonstrating its presence using hyperfine couplings obtained from Q-band 1 H ENDOR, 2D 14 N HYSCORE and DFT methods. The DFT calculations of the BChl g '/BChl g ' homodimeric primary donor, which are based on the recently published X-ray crystal structure, predict that the unpaired electron spin is equally delocalized over both BChl g ' molecules and provide an excellent match to the experimental hyperfine couplings of the anaerobic samples. Exposure to dioxygen leads to substantial changes in the hyperfine interactions, indicative of greater localization of the unpaired electron spin. The measured hyperfine couplings are reproduced in the DFT calculations by replacing one of the BChl g ' molecules of the primary donor with a Chl a F ' molecule. The calculations reveal that the spin density becomes localized on BChl g ' in the heterodimeric primary donor. Time-dependent DFT calculations demonstrate that conversion of either or both of the accessory BChl g molecules and/or one of the BChl g ' molecules of P 800 to Chl a F ' results in minor effects on the energy of the charge-separated states. In contrast, if both of the BChl g ' molecules of P 800 are converted a large increase in the energy of the charge-separated state occurs. This suggests that the reaction center remains functional when only one half of the dimer is converted, however, conversion of both halves of the P 800 dimer leads to loss of function.