Modified molecular interactions of the pheophytin and plastoquinone electron acceptors in photosystem II of chlorophyll D-containing Acaryochloris marina as revealed by FTIR spectroscopy.

Acaryochloris marina is a unique cyanobacterium that contains chlorophyll (Chl) d as a major pigment. Because Chl d has smaller excitation energy than Chl a used in ordinary photosynthetic organisms, the energetics of the photosystems of A. marina have been the subject of interest. It was previously shown that the redox potentials (E m's) of the redox-active pheophytin a (Pheo) and the primary plastoquinone electron acceptor (QA) in photosystem II (PSII) of A. marina are higher than those in Chl a-containing PSII, to compensate for the smaller excitation energy of Chl d (Allakhverdiev et al., Proc Natl Acad Sci USA 107: 3924-3929, 2010; ibid. 108: 8054-8058, 2011). To clarify the mechanisms of these E m increases, in this study, we have investigated the molecular interactions of Pheo and QA in PSII core complexes from A. marina using Fourier transform infrared (FTIR) spectroscopy. Light-induced FTIR difference spectra upon single reduction of Pheo and QA showed that spectral features in the regions of the keto and ester C=O stretches and the chlorin ring vibrations of Pheo and in the CO/CC stretching region of the Q A (-) semiquinone anion in A. marina are significantly different from those of the corresponding spectra in Chl a-containing cyanobacteria. These observations indicate that the molecular interactions, including the hydrogen bond interactions at the C=O groups, of these cofactors are modified in their binding sites of PSII proteins. From these results, along with the sequence information of the D1 and D2 proteins, it is suggested that A. marina tunes the E m's of Pheo and QA by altering nearby hydrogen bond networks to modify the structures of the binding pockets of these cofactors.