Excited-state structure and energy-transfer dynamics in various photosynthetic antenna complexes: hole-burning and modeling studies

Abstract

Natural photosynthesis has been an inspiration for solving humankind’s urgent demand for replacing fossil energy sources with renewable forms of energy. Knowledge of the molecular mechanisms that lies behind photosynthetic processes is essential for designing novel devices capable of producing solar fuel. Great efforts are being made to understand the first steps of photosynthesis, in particular light-harvesting and excitation energy transfer (EET). In this work, to overcome the static disorder in protein complexes and provide insight into both inhomogeneous and homogeneous line broadening, as well as the excitonic structure and dynamics in various photosynthetic proteins, we use site-selective frequency-domain hole burning (HB) spectroscopy. Complexes studied in detail include: i) wild type (WT) CP29 and CP47 antenna complexes of Photosystem II (PSII), and ii) chlorosome-baseplate proteins of two different green bacteria families (Cb. tepidum and Cfx. aurantiacus). Experimental and modeling results obtained for these complexes shed more light on their excitonic structure and EET dynamics. Simultaneous modeling of various types of optical spectra is based on a non-Markovian reduced density matrix approach. For example, we demonstrate that improved simultaneous fits of absorption, emission, circularly polarized luminescence, circular dichroism, and nonresonant hole-burned spectra, provide new information on the excitonic structure of intact and destabilized CP47 complexes and their lowest energy state(s). Regarding the reconstituted wild-type CP29 protein antenna we show that, depending on the laser excitation frequency, reconstituted complexes display two (independent) low-E states (i.e., the A and B traps) with different HB and emission spectra. We argue that with two subpopulations identified, only the major one corresponds to the native folding of CP29, whereas the minor conformation occurs only in reconstituted complexes. The lowest energy state of the major subpopulation is mostly delocalized over the a611, a612, a615 Chl trimer, and that of the minor one is localized on Chl a604. Studies of the Cb. tepidum and Cfx. aurantiacus baseplates reveal that in both complexes excitation energy is transferred to a localized low-energy trap state near 818 nm with similar rates, most likely via exciton hopping. These data are consistent with the model in which baseplate CsmA proteins are arranged as dimers containing two Bchl a molecules sandwiched between the hydrophobic protein regions.