Shedding Light on Primary Donors in Photosynthetic Reaction Centers

Abstract

Chlorophylls (Chl)s exist in a variety of flavors and are ubiquitous in both the energy and electron transfer processes of photosynthesis. The functions they perform often occur on the ultrafast (fs–ns) time scale and until recently, these have been difficult to measure in real time. Further, the complexity of the binding pockets and the resulting protein-matrix effects that alter the respective electronic properties have rendered theoretical modeling of these states difficult. Recent advances in experimental methodology, computational modeling, and emergence of new reaction center (RC) structures have renewed interest in these processes and allowed researchers to elucidate previously ambiguous functions of Chls and related pheophytins. This is complemented by a wealth of experimental data obtained from decades of prior research. Studying the electronic properties of Chl molecules has advanced our understanding of both the nature of the primary charge separation and subsequent electron transfer processes of RCs. In this review, we examine the structures of primary electron donors in Type I and Type II RCs in relation to the vast body of spectroscopic research that has been performed on them to date. Further, we present density functional theory calculations on each oxidized primary donor to study both their electronic properties and our ability to model experimental spectroscopic data. This allows us to directly compare the electronic properties of hetero- and homodimeric RCs.

Primary donor triplet states of Photosystem I and II studied by Q-band pulse ENDOR spectroscopy

“…Charge recombination from the (triplet) primary RP then leads to the formation of the triplet state of the primary donor (Okamura et al 1987 ; Telfer et al 1988 ; Setif and Bottin 1989 ; Budil and Thurnauer 1991 ; Brettel 1997 ; Lubitz 2002 ). Note, that it is not a priori clear on which of the Chls belonging to the RC the triplet state is located; a similar problem exists for the earliest steps of charge separation where different Chls or groups of Chls have been discussed as potential primary donor (Gorka et al 2021 ), i.e., the exact nature of the primary donor is not fully understood. In contrast, the location of the longer-lived oxidized “primary donor” P ·+ has been well established over the years using a combination of various spectroscopic techniques, mutagenesis, isotope labeling and the availability of high-resolution crystal structures (Gorka et al 2021 ).…”

“…Note, that it is not a priori clear on which of the Chls belonging to the RC the triplet state is located; a similar problem exists for the earliest steps of charge separation where different Chls or groups of Chls have been discussed as potential primary donor (Gorka et al 2021 ), i.e., the exact nature of the primary donor is not fully understood. In contrast, the location of the longer-lived oxidized “primary donor” P ·+ has been well established over the years using a combination of various spectroscopic techniques, mutagenesis, isotope labeling and the availability of high-resolution crystal structures (Gorka et al 2021 ). We follow the standard practice to name the “primary donor” triplets generated by charge recombination 3 P700 and 3 P680 in PSI and PSII, respectively, without implying the assignment to a specific cofactor(s), and also use the term “primary donor” for the long-lived P ·+ state in both PSI and PSII.…”

Capacity and kinetics of light-induced cytochrome oxidation in intact cells of photosynthetic bacteria

“…The donor side, however, is more tolerant of possible donors in different strains 9 , 10 . Many purple bacteria (e.g., Rvx.…”

Coupled charge and energy transfer dynamics in light harvesting complexes from a hybrid hierarchical equations of motion approach

“…Photosynthetic systems rely on both electronic excitation energy transfer and charge transfer processes to perform the reactions that sustain life on Earth. [1][2][3][4][5] For example, excitation energy transfer (EET) and charge transfer (CT) play fundamental roles in reaction centers, 4 where light energy from the Sun is harvested to drive chemical reactions. Charge transfer is also likely have an important photo-protective function in photosynthetic organisms, [6][7][8][9][10] by quenching excess excitation energy and preventing damage to photosynthetic systems.…”