Diverse Transient\nChiral Dynamics in Evolutionary\nDistinct Photosynthetic Reaction Centers

The evolution of photosynthetic reaction centers (RCs)\nfrom anoxygenic\nbacteria to higher-order oxygenic cynobacteria and plants highlights\na remarkable journey of structural and functional diversification\nas an adaptation to environmental conditions. The role of chirality\nin these centers is important, influencing the arrangement and function\nof key molecules involved in photosynthesis. Investigating the role\nof chirality may provide a deeper understanding of photosynthesis\nand the evolutionary history of life on Earth. In this study, we explore\nchirality-related energy transfer in two evolutionarily distinct RCs:\none from the anoxygenic purple sulfur bacterium Thermochromatium\ntepidum (BRC) and the other from the oxygenic cyanobacterium Thermosynechococcus vulcanus (PSII RC), utilizing\ntwo-dimensional electronic spectroscopy (2DES). By employing circularly\npolarized laser pulses, we can extract transient chiral dynamics within\nthese RCs, offering a detailed view of their chiral contribution to\nenergy transfer processes. We also compute traditional 2DES and compare\nthese results with spectra related to circular dichroism. Our findings\nindicate that two-dimensional circular dichroism spectroscopy effectively\nreveals chiral dynamics, emphasizing the structural symmetries of\npigments and their interactions with associated proteins. Despite\nhaving similar pigment–protein architectures, the BRC and PSII\nRC exhibit significantly different chiral dynamics on an ultrafast\ntime scale. In the BRC, the complex contributions of pigments such\nas <i>BCh</i><sub><i>M</i></sub>, <i>BPh</i><sub><i>L</i></sub>, <i>BCh</i>, and <i>P</i><sub><i>M</i></sub> to key excitonic states lead\nto more pronounced chiral features and dynamic behavior. In contrast,\nthe PSII RC, although significantly influenced by <i>Chl</i><sub><i>D</i>1</sub> and <i>Chl</i><sub><i>D</i>2</sub>, shows less complex chiral effects and more subdued\nchiral dynamics. Notably, the PSII RC demonstrates a faster decay\nof coherence to localized excitonic populations compared to the BRC,\nwhich may represent an adaptive mechanism to minimize oxidative stress\nin oxygenic photosystems. By examining and comparing the chiral excitonic\ninteractions and dynamics of BRC and PSII RC, this study offers valuable\ninsights into the mechanisms of photosynthetic complexes. These findings\ncould contribute to understanding how the functional optimization\nof photosynthetic proteins in ultrafast time scales is linked to biological\nevolution.