Electron-Nuclear Interactions in Natural Photosynthetic and Biomimetic Model Systems

This dissertation presents the application of two-dimensional electronic-vibrational (2DEV) spectroscopy to a progression of natural photosynthetic and biomimetic model systems where electron-nuclear interactions exert a significant influence on the overall functionality. In the introduction, we start by describing the unique aspects of the 2DEV spectroscopic method, including improved frequency resolution and the capability to track electronic-vibrational correlations, which are leveraged in the work presented in the subsequent chapters. Following this, the first half of this dissertation (Chapters 2-4) covers applications of 2DEV spectroscopy to light-harvesting complex II (LHCII) under various excitation conditions, as well as the development of theoretical models to aid in the understand of the observed spectra. Together, these experiments unveil the critical role of electronic-vibrational (or vibronic) mixing in facilitating efficient, ultrafast excitation energy transfer (EET) over the entire photosynthetically active region of the solar spectrum. Specifically, vibronic mixing is seen to facilitate EET over moderately large energy gaps, thus largely influencing the potential energy landscape, and ultimately bridging the spatial domains of groups of electronically coupled chlorophylls. In order to more deeply understand the mechanisms of vibronic mixing at play in the natural system, we describe the subsequent development of a model vibronic heterodimer system. This model, although still basic in comparison to LHCII, allows for a more critical examination of the observed 2DEV spectral features and strongly suggests that non-Condon effects are central to the EET mechanism in the complex. In the second half of this dissertation (Chapters 5-7), emphasis is placed on the photochemistry and photophysics relevant to photosynthetic reaction centers, rather than light-harvesting complexes. In particular, the application of 2DEV spectroscopy to the photosystem II reaction center (PSII-RC) is able to clearly distinguish, for the first time, the initial charge separation step which triggers the light to energy conversion process in the photosynthetic engine of green plants and algae. These experiments also reveal the role of exciton-charge transfer mixing as a potential mechanism for ensuring efficient charge separation in the PSII-RC. The charge separated species formed in this step ultimately triggers water splitting—leading to the production of molecular oxygen—which is responsible for life on earth as we know it. Specifically, this process is facilitated by the favorable energetics of an intervening proton-coupled electron transfer (PCET) reaction. However, studying this process directly in the natural system is difficult. In the remaining chapters, 2DEV spectroscopy is first used to study proton transfer in a model system, Indigo Carmine (a derivative of the well-known dye, Indigo). In this experiment, the long-debated mechanism of excited state intramolecular proton transfer is clarified and the role of the solvent in promoting this reaction is investigated. Additionally, this work distinguishes how proton transfer manifests in 2DEV spectra and serves to lay the groundwork for the subsequent investigation of a biomimetic model system for the PCET reaction in PSII. In the study of the biomimetic species, the observation of a non-equilibrium reaction pathway allows for nuanced insight into the complex dynamics and synergistic molecular motions involved in photoinduced PCET.We conclude with a discussion of future pursuits of the elusive relationship between electrons and nuclei in both natural and bioinspired photosynthetic systems, as well as promising improvements and other applications for the emerging method of 2DEV spectroscopy