Structure and Function of Quinones in Biological Solar Energy Transduction: A High-Frequency D-Band EPR Spectroscopy Study of Model Benzoquinones

Abstract

Quinones are utilized as charge-transfer cofactors in a wide variety of reactions that are crucial for photosynthesis and respiration. In photosynthetic protein complexes, both Type I and Type II, including oxygenic and anoxygenic reaction centers contain quinone cofactors that are known to participate in electron- and proton-transfer processes. Type II reaction centers, purple bacterial reaction centers, and photosystem II utilize benzoquinone molecules, ubiquinone, and plastoquinone, respectively, to facilitate proton-coupled electron transfer reactions. Here, we report a systematic study of the principal components of the g-tensor of an extensive library of model benzosemiquinone anion radicals in both protic (2-isopropanol) and aprotic (dimethyl sulfoxide) solvents using high-frequency EPR spectroscopy. A detailed comparison of the experimental g-values of the benzosemiquinone models at D-band EPR frequency allows for the discrimination of substituent effects and solvent hydrogen bonds on the principal components of the g-tensor. Further, we compare the primary plastosemiquinone, Q(A)(-), of photosystem II with the substituent and solvent hydrogen bond effects of benzosemiquinone models in vitro. This study significantly extends the experimental basis for elucidating the role of both molecular structure and interactions with environment on the functional tuning of quinone cofactors in biological solar energy transduction.