Solid-State NMR Analysis of the Dynamics of Cofactors: Comparison of Heliobacterial and Purple Bacterial Reaction Centers

Photosynthetic reaction centers (RCs) serve as natural engines converting solar energy to chemical energy. Understanding the principles of efficient charge separation and light-induced electron transfer (ET) between the chlorophyll-type pigments might guide the synthesis for artificial photosynthetic systems. We present detailed insight into the dynamics at the atomic level using solid-state NMR techniques applied to the RCs of <i>Heliobacillus (Hb.) mobilis</i> (HbRCs) and the purple bacterium <i>Rhodobacter (R.) sphaeroides</i> (PbRCs). It is assumed that heliobacteria were among the first phototrophic organisms; therefore, their RC can be regarded as ancient. They are constructed homodimerically with perfect <i>C</i>₂ symmetry, enabling ET over both branches of cofactors. Modern RCs of <i>R. sphaeroides</i> wild-type (WT) have higher redox power and are functionally highly asymmetric. The dynamics of the cofactors in both RCs has been explored using nuclear hyperpolarization, induced by the solid-state photochemically induced dynamic nuclear polarization (photo-CIDNP) effect. Based on the individual incorporation of ¹³C positions of the cofactors (through supplementation by ¹³C-δ-aminolevulinic acid), photo-CIDNP magic-angle spinning (MAS) NMR experiments provide access to the local dynamics of the cofactors along the ET path over a broad range of time scales. Theoretical analysis of the dynamic deformation of these macrocycles is also discussed in terms of function. The dynamics observed in HbRCs appears to be correlated to ET. The cofactors in PbRC are significantly less dynamic than those in the HbRC. Relevance for efficiency and redox properties are discussed.