De novo design of proteins housing excitonically coupled chlorophyll special pairs

Identifier:  imarina:9369652

Handle: https://hdl.handle.net/20.500.11797/imarina9369652

Authors:  Ennist, NM; Wang, SZ; Kennedy, MA; Curti, M; Sutherland, GA; Vasilev, C; Redler, RL; Maffeis, V; Shareef, S; Sica, AV; Hua, AS; Deshmukh, AP; Moyer, AP; Hicks, DR; Swartz, AZ; Cacho, RA; Novy, N; Bera, AK; Kang, AL; Sankaran, B; Johnson, MP; Phadkule, A; Reppert, M; Ekiert, D; Bhabha, G; Stewart, L; Caram, JR; Stoddard, BL; Romero, E; Hunter, CN; Baker, D

Abstract:
Natural photosystems couple light harvesting to charge separation using a 'special pair' of chlorophyll molecules that accepts excitation energy from the antenna and initiates an electron-transfer cascade. To investigate the photophysics of special pairs independently of the complexities of native photosynthetic proteins, and as a first step toward creating synthetic photosystems for new energy conversion technologies, we designed C 2-symmetric proteins that hold two chlorophyll molecules in closely juxtaposed arrangements. X-ray crystallography confirmed that one designed protein binds two chlorophylls in the same orientation as native special pairs, whereas a second designed protein positions them in a previously unseen geometry. Spectroscopy revealed that the chlorophylls are excitonically coupled, and fluorescence lifetime imaging demonstrated energy transfer. The cryo-electron microscopy structure of a designed 24-chlorophyll octahedral nanocage with a special pair on each edge closely matched the design model. The results suggest that the de novo design of artificial photosynthetic systems is within reach of current computational methods. A de novo-designed protein that precisely assembles a chlorophyll dimer has been developed. The design matches the conformation of the native 'special pair' of chlorophylls that functions as the primary electron donor in natural photosynthetic reaction centers. In the designed protein, excitonically coupled chlorophylls participate in energy transfer. The proteins were also redesigned to assemble into 24-chlorophyll nanocages.