Structural basis for excited light transfer within bacterial photosynthetic supercomplex.

Abstract

Single-particle cryogenic electron microscopy (cryo-EM) enables the visualization of membrane protein supercomplexes in their native-like conditions. In green sulfur bacteria (GSB), the photochemical reaction center (RC) features a homodimeric architecture for charge separation across the membrane. We extracted the photosynthetic supercomplex from Chlorobaculum tepidum cells with a mild detergent and determined high-resolution structures of the supercomplex using single-particle cryo-EM. In the cryo-EM density, the supercomplex is assembled based on a symmetric RC core with two Fenna-Matthews-Olson (FMO) trimers, two cytochrome c subunits (PscC), and small membrane subunits. The two FMO trimers bind to the dimeric RC cytoplasmic surface with different interfaces, resulting in an asymmetric feature of the supercomplex. The cryo-EM density also reveals two accessory protein subunits, PscE and PscF, which have not been identified before. We also discovered additional pigments within the complex, especially a linker bacteriochlorophyll (BChl) located in one of the two FMO-PscA interfaces, possibly mediating the exciton transfer from the FMO trimer to the RC core. We further computed the fluorescence resonance energy transfer (FRET) rate between determined pigments and found that the excited light energy transfer is biased on one of the two FMO-PscA branches. Our structure of the GSB photosynthetic supercomplex provides mechanistic insights into the routes for light excitation energy transfer and a possible evolutionary transition intermediate of the bacterial photosynthetic supercomplex from the primitive homodimeric RC.