Why the Electron Chooses One of Two Symmetry-Related Paths in the Type II Bacterial Photosynthetic Reaction Centers

Photosynthetic reaction centers carry out a series of electron and proton transfer reactions that convert the energy of light into high energy reduced products and add to the proton gradient. All photosynthetic reaction centers (Photosystems I, II, Heliobacter, and bacterial reaction centers (bRCs)) have their charge separating cofactors arranged with two, c2-symmetric paths from primary donor to terminal acceptor. In Type II reaction centers (PSII and bRCs), electrons utilize only one active branch. In bRCs the electron transfer occurs in the A branch from the excited state of dimer P860 through BChlA, BPhA, to QA, and then to the B-branch QB. B-branch BChlB and BPhB do not participate. A similar path is found in PSII. These proteins challenge our understanding of how proteins can turn on or off the activity of bound ligands. The shift of the electrochemical midpoint potential (Em) of each cofactor by the protein environment is calculated using the continuum electrostatics within the MultiConformation Continuum Electrostatic program (MCCE). In bRCs from Rhodobacter sphaeroides, the electrostatic potentials favor reduction of the active branch cofactors. The residues that contribute to a more positive potential on the A branch are identified. These are often distant from the cofactors. The large difference of the potential at the competing BChls may direct the electron transfer to the A branch. Residues TyrM210 and PheL181 are at symmetrical positions on the A and B branches, near P860 and between BChlA or BChlB. Mutated bRCs that swap the Tyr and Phe (YF mutant), have been shown to support some electron transfer to the B-branch cofactors. The calculated Ems in the bRC with the YF swap show that more positive B-branch potentials help explain the electron transfer from excited P860 to the normally inactive B branch.