title: Protein influence on charge-asymmetry of the primary donor in photosynthetic bacterial reaction centers containing a heterodimer: effects on photophysical properties and electron transfer.
abstract: The substantial electronic distinctions between bacteriochlorophyll (BChl) and its Mg-free analogue bacteriopheophytin (BPh) are exploited in two sets of Rhodobacter capsulatus reaction center (RC) mutants that contain a heterodimeric BChl-BPh primary electron donor (D). The BPh component of the M-heterodimer (Mhd) or L-heterodimer (Lhd) obtains from substituting a Leu for His M200 or for His L173, respectively. Lhd-β and Mhd-β RCs serve as the initial templates in the two mutant sets, where β denotes that the L-side BPh acceptor (HL) has been replaced by a BChl (due to substituting His for Leu M212). Three variants each of Lhd-β and Mhd-β mutants were constructed: (1) a swap (denoted YF) of the native Phe (L181) and Tyr (M208) residues, which flank D and the nearby M- and L-side monomeric BChl cofactors, respectively, giving Tyr (L181) and Phe (M208); (2) addition of a hydrogen bond (denoted L131LH) to the ring V keto group of the L-macrocycle of D, via replacing the native Leu at L131 with His; (3) the combination of 1 and 2. A low yield of electron transfer (ET) to the M-side BPh (HM) is observed in all four Lhd-containing RCs. Comparison with the yield of ET to β on the L-side shows that electron density on the L-macrocycle of D* favors ET to the M-side cofactors and vice versa. Increasing or decreasing the electronic asymmetry of D* via the YF, L131LH mutations or the combination results in consistent trends in the characteristics of the long-wavelength ground state absorption band of D, the rate constant of internal conversion of D* to the ground state, and the rate constants for ET to both the L- and M-side cofactors. A surprising correlation is that an increase in the charge asymmetry in D* not only increases the D* internal-conversion rate constant, but also the rate constants for ET to both the L- and M-side cofactors, spanning time scales of tens of picoseconds to several nanoseconds. The YF swap has a previously unrecognized effect on the electronic asymmetry of D*, resulting in increased charge asymmetry for the Mhd and decreased charge asymmetry for the Lhd. This result indicates that the native Tyr (M208) and Phe (L181) in the wild-type RC promote an electron distribution in P* that is the reverse of that favorable for ET to the photoactive L-branch. This conclusion reinforces the view that the native configuration of these residues promotes ET to the L branch primarily by poising the free energies of the charge-separated states. Overall, this work addresses the extent to which electronic couplings complement energetics in underpinning the directionality of ET in the bacterial RC.
authors.affiliation: Department of Chemistry, Washington University, St. Louis, Missouri 63130, USA.
authors.forename: Michelle A
authors.initials: MA
authors.lastname: Harris
authors.forename: Craig A
authors.initials: CA
authors.lastname: Luehr
authors.forename: Kaitlyn M
authors.initials: KM
authors.lastname: Faries
authors.forename: Marc
authors.initials: M
authors.lastname: Wander
authors.forename: Lucas
authors.initials: L
authors.lastname: Kressel
authors.forename: Dewey
authors.initials: D
authors.lastname: Holten
authors.forename: Deborah K
authors.initials: DK
authors.lastname: Hanson
authors.forename: Philip D
authors.initials: PD
authors.lastname: Laible
authors.forename: Christine
authors.initials: C
authors.lastname: Kirmaier
mesh_terms: D019281:Dimerization; D004579:Electron Transport; D004583:Electrons; D006860:Hydrogen Bonding; D008958:Models, Molecular; D009154:Mutation; D055668:Photochemical Processes; D045322:Photosynthetic Reaction Center Complex Proteins / Q000737:chemistry / Q000378:metabolism*; D012242:Rhodobacter sphaeroides / Q000737:chemistry / Q000235:genetics / Q000378:metabolism*
chemical_list: D045322:Photosynthetic Reaction Center Complex Proteins