Protein Influence on Charge-Asymmetry of the Primary Donor in Photosynthetic Bacterial Reaction Centers Containing a Heterodimer: Effects on Photophysical Properties and Electron Transfer

• Published in: The journal of physical chemistry. B Vol. 117; no. 15; pp. 4028 - 4041
• Main Authors: Harris, Michelle A, Luehr, Craig A, Faries, Kaitlyn M, Wander, Marc, Kressel, Lucas, Holten, Dewey, Hanson, Deborah K, Laible, Philip D, Kirmaier, Christine
• Format: Journal Article
• Language: English
• Published: Washington, DC American Chemical Society 18.04.2013
• Subjects: Asymmetry; Bacteria; Biological and medical sciences; Charge; Dimerization; Electron transfer; Electron Transport; Electronics; Electrons; Fundamental and applied biological sciences. Psychology; Ground state; Hydrogen Bonding; Magnetohydrodynamics; Models, Molecular; Molecular biophysics; Mutation; Photochemical Processes; Photochemistry. Photosynthesis. Bioluminescence; Photosynthetic Reaction Center Complex Proteins - chemistry; Photosynthetic Reaction Center Complex Proteins - metabolism; Radiation-biomolecule interaction; Rate constants; Rhodobacter capsulatus; Rhodobacter sphaeroides - chemistry; Rhodobacter sphaeroides - genetics; Rhodobacter sphaeroides - metabolism; Reaction mechanism; Electron transfer; Bacteria; Asymmetry; Photosynthesis; Protein
• ISSN: 1520-6106; 1520-5207
• DOI: 10.1021/jp401138h

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Mhd-β RCs serve as the initial templates in the two mutant sets, where β denotes that the L-side BPh acceptor (HL) has been replaced by a BChl (due to substituting His for Leu M212).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.