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Title: Manipulating the Energetics and Rates of Electron Transfer in Rhodobacter capsulatus Reaction Centers with Asymmetric Pigment Content

Abstract

Seemingly redundant parallel pathways for electron transfer (ET), composed of identical sets of cofactors, are a cornerstone feature of photosynthetic reaction centers (RCs) involved in light-energy conversion. In native bacterial RCs, both A and B branches house one bacteriochlorophyll (BChl) and one bacteriopheophytin (BPh), but the A branch is used exclusively. Described herein are the results-obtained for two Rhodobacter capsulatus RCs with an unnaturally high degree of cofactor asymmetry, two BPh on the RC's B side and two BChl on the A side. These pigment changes derive, respectively, from the His(M180)Leu mutation [a BPh ((Phi(B)) replaces the B-side BChl (BB)], and the Leu(M212)His mutation [a BChl (beta(A))) replaces the A-side BPh (H-A)]. Additionally, Tyr(M208)Phe was employed to disfavor ET to the A branch; in one mutant, Val(M131)Glu creates a hydrogen bond to H-B to enhance ET to H-B. In both Phi(B) mutants, the decay kinetics of the excited primary ET donor (P*) resolve three populations with lifetimes of similar to 9 ps (50-60%), similar to 40 ps (10-20%), and similar to 200 ps (20-30%), with P+Phi(-)(B) formed predominantly from the 9 ps fraction. The 50-60% yield of P+Phi(B)- is the highest yet observed for a Phi(B)-containing RC. The results providemore » insight into factors needed for efficient multistep ET.« less

Authors:
 [1];  [2];  [2];  [1];  [2]; ORCiD logo [1]
  1. Department of Chemistry, Washington University, St. Louis, Missouri 63130, United States
  2. Biosciences Division, Argonne National Laboratory, Lemont, Illinois 60439, United States
Publication Date:
Research Org.:
Argonne National Lab. (ANL), Argonne, IL (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)
OSTI Identifier:
1416978
DOE Contract Number:
AC02-06CH11357
Resource Type:
Journal Article
Resource Relation:
Journal Name: Journal of Physical Chemistry. B, Condensed Matter, Materials, Surfaces, Interfaces and Biophysical Chemistry; Journal Volume: 121; Journal Issue: 29
Country of Publication:
United States
Language:
English

Citation Formats

Faries, Kaitlyn M., Dylla, Nicholas P., Hanson, Deborah K., Holten, Dewey, Laible, Philip D., and Kirmaier, Christine. Manipulating the Energetics and Rates of Electron Transfer in Rhodobacter capsulatus Reaction Centers with Asymmetric Pigment Content. United States: N. p., 2017. Web. doi:10.1021/acs.jpcb.7b01389.
Faries, Kaitlyn M., Dylla, Nicholas P., Hanson, Deborah K., Holten, Dewey, Laible, Philip D., & Kirmaier, Christine. Manipulating the Energetics and Rates of Electron Transfer in Rhodobacter capsulatus Reaction Centers with Asymmetric Pigment Content. United States. doi:10.1021/acs.jpcb.7b01389.
Faries, Kaitlyn M., Dylla, Nicholas P., Hanson, Deborah K., Holten, Dewey, Laible, Philip D., and Kirmaier, Christine. 2017. "Manipulating the Energetics and Rates of Electron Transfer in Rhodobacter capsulatus Reaction Centers with Asymmetric Pigment Content". United States. doi:10.1021/acs.jpcb.7b01389.
@article{osti_1416978,
title = {Manipulating the Energetics and Rates of Electron Transfer in Rhodobacter capsulatus Reaction Centers with Asymmetric Pigment Content},
author = {Faries, Kaitlyn M. and Dylla, Nicholas P. and Hanson, Deborah K. and Holten, Dewey and Laible, Philip D. and Kirmaier, Christine},
abstractNote = {Seemingly redundant parallel pathways for electron transfer (ET), composed of identical sets of cofactors, are a cornerstone feature of photosynthetic reaction centers (RCs) involved in light-energy conversion. In native bacterial RCs, both A and B branches house one bacteriochlorophyll (BChl) and one bacteriopheophytin (BPh), but the A branch is used exclusively. Described herein are the results-obtained for two Rhodobacter capsulatus RCs with an unnaturally high degree of cofactor asymmetry, two BPh on the RC's B side and two BChl on the A side. These pigment changes derive, respectively, from the His(M180)Leu mutation [a BPh ((Phi(B)) replaces the B-side BChl (BB)], and the Leu(M212)His mutation [a BChl (beta(A))) replaces the A-side BPh (H-A)]. Additionally, Tyr(M208)Phe was employed to disfavor ET to the A branch; in one mutant, Val(M131)Glu creates a hydrogen bond to H-B to enhance ET to H-B. In both Phi(B) mutants, the decay kinetics of the excited primary ET donor (P*) resolve three populations with lifetimes of similar to 9 ps (50-60%), similar to 40 ps (10-20%), and similar to 200 ps (20-30%), with P+Phi(-)(B) formed predominantly from the 9 ps fraction. The 50-60% yield of P+Phi(B)- is the highest yet observed for a Phi(B)-containing RC. The results provide insight into factors needed for efficient multistep ET.},
doi = {10.1021/acs.jpcb.7b01389},
journal = {Journal of Physical Chemistry. B, Condensed Matter, Materials, Surfaces, Interfaces and Biophysical Chemistry},
number = 29,
volume = 121,
place = {United States},
year = 2017,
month = 7
}
  • From the crystal structures of reaction centers (RCs) from purple photosynthetic bacteria, two pathways for electron transfer (ET) are apparent but only one pathway (the A side) operates in the native protein-cofactor complex. Partial activation of the B-side pathway has unveiled the true inefficiencies of ET processes on that side in comparison to analogous reactions on the A side. Of significance are the relative rate constants for forward ET and the competing charge recombination reactions. On the B side, these rate constants are nearly equal for the secondary charge-separation step (ET from bacteriopheophytin to quinone), relegating the yield of thismore » process to < 50%. Herein we report efforts to optimize this step. In surveying all possible residues at position 131 in the M subunit, we discovered that when glutamic acid replaces the native valine the efficiency of the secondary ET is nearly two-fold higher than in the wild-type RC. The positive effect of M131 Glu is likely due to formation of a hydrogen bond with the ring V keto group of the B-side bacteriopheophytin leading to stabilization of the charge-separated state involving this cofactor. In conclusion, this change slows charge recombination by roughly a factor of two and affords the improved yield of the desired forward ET to the B-side quinone terminal acceptor.« less
  • From the crystal structures of reaction centers (RCs) from purple photosynthetic bacteria, two pathways for electron transfer (ET) are apparent but only one pathway (the A side) operates in the native protein-cofactor complex. Partial activation of the B-side pathway has unveiled the true inefficiencies of ET processes on that side in comparison to analogous reactions on the A side. Of significance are the relative rate constants for forward ET and the competing charge recombination reactions. On the B side, these rate constants are nearly equal for the secondary charge-separation step (ET from bacteriopheophytin to quinone), relegating the yield of thismore » process to < 50%. Herein we report efforts to optimize this step. In surveying all possible residues at position 131 in the M subunit, we discovered that when glutamic acid replaces the native valine the efficiency of the secondary ET is nearly two-fold higher than in the wild-type RC. The positive effect of M131 Glu is likely due to formation of a hydrogen bond with the ring V keto group of the B-side bacteriopheophytin leading to stabilization of the charge-separated state involving this cofactor. In conclusion, this change slows charge recombination by roughly a factor of two and affords the improved yield of the desired forward ET to the B-side quinone terminal acceptor.« less
  • The kinetics and relative yields of the two decay pathways of the initially observed transient state (D{sup {plus minus}}) in photosynthetic reaction centers from the His{sup M200} {yields} Leu mutant of Rhodobacter capsulatus have been studied at 285 and 77 K. At both temperatures, the lifetime of D{sup {plus minus}}, which has mainly the character of the lowest intradimer charge-transfer state of the bacteriochlorophyll/bacteriopheophytin heterodimer, is about 17 ps; the yields of electron transfer from D{sup {plus minus}} to the normal bacteriopheophytin acceptor and of internal conversion (charge recombination) to the ground state are both about 50% at 285 andmore » 77 K. The finding that the rates of these two energetically different decay pathways of D{sup {plus minus}} are both essentially independent of temperatures is discussed in terms of molecular factors that may underlie activationless electron transfer in the reaction center and contribute to the high quantum yield of charge separation.« less
  • Resonance Raman (RR) spectra are reported for photosynthetic reaction centers (RC's) from the purple bacterium Rhodobacter sphaeroides. The spectra of quinone-reduced RC's were obtained by using a large number of excitation wavelengths (23) in the 335-875-nm range. These wavelengths span the B[sub x], B[sub y], Q[sub x], and Q[sub y] absorption bands of the special pair bacteriochlorophyll (P), accessory bacteriochlorophyll (BCh), and bacteriopheophytin (BPh) pigments. The number of exciting lines and their wavelengths were chosen to optimize the selective excitation of the different pigments in the RC and to elicit the full complement of RR scattering from the individual pigments.more » The RR spectra of the quinone-reduced RC's were compared with one another and with those of chemically oxidized RC's, tetrapyrrolic model compounds, and BCh/BPh in solution. On the basis of these comparisons, a self-consistent set of vibrational assignments is proposed for the high-frequency (1425-1750 cm[sup [minus]1]) carbonyl and skeletal modes of the six bacteriochlorin pigments in the protein. These assignments were aided by the results of semiempirical normal coordinate calculations. 59 refs., 11 figs., 3 tabs.« less