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Title: Switching sides—Reengineered primary charge separation in the bacterial photosynthetic reaction center

Abstract

We report 90% yield of electron transfer (ET) from the singlet excited state P* of the primary electron-donor P (a bacteriochlorophyll dimer) to the B-side bacteriopheophytin (HB) in the bacterial photosynthetic reaction center (RC). Starting from a platform Rhodobacter sphaeroides RC bearing several amino acid changes, an Arg in place of the native Leu at L185—positioned over one face of HB and only ~4 Å from the 4 central nitrogens of the HB macrocycle—is the key additional mutation providing 90% yield of P+HB-. This all but matches the near-unity yield of A-side P+HA- charge separation in the native RC. The 90% yield of ET to HB derives from (minimally) 3 P* populations with distinct means of P* decay. In an ~40% population, P* decays in ~4 ps via a 2-step process involving a short-lived P+BB- intermediate, analogous to initial charge separation on the A side of wild-type RCs. In an ~50% population, P* → P+HB- conversion takes place in ~20 ps by a superexchange mechanism mediated by BB. An ~10% population of P* decays in ~150 ps largely by internal conversion. These results address the long-standing dichotomy of A- versus B-side initial charge separation in native RCs and have implicationsmore » for the mechanism(s) and timescale of initial ET that are required to achieve a near-quantitative yield of unidirectional charge separation« less

Authors:
ORCiD logo; ORCiD logo; ORCiD logo; ; ORCiD logo; ORCiD logo; ORCiD logo
Publication Date:
Research Org.:
Washington Univ., St. Louis, MO (United States); Argonne National Lab. (ANL), Argonne, IL (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1580676
Alternate Identifier(s):
OSTI ID: 1671638; OSTI ID: 1696796
Grant/Contract Number:  
AC02-06CH11357; SC0002036
Resource Type:
Published Article
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Volume: 117 Journal Issue: 2; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences
Country of Publication:
United States
Language:
English
Subject:
14 SOLAR ENERGY; 59 BASIC BIOLOGICAL SCIENCES; bacteriochlorophyll dimer; mutant reaction center; protein dynamics; protein distributions; ultrafast transient absorption spectroscopy; electron transfer; photosynthesis; ultrafast spectroscopy

Citation Formats

Laible, Philip D., Hanson, Deborah K., Buhrmaster, James C., Tira, Gregory A., Faries, Kaitlyn M., Holten, Dewey, and Kirmaier, Christine. Switching sides—Reengineered primary charge separation in the bacterial photosynthetic reaction center. United States: N. p., 2019. Web. doi:10.1073/pnas.1916119117.
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Laible, Philip D., Hanson, Deborah K., Buhrmaster, James C., Tira, Gregory A., Faries, Kaitlyn M., Holten, Dewey, & Kirmaier, Christine. Switching sides—Reengineered primary charge separation in the bacterial photosynthetic reaction center. United States. https://doi.org/10.1073/pnas.1916119117
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Laible, Philip D., Hanson, Deborah K., Buhrmaster, James C., Tira, Gregory A., Faries, Kaitlyn M., Holten, Dewey, and Kirmaier, Christine. Tue . "Switching sides—Reengineered primary charge separation in the bacterial photosynthetic reaction center". United States. https://doi.org/10.1073/pnas.1916119117.
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@article{osti_1580676,
title = {Switching sides—Reengineered primary charge separation in the bacterial photosynthetic reaction center},
author = {Laible, Philip D. and Hanson, Deborah K. and Buhrmaster, James C. and Tira, Gregory A. and Faries, Kaitlyn M. and Holten, Dewey and Kirmaier, Christine},
abstractNote = {We report 90% yield of electron transfer (ET) from the singlet excited state P* of the primary electron-donor P (a bacteriochlorophyll dimer) to the B-side bacteriopheophytin (HB) in the bacterial photosynthetic reaction center (RC). Starting from a platform Rhodobacter sphaeroides RC bearing several amino acid changes, an Arg in place of the native Leu at L185—positioned over one face of HB and only ~4 Å from the 4 central nitrogens of the HB macrocycle—is the key additional mutation providing 90% yield of P+HB-. This all but matches the near-unity yield of A-side P+HA- charge separation in the native RC. The 90% yield of ET to HB derives from (minimally) 3 P* populations with distinct means of P* decay. In an ~40% population, P* decays in ~4 ps via a 2-step process involving a short-lived P+BB- intermediate, analogous to initial charge separation on the A side of wild-type RCs. In an ~50% population, P* → P+HB- conversion takes place in ~20 ps by a superexchange mechanism mediated by BB. An ~10% population of P* decays in ~150 ps largely by internal conversion. These results address the long-standing dichotomy of A- versus B-side initial charge separation in native RCs and have implications for the mechanism(s) and timescale of initial ET that are required to achieve a near-quantitative yield of unidirectional charge separation},
doi = {10.1073/pnas.1916119117},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 2,
volume = 117,
place = {United States},
year = {2019},
month = {12}
}
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