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

Laible, Philip D.; Hanson, Deborah K.; Buhrmaster, James C.; Tira, Gregory A.; Faries, Kaitlyn M.; Holten, Dewey; Kirmaier, Christine

doi:10.1073/pnas.1916119117

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

Journal Article · 30 December 2019 · Proceedings of the National Academy of Sciences of the United States of America

DOI: https://doi.org/10.1073/pnas.1916119117 · OSTI ID:1580676

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; Tira, Gregory A.;

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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 (H _B ) 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 H _B and only ∼4 Å from the 4 central nitrogens of the H _B macrocycle—is the key additional mutation providing 90% yield of P ⁺ H _B ⁻ . This all but matches the near-unity yield of A-side P ⁺ H _A ⁻ charge separation in the native RC. The 90% yield of ET to H _B 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 ⁺ B _B ⁻ intermediate, analogous to initial charge separation on the A side of wild-type RCs. In an ∼50% population, P* → P ⁺ H _B ⁻ conversion takes place in ∼20 ps by a superexchange mechanism mediated by B _B . 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.

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Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States); Washington Univ., St. Louis, MO (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: AC02-06CH11357; SC0002036

OSTI ID:: 1580676

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Issue: 2 Vol. 117; ISSN 0027-8424

Publisher:: National Academy of SciencesCopyright Statement

Country of Publication:: United States

Language:: English

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59 BASIC BIOLOGICAL SCIENCES
bacteriochlorophyll dimer
electron transfer
mutant reaction center
photosynthesis
protein distributions
protein dynamics
ultrafast spectroscopy
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Title: Switching sides—Reengineered primary charge separation in the bacterial photosynthetic reaction center

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