Two-Dimensional Electronic Spectroscopy of a Minimal Photosystem I Complex Reveals the Rate of Primary Charge Separation

Parveen Akhtar, Ido Caspy, Paweł J. Nowakowski, Tirupathi Malavath, Nathan Nelson, Howe Siang Tan*, Petar H. Lambrev*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

17 Scopus citations

Abstract

Photosystem I (PSI), found in all oxygenic photosynthetic organisms, uses solar energy to drive electron transport with nearly 100% quantum efficiency, thanks to fast energy transfer among antenna chlorophylls and charge separation in the reaction center. There is no complete consensus regarding the kinetics of the elementary steps involved in the overall trapping, especially the rate of primary charge separation. In this work, we employed two-dimensional coherent electronic spectroscopy to follow the dynamics of energy and electron transfer in a monomeric PSI complex fromSynechocystisPCC 6803, containing only subunits A-E, K, and M, at 77 K. We also determined the structure of the complex to 4.3 Å resolution by cryoelectron microscopy with refinements to 2.5 Å. We applied structure-based modeling using a combined Redfield-Förster theory to compute the excitation dynamics. The absorptive 2D electronic spectra revealed fast excitonic/vibronic relaxation on time scales of 50-100 fs from the high-energy side of the absorption spectrum. Antenna excitations were funneled within 1 ps to a small pool of chlorophylls absorbing around 687 nm, thereafter decaying with 4-20 ps lifetimes, independently of excitation wavelength. Redfield-Förster energy transfer computations showed that the kinetics is limited by transfer from these red-shifted pigments. The rate of primary charge separation, upon direct excitation of the reaction center, was determined to be 1.2-1.5 ps-1. This result implies activationless electron transfer in PSI.

Original languageEnglish
Pages (from-to)14601-14612
Number of pages12
JournalJournal of the American Chemical Society
Volume143
Issue number36
DOIs
StatePublished - 15 Sep 2021

Funding

FundersFunder number
Eötvös Loránd Research NetworkKÖ-37/2020
Singapore Ministry of Education Academic Research FundRG14/20, RG2/19
National Institutes of Health
National Institute of General Medical SciencesR01GM129325
National Institute of General Medical Sciences
National Institute of Allergy and Infectious Diseases
Wellcome Trust
Medical Research Council
Biotechnology and Biological Sciences Research Council
German-Israeli Foundation for Scientific Research and DevelopmentG-1483-207/2018
German-Israeli Foundation for Scientific Research and Development
Israel Science Foundation569/17
Israel Science Foundation
Nemzeti Kutatási Fejlesztési és Innovációs Hivatal2018-1.2.1-NKP-2018-000009
Nemzeti Kutatási Fejlesztési és Innovációs Hivatal
National Research, Development and Innovation Office

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