TY - JOUR
T1 - Consistent Model of Ultrafast Energy Transfer in Peridinin Chlorophyll- A Protein Using Two-Dimensional Electronic Spectroscopy and Förster Theory
AU - Toa, Zi S.D.
AU - Degolian, Mary H.
AU - Jumper, Chanelle C.
AU - Hiller, Roger G.
AU - Scholes, Gregory D.
N1 - Funding Information:
Z.S.D.T. would like to thank Dr. Jacob Dean for getting him started on 2DES, enlightening discussions about the investigation, and providing helpful comments on the manuscript. Z.S.D.T. also acknowledges Elliot J. Taffet for inspiring and enlightening discussions regarding the quantum chemistry of peridinin. Z.S.D.T. acknowledges funding from the Taylor Fellowship provided by the Department of Chemistry, Princeton University. M.H.d. acknowledges funding from the Department of Chemistry, Princeton University, for undergraduate research. This work is generously funded by the Bioinspired Light-Escalated Chemistry Energy Frontier Research Center funded by the U.S. Department of Energy, Office of Science, Office of Basic Energy Sciences, under Award DE-SC0019370.
Publisher Copyright:
© 2019 American Chemical Society.
PY - 2019
Y1 - 2019
N2 - Solar light harvesting begins with electronic energy transfer in structurally complex light-harvesting antennae such as the peridinin chlorophyll-a protein from dinoflagellate algae. Peridinin chlorophyll-a protein is composed of a unique combination of chlorophylls sensitized by carotenoids in a 4:1 ratio, and ultrafast spectroscopic methods have previously been utilized in elucidating their energy-transfer pathways and timescales. However, due to overlapping signals from various chromophores and competing pathways and timescales, a consistent model of intraprotein electronic energy transfer has been elusive. Here, we used a broad-band two-dimensional electronic spectroscopy, which alleviates the spectral congestion by dispersing excitation and detection wavelengths. Interchromophoric couplings appeared as cross peaks in two-dimensional electronic spectra, and these spectral features were observed between the peridinin S2 states and chlorophyll-a Qx and Qy states. In addition, the inherently high time and frequency resolutions of two-dimensional electronic spectroscopy enabled accurate determination of the ultrafast energy-transfer dynamics. Kinetic analysis near the peridinin S1 excited-state absorption, which forms in 24 fs after optical excitation, reveals an ultrafast energy-transfer pathway from the peridinin S2 state to the chlorophyll-a Qx state, a hitherto unconfirmed pathway critical for fast interchromophoric transfer. We propose a model of ultrafast peridinin chlorophyll-a protein photophysics that includes (1) a conical intersection between peridinin S2 and S1 states to explain both the ultrafast peridinin S1 formation and the residual peridinin S2 population for energy transfer to chlorophyll-a, and (2) computationally and experimentally derived peridinin S2 site energies that support the observed ultrafast peridinin S2 to chlorophyll-a Qx energy transfer.
AB - Solar light harvesting begins with electronic energy transfer in structurally complex light-harvesting antennae such as the peridinin chlorophyll-a protein from dinoflagellate algae. Peridinin chlorophyll-a protein is composed of a unique combination of chlorophylls sensitized by carotenoids in a 4:1 ratio, and ultrafast spectroscopic methods have previously been utilized in elucidating their energy-transfer pathways and timescales. However, due to overlapping signals from various chromophores and competing pathways and timescales, a consistent model of intraprotein electronic energy transfer has been elusive. Here, we used a broad-band two-dimensional electronic spectroscopy, which alleviates the spectral congestion by dispersing excitation and detection wavelengths. Interchromophoric couplings appeared as cross peaks in two-dimensional electronic spectra, and these spectral features were observed between the peridinin S2 states and chlorophyll-a Qx and Qy states. In addition, the inherently high time and frequency resolutions of two-dimensional electronic spectroscopy enabled accurate determination of the ultrafast energy-transfer dynamics. Kinetic analysis near the peridinin S1 excited-state absorption, which forms in 24 fs after optical excitation, reveals an ultrafast energy-transfer pathway from the peridinin S2 state to the chlorophyll-a Qx state, a hitherto unconfirmed pathway critical for fast interchromophoric transfer. We propose a model of ultrafast peridinin chlorophyll-a protein photophysics that includes (1) a conical intersection between peridinin S2 and S1 states to explain both the ultrafast peridinin S1 formation and the residual peridinin S2 population for energy transfer to chlorophyll-a, and (2) computationally and experimentally derived peridinin S2 site energies that support the observed ultrafast peridinin S2 to chlorophyll-a Qx energy transfer.
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U2 - 10.1021/acs.jpcb.9b04324
DO - 10.1021/acs.jpcb.9b04324
M3 - Article
C2 - 31282681
AN - SCOPUS:85070837507
SN - 1520-6106
SP - 6410
EP - 6420
JO - Journal of Physical Chemistry B
JF - Journal of Physical Chemistry B
ER -