Article pubs.acs.org/JPCB
Excitation Energy Transfer in the Peridinin-Chlorophyll a‑Protein Complex Modeled Using Configuration Interaction William P. Bricker and Cynthia S. Lo* Department of Energy, Environmental and Chemical Engineering, Washington University, Saint Louis, Missouri 63130, United States ABSTRACT: We modeled excitation energy transfer (EET) in the peridinin-chlorophyll a-protein (PCP) complex of dinoflagellate Amphidinium carterae to determine which pathways contribute dominantly to the high efficiency of this process. We used complete active space configuration interaction (CAS-CI) to calculate electronic structure properties of the peridinin (PID) and chlorophyll a (CLA) pigments in PCP and the transition density cube (TDC) method to calculate Coulombic couplings between energy transfer donors and acceptors. Our calculations show that the S1 → Qy EET pathway from peridinin to chlorophyll a is the dominant energy transfer pathway in PCP, with two sets of interactionsbetween PID612 and CLA601 and between PID622 and CLA602contributing most strongly. EET lifetimes for these two interactions were calculated to be 2.66 and 2.90, with quantum efficiencies of 85.75 and 84.65%, respectively. The calculated Coulombic couplings for EET between two peridinin molecules in the strongly allowed S2 excited states are extremely large and suggest excitonic coupling between pairs of peridinin S2 states. This methodology is also broadly applicable to the study of EET in other photosynthetic complexes and/or organic photovoltaics, where both single and double excitations are present and donor and acceptor molecules are tightly packed.
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INTRODUCTION The study of solar energy utilization in photosynthetic organisms, including light harvesting and energy transfer, may give us clues as to how to better capture and store energy in bioinspired or artificial photosynthetic systems. Naturally, there are differences in how photosynthetic organisms behave compared to photovoltaic systems; the organisms’ main concern is to utilize sunlight to store energy in the form of chemical bonds, not necessarily to convert all available energy to electrical power output, given appropriate thermodynamic limitations.1,2 As such, photosynthetic organisms, such as algae, exhibit incredibly high (near 100%) quantum efficiencies in excitation energy transfer, and we seek to better understand the underlying origins of these processes. We choose as our model the peridinin-chlorophyll a-protein (PCP) complex, which is commonly found in dinoflagellates. The structure of PCP in dinoflagellate Amphidinium carterae has been successfully determined using X-ray crystallography,3 as shown in Figure 1.4−6 PCP is a protein trimer, with eight peridinin (PID) carotenoids and two chlorophyll a (CLA) pigments per protein monomer (Figure 2). Peridinin contains a polyene backbone, which is broken up by a lactone ring and an allene group (Figure 2). Thus, energy transfer between similar pigments (i.e., peridinin to peridinin) and dissimilar pigments (i.e., peridinin to chlorophyll a) may be investigated in this complex. The PCP complex in Amphidinium carterae has attracted attention from both experimentalists and theorists due to its small size, interesting excitation energy transfer (EET) properties due in part to the unique peridinin carotenoid, © 2014 American Chemical Society
Figure 1. PCP contains two pigmentsperidinin (PID) and chlorophyll a (CLA)and a lipid moleculedigalactosyl diacyl glycerol (DGD). Peridinin molecules are colored based on their respective geometries, where PID611 and PID621 are blue, PID612 and PID622 are orange, PID613 and PID623 are green, and PID614 and PID624 are yellow. Chlorophyll a molecules are red, DGDs are gray, and the protein backbone is white. This graphic contains all molecules contained in one monomer of the PCP trimer (chain M), and all atomic coordinates are obtained from the Protein Data Bank (PDB ID 1PPR).4 This graphic was generated using VMD.5
Received: February 17, 2014 Revised: July 8, 2014 Published: July 9, 2014 9141
dx.doi.org/10.1021/jp5017054 | J. Phys. Chem. B 2014, 118, 9141−9154
The Journal of Physical Chemistry B
Article
Figure 3. Excitation energy transfer pathways in PCP, with three PID to CLA pathways labeled: k1 (S1 → Qy), k2 (S2 → Qx), and k3 (S1 → Qx). Experimental internal conversion rates are included from S2 → S1, S1 → S0, and Qy → S0. Peridinin is initially excited via the strongly allowed S0 → S2 transition. Figure 2. Two pigment molecules in PCP: peridinin and chlorophyll a. Carbon atoms in the peridinin polyene chain are numbered from right to left, and the phytyl tail (R) of chlorophyll a is not included. Standard porphyrin x and y axes are labeled.
shown that the ICT state develops due to S1 and S2 mixing, which possibly facilitates energy transfer from peridinin to chlorophyll a.21 Several computational studies have incorporated various levels of EET theory into an analysis of the PCP complex, which has been facilitated by the availability of a crystal structure of PCP in A. carterae, as determined by X-ray crystallography to a resolution of 2.0 A.3 Förster resonance energy transfer (FRET) with the ideal dipole approximation (IDA) or a multipole expansion has been used to calculate the electronic interaction between transition dipole moments of donor and acceptor molecules.22 Damjanović et al. calculated significant S1 → Qy transfer but none using the S2 → Qx pathway and a possibility of excitonically coupled S2 states; however, they struggled to calculate accurate Coulombic couplings.7 By reconstituting PCP with non-native chlorophyll ́ et al. found that the S1/ICT state had a lifetime species, Polivka of 2.7 ps in the native complex, compared to 5.9 ps (chlorophyll b), 2.9 ps (chlorophyll a), 2.2 ps (acetyl chlorophyll a), 1.9 ps (chlorophyll d), and 0.45 ps (bacteriochlorophyll a) in the reconstituted PCP complexes, of which all of the lifetimes were reproduced accurately using the FRET model when normalized to the energy transfer rates in the native PCP complex.23 In pure polyene molecules, the S1 excited state has a vanishingly small transition dipole moment due to forbidden symmetry with the ground state, and even though the peridinin molecule breaks up the polyene chain with the lactone ring and the allene group, a small but non-negligible transition dipole moment is still expected.7 The magnitude of the S1 transition dipole moment of peridinin has been estimated to be 0.86−3.0 D, which is small compared to the transition dipole moment of the S2 state of peridinin, which is estimated to be 10.6−12.4 D.7,24 The study of EET in a light-harvesting complex necessitates appropriate theory that properly treats transitions between donor and acceptor molecules. In FRET, the transition dipole moments of a donor and acceptor molecule are coupled via a Coulombic interaction. This model is based on a weak electronic coupling between donor and acceptor molecules and carries several assumptions. First, the bath must equilibrate after donor excitation that is much faster than the rate of EET. Second, the bath coupling is greater than the donor-to-acceptor coupling. These conditions make the EET incoherent and irreversible.25 Due to recent evidence of quantum coherence in the Fenna−Mathews−Olsen (FMO) light-harvesting com-
and high quantum efficiency (85−95%) for EET between peridinin and chlorophyll a.7−9 Indeed, a recent study on PCP in the related dinoflagellate Symbiodinium also reported a very high peridinin to chlorophyll a energy transfer efficiency of 95%.10 Furthermore, the rate of energy transfer from peridinin to chlorophyll a in A. carterae PCP has been estimated to have a lifetime of 2.3−3.2 ps.9,11−13 The peridinin molecules surrounding the chlorophyll a molecules are excited from the S0 (1A−g ) ground state to the strongly allowed S2 (1B+u ) excited state, and the S0 → S1 (2A−g ) excitation is symmetry-forbidden, as is typical in similar polyenes. Once the S2 state of peridinin is excited, EET to chlorophyll a via the S2 → Qx pathway must compete with extremely rapid internal conversion to the S1 state in peridinin. EET via the S2 → Qx pathway has been previously estimated to have a transfer efficiency of only ∼25% in PCP due to an early (
