J. Phys. Chem. B 2003, 107, 5995-6002
5995
β-Carotene to Chlorophyll Singlet Energy Transfer in the Photosystem I Core of Synechococcus elongatus Proceeds via the β-Carotene S2 and S1 States Frank L. de Weerd,* John T. M. Kennis, Jan P. Dekker, and Rienk van Grondelle Department of Biophysics and Physics of Complex Systems, DiVision of Physics and Astronomy, Faculty of Sciences, Vrije UniVersiteit, De Boelelaan 1081, 1081 HV Amsterdam, The Netherlands ReceiVed: December 18, 2002; In Final Form: April 4, 2003
In this work, we describe the ultrafast excitation transfer dynamics of β-carotene in trimeric photosystem I preparations from Synechococcus elongatus. β-Carotene was excited with a femtosecond laser, and the changes in absorption were followed in the spectral region 490-740 nm. The lifetime of the β-carotene S2 (1Bu+) states is ∼60 fs, significantly shorter than that in nonpolar solution (150 fs), demonstrating efficient energy transfer to the chlorophylls from these states. About 70% of the remaining population of β-carotene S1 (2Ag-) states is not in contact with the chlorophylls (lifetime 10 ps), whereas ∼30% transfers its energy efficiently to chlorophylls (lifetime 3 ps). We ascribe the S1 transfer to a fraction of the β-carotenes (possibly the ones adopting a cis configuration) that exhibit favorable π-π stacking with nearby chlorophylls. We estimate that ∼70% of initial β-carotene S2 excitations is transferred to the chlorophylls, namely, ∼60% from S2 on a 60 fs time scale and ∼10% from S1 on a 3 ps time scale, making the S2 state to a major extent responsible for the larger yield of β-carotene to chlorophyll singlet energy transfer in comparison with the photosystem II core proteins.
Introduction Carotenoids (Cars) play a major role in photosynthesis: on one hand, they quench singlet oxygen and chlorophyll (Chl) triplets (that can lead to the formation of singlet oxygen), while on the other hand, they harvest sunlight in a spectral region where Chls do not absorb. In the photosynthetic apparatus, β-carotene is the only carotenoid (Car) species bound to the core complexes (reaction center (RC) and core antenna) of photosystem I (PSI) and photosystem II (PSII). In both photosystems, excitation energy is transferred via the core antennas to the RC, where an ultrafast charge separation (∼picosecond) is initiated.1 In this study, we address the energy transfer from β-carotene to chlorophyll (Chl) in the PSI core complex of the cyanobacterium Synechococcus elongatus. In the crystal structure of the PSI core antenna complex of S. elongatus at 2.5 Å resolution, 96 Chl molecules and 22 Cars have been identified per monomeric unit.2 Six Chl molecules were assigned to the centrally positioned RC, whereas the remaining Chls are packed in a bowllike structure closely surrounding the RC, plus two peripheral domains, where the Chls are organized in two discrete layers near the stromal and luminal sides of the membrane. These peripheral domains possess a sequence homology with the PSII core antennas CP43 and CP47.3 The PSI antenna also contains the so-called “red” pigments, Chls with a longer transition wavelength than that of the primary electron donor P700 (for review, see ref 4). For S. elongatus, the subject of this study, red Chl pools denoted C708 and C719 (room temperature absorption maxima at 702 and 708 nm, respectively) were identified.5,6 Another pool was proposed to peak at 715 nm at 4 K.7 The C708 form may originate from Chl dimers in * To whom correspondence should be addressed. Tel: (+31) 20 4447934. Fax: (+31) 20 4447999. E-mail:
[email protected].
the inner ring and the C719 form was proposed to arise from a tightly coupled trimer in the periphery.2,6,8-10 Of the 22 Cars in the crystal structure, 21 were modeled as complete β-carotenes. These β-carotenes showed several isomerization states: for 16 β-carotenes, an all-trans configuration was found, whereas five β-carotenes adopted a variety of configurations containing one or two cis bonds. All 22 Cars are in van der Waals contact (90%). In other words, the probability that in a particular monomer Chl is not excited is small (
