ARTICLE pubs.acs.org/JPCA
Dynamics of Exciton Relaxation in LH2 Antenna Probed by Multipulse Nonlinear Spectroscopy Vladimir I. Novoderezhkin,† Thomas A. Cohen Stuart,‡ and Rienk van Grondelle*,‡ † ‡
A. N. Belozersky Institute of Physico-Chemical Biology, Moscow State University, Leninskie Gory, 119992 Moscow, Russia Department of Biophysics, Faculty of Sciences, Vrije Universiteit, De Boelelaan 1081, 1081 HV Amsterdam, The Netherlands
bS Supporting Information ABSTRACT: We explain the relaxation dynamics in the LH2-B850 antenna as revealed by multipulse pump-dump-probe spectroscopy (Th. A. Cohen Stuart, M. Vengris, V. I. Novoderezhkin, R. J. Cogdell, C. N. Hunter, R. van Grondelle, submitted). The theory of pumpdump-probe response is evaluated using the doorway-window approach in combination with the modified Redfield theory. We demonstrate that a simultaneous fit of linear spectra, pump-probe, and pump-dump-probe kinetics can be obtained at a quantitative level using the disordered exciton model, which is essentially the same as used to model the spectral fluctuations in single LH2 complexes (Novoderezhkin, V.; Rutkauskas, D.; van Grondelle, R. Biophys. J. 2006, 90, 2890). The present studies suggest that the observed relaxation rates are strongly dependent on the realization of the disorder. A big spread of the rates (exceeding 3 orders of magnitude) is correlated with the disorder-induced changes in delocalization length and overlap of the exciton wave functions. We conclude that the bulk kinetics reflect a superposition of many pathways corresponding to different physical limits of energy transfer, varying from sub-20 fs relaxation between delocalized and highly spatially overlapping exciton states to >20 ps jumps between states localized at the opposite sides of the ring.
1. INTRODUCTION In photosynthetic purple bacteria solar photons are absorbed by light-harvesting antenna complexes LH1 and LH2 consisting of ordered arrays of bacteriochlorophylls (BChl) noncovalently bound to proteins.1 The peripheral LH2 complex consists of a highly symmetric and tightly packed ring of 18 (or 16) BChls together with a second ring of 9 (or 8) weakly interacting BChls.2-4 These rings determine the absorption bands at 850 and 800 nm, respectively (denoted as B850 and B800). The LH1 core complex forms a quasi-circular structure, either closed with 32 BChls5,6 or open with 30 BChls7 surrounding the reaction center. Due to strong pigment-pigment interactions within the LH1 and LH2-B850 rings these antennas are characterized by a complicated manifold of collective electronic excitations (excitons) with a high degree of delocalization. Coupling of excitations to phonons and conformational motion of the pigment-protein matrix generally produces more localized states due to static disorder and polaron effects. Experimental studies (using nonlinear optical spectroscopy, single molecule techniques, etc.) in combination with quantitative modeling resulted in a detailed and consistent picture of the excitation dynamics in LH1/LH2 complexes (for a review, see refs 8 and 9). Pump-Probe Studies of Exciton Equilibration. The most intriguing phenomenon is the extremely fast (10-100 fs) relaxation within the ring-like LH1/LH2 antennas. The direct observation r 2011 American Chemical Society
of fast equilibration within the LH1 and LH2-B850 antennae (including relaxation of the exciton states and migration of the quasi-steady-state exciton wavepacket) is possible by transient absorption (TA) studies via the picosecond/femtosecond pumpprobe technique. Such measurements have revealed the initial ultrafast (sub-100 fs) relaxation in LH1/LH2 complexes followed by slower (picosecond) dynamics.10-22 The relaxation in these complexes gives rise to specific TA dynamics that is typical for assemblies of excitonically coupled antenna pigments but is absent in isolated dimeric subunits and monomers. Thus, Visser et al.11 found a pronounced TA dynamics for LH1 of Rhodospirillium rubrum with an 8-12 nm red shift reflecting fast exciton equilibration, whereas no red-shift dynamics was found in the lowest-state absorption band of the B820 dimeric subunit as well as for monomeric BChl. A short-pulse (35-50 fs) pump-probe study of LH1 and LH2 of Rhodobacter sphaeroides14-17 showed relaxation components in the 10-100 fs range (short-lived
