On the Nature of Energy Transfer at Low Temperatures in the BChl a Pigment-Protein Complex of Green Sulfur Bacteria R. J. W. Louwe and T. J. Aartsma* Department of Biophysics, Huygens Laboratory, Leiden UniVersity, P. O. Box 9504, 2300 RA Leiden, The Netherlands ReceiVed: October 29, 1996; In Final Form: February 21, 1997 X The technique of accumulated photon echoes was used to study optical dephasing of the lowest Q Y transitions of the bacteriochlorophyll a complex of the green sulfur bacteria Prosthecochloris aestuarii. Variations in the photon echo decay as a function of wavelength are interpreted in terms of (phonon-assisted) downward relaxation within the Q Y manifold as a mechanism of energy transfer at the lowest temperatures. A temperature dependence study revealed contributions to the total dephasing both from transitions within so-called two level systems (TLS) of the host as well as activation of transitions to higher electronic levels within the Q Y manifold at temperatures above 5 K. Conclusions are drawn about the nature of energy transfer at low temperatures. Introduction Energy transfer has already been a subject of interest for many years and often a distinction is made between the weak coupling case and the strong coupling case, usually referring to the strength of the (dipolar) interaction between the pigments relative to the strength of the electron-phonon coupling. A more general description of the energy transfer process is offered by the generalized master equation (GME) or the (equivalent) stochastic Liouville equation (SLE) 1 approach. It has been shown that these theories represent a unifying approach, comprising both limiting cases. 2-4 For energy transfer in photosynthetic antenna systems, where the intermediate coupling case might be applicable, however, the situation is complicated due to several factors. Although some antenna systems possess a high degree of symmetry, 5 reflected in specific properties of the electronic hamiltonian of the system and of the electronic transitions, this high degree of symmetry is not a general feature of antenna systems (see, e.g., refs 6-8). In particular, in the case of low symmetry, variations in site energy are to be expected which are not known a priori and will be comparable to or even larger than the strength of the interaction between the individual pigments. 9 Furthermore, the various spectra of the electronic transitions of these systems are characterized by a large inhomogeneous broadening. Con- cerning the broadening mechanisms, usually a distinction is made between static and dynamic processes, reflecting in- homogeneous and homogeneous broadening of the electronic transitions, respectively. Both can be subdivided further into local processes, modulating the site energies of the individual pigments, and nonlocal processes, modulating the strength of the interaction between the pigments. Recent dephasing and spectral diffusion studies on various pigments in glasses, polymers, and proteins show that relaxation processes of these amorphous solids occur on all time scales. 10-13 In antenna systems these fluctuations of the site energies will be observable as fluctuations of the eigenenergies of the system on all time scales and therefore a general distinction between dynamic and static processes should not be made without considering the time scale of the experiment. Due to all these complicating factors, a full description of energy transfer in photosynthetic antenna systems using the SLE or GME is a formidable task. The (in-)coherent nature of the energy transfer mechanism in photosynthetic antenna systems is still a subject of discussion, often based on experiments which do not measure the coherence of the excited states directly. All these considerations prompted us to measure the coher- ence directly using the accumulated photon echo technique to gain more insight in the coherence of energy transfer. In this article we present data on the BChl a pigment-protein complex from green sulfur bacteria, often referred to as the Fenna- Matthews-Olson (FMO) complex. The structure of this pigment-protein complex has been elucidated by X-ray crystal- lography with near atomic resolution 7,8 and it consists of three subunits in C 3 symmetry, whereby each subunit contains seven BChl a’s. The nearest-neighbor distance between the BChls within each subunit is on the average about 12 Å and that between BChls belonging to different subunits 24 Å, yielding interactions between the BChls with a maximum of ap- proximately 200 cm -1 and 20 cm -1 , respectively. The FMO-complex has been fairly well characterized spectroscopically 14-17 and shows a well-resolved Q Y absorption region at cryogenic temperatures in optical steady state spectra. The absorption spectrum and circular dichroism spectrum can be simulated reasonably well by using exciton theory. 18,19 So far, it has been impossible, however, to obtain a set of parameters for this model that would simulate the linear dichroic (LD), the triplet minus singlet (T - S), and the linear dichroic triplet minus singlet (LD-(T - S)) spectra simultaneously to the same degree of accuracy. 20 Time-resolved spectroscopy has mostly been applied at room temperature 21-25 on different time scales and indicates that thermal equilibration and probably localization of an excitation to the lowest energy state of the complex occurs in less than 1 ps, although the time constants found in the different experi- ments vary somewhat. At lower temperatures such studies are rather scarse. At 77 K, Zhou et al. 25 showed that the fluorescence decay was dominated by a component with a time constant of 2 ns. Very recently, Savikhin and Struve 26 presented results of transient absorption experiments on the FMO-complex of Chlorobium tepidum at 19 K, showing that thermal equilibra- tion in the Q Y manifold slows down by almost 2 orders of * Author to whom correspondence should be addressed. X Abstract published in AdVance ACS Abstracts, August 1, 1997. 7221 J. Phys. Chem. B 1997, 101, 7221-7226 S1089-5647(96)03370-6 CCC: $14.00 © 1997 American Chemical Society