Short-Range Exciton Couplings in LH2 Photosynthetic Antenna Proteins Studied by High Hydrostatic Pressure Absorption Spectroscopy Ko ˜ u Timpmann, ² Aleksandr Ellervee, ² To ˜ nu Pullerits, ‡ Rein Ruus, ² Villy Sundstro 1 m, ‡ and Arvi Freiberg* ,² Institute of Physics, UniVersity of Tartu, Riia 142, 51014 Tartu, Estonia, and Department of Chemical Physics, Lund UniVersity, P.O. Box 124, S-22100 Lund, Sweden ReceiVed: September 27, 2000; In Final Form: February 14, 2001 The effects of high hydrostatic pressure (up to 8 kbar) on bacteriochlorophyll a Q y electronic absorption bands of LH2 photosynthetic antenna complexes have been studied at ambient temperature. A variety of samples were studied, including intact membranes and isolated complexes from wild type and mutant photosynthetic bacteria Rhodobacter sphaeroides, Rhodopseudomonas acidophila, and Rhodospirillum molischianum. The spectra of the complexes universally red shift and broaden under elastic compression, while the variations of the integrated intensity remain within the experimental uncertainty. A qualitatively different slope and variation of the slope of the pressure-induced shift is observed for the B800 and B850 absorption bands of LH2 complexes belonging to quasi-monomer and aggregated pigments, respectively. For the complexes from Rhodobacter sphaeroides, e.g., the corresponding slopes are -28 ( 2 and -65 ( 2 cm -1 /kbar. The shift rate of the B800 band declines with pressure, while the opposite is observed for the B850 band. The shifts show little if any correlation with hydrogen bonds. Using simple phenomenological arguments and numerical simulations of molecular exciton spectra, it is shown that the shift of the B800 band is governed by pigment-protein interactions, while in addition to that, interpigment couplings (including long-range dipolar and short-range orbital overlap interactions) are instrumental for the B850 band shift. The compressibility of the B800 bacteriochlorophyll binding sites deduced from the B800 band shift at ambient pressure is ∼0.02 kbar -1 , and it decreases nonlinearly with pressure. Inter-pigment couplings are responsible for approximately one-third of both the total ambient-pressure solvent shift of the B850 absorption band and its pressure-induced growth. A slight increase with pressure of the B850 band shift due to orbital overlap couplings is predicted. Introduction The optical properties of molecular systems depend on intermolecular interactions sensitive to distances and relative orientations of the coupled molecules. The main objective of this work is to study the character of the couplings between the bacteriochlorophyll a (Bchl) chromophores in peripheral (LH2) antenna protein complexes of purple photosynthetic bacteria using hydrostatic compression of the sample. The lowest, Q y , molecular electronic transition-related absorp- tion band in the LH2 antenna complex has been shown to have a substantial exciton character. 1-6 In the absence of a direct orbital overlap, the resonant interaction between the chro- mophores causing the excitation transfer is mediated by a Coulomb interaction between the electronic transition densities of the molecules. In the multipolar expansion of the interaction potential usually only the dipole-dipole term is retained, giving a familiar R -3 distance dependence of the interaction energy. This approximation is valid at distances large compared to the molecular size, which is evidently not the case in the LH2 protein complexes where the closest approach between the Bchl molecules (having a core diameter ∼0.9 nm) is ∼0.35 nm 7,8 (see Figure 1). Under these circumstances, not only may the dipole-dipole approximation fail but also the electron density distributions of the adjacent Bchl molecules may overlap, 9-11 causing substantial deviations from the standard exciton model. Charge-transfer configurations have been found to play a central role in promoting orbital overlap dependent interac- tions. The expected distance dependence of those interactions is exp(- γR), where γ is the decay constant that describes the attenuation of the coupling with distance, R. 9,11 The dipolar approximation as a well-established theoretical approach has been routinely applied to interpret exciton spectra in molecular crystals of aromatic series, such as anthracene and tetracene. 1,2 And yet, the pressure experiments on the same series of crystals have shown that the factor group or Davydov splitting increases much stronger than expected based on not only dipolar but also multipolar terms of expansion of resonant interac- tions. 12-15 This has been taken as an indication of a short-range character of the intermolecular couplings. Here, we shall take a similar approach to test the electronic coupling mechanisms in the LH2 antenna protein complexes by studying their spectra under compression. Precise tuning of the absorption properties of antenna protein complexes seems to be involved both in the funneling of exciton energy toward the reaction center (RC) protein complex 16-19 and in the adaptation of some of these photosynthetic organisms to varying environmental conditions. 20 Two near-infrared bands at about 800 and 850 nm characterize the absorption spectra of * Corresponding author. Tel.: +3727383024. Fax: +3727383033. E-mail: freiberg@fi.tartu.ee. ² University of Tartu. ‡ Lund University. 8436 J. Phys. Chem. B 2001, 105, 8436-8444 10.1021/jp003496f CCC: $20.00 © 2001 American Chemical Society Published on Web 08/10/2001