Is there an excitonic interaction or antenna system in bacteriorhodopsin?

Abstract

The presence of a biphasic circular dichroism (CD) observed in the visible absorption spectrum of retinal in bacteriorhodopsin (bR) has been believed for many years to be due to excitonic-type interaction within the trimeric structure of the retinal in the protein membrane. In the present work, we present data and discuss previous observations that strongly suggest the absence of such an exdtonic interaction. The magnetic CD spectrum of the trimer is found to be similar to that of the monomer and shows no sign of absorption to the doubly degenerate state predicted to be present from the exciton theory. This, together with the previous observations on the CD spectra of the photocycle intermediates of bR as weli as the linear polarization studies of the fluorescence and the daughter absorption, sheds doubt on the presence of exciton interaction and thus suggests the presence ofneither an antenna system nor a viable special reaction center in bR. As a result, the PSB is deprotonated during the L550 -412step, which initiates a proton pumping process that leads to an increase in the proton concentration on the outside surface of the membrane (6). The created proton gradient across the membrane is then used to transform ADP into ATP in the final step of the photosynthesis of bR (refs. 1 and 2; for a review, see ref. 7). In the above transformations, light energy is converted into ATP (chemical energy) by means ofa conversion into electric energy on different time scales. The first step of the conversion occurs when rapid isomerization of the retinal occurs (8)(9)(10)(11). This leads to charge separation of the protonated Schiff base from its counter ion(s). A change in the protein conformation on the microsecond time scale then occurs in response to the electric force resulting from the charge separation. The protein conformation changes are shown (12) to control the rate of the deprotonation process of the PSB. The latter process leads to further charge separation resulting from pumping protons from inside the membrane to its exterior (6). This leads to the proton gradients required for the conversion of the electric energy to the chemical energy through the conversion of ADP into ATP (2, 7).The question immediately arises as to what happens between the absorption process and retinal isomerization. Does the molecule that absorbs the photon undergo isomerization or is there an antenna system, like the one known to be present in chlorophyll, that transfers the excitation energy from the absorbing molecule to a "special reaction center?" For this to take place, an exciton coupling needs to be present that would allow the transfer of the excitation energy to take place in a time shorter than isomerization times. Two important experimental observations on bR strongly suggested the presence of such excitonic coupling. (i) The purple membrane protein molecules are found in rigid clusters of three in the membrane with a threefold symmetry axis perpendicular to the plane of the membrane at the center of each cluster (...

Excitation Energy-Transfer and the Relative Orientation of Retinal and Carotenoid in Xanthorhodopsin

“…The observed constant anisotropy in Fig. 6 C, at its theoretical high limit, is in agreement with the suggested lack of energy transfer between the retinal chromophores of monomers within the bacteriorhodopsin trimer (37,39,49). In xanthorhodopsin, at wavelengths where absorption of the carotenoid dominates, the anisotropy decreases to ;0.1 (minima at 486 and 520 nm).…”

Xanthorhodopsin: Proton pump with a carotenoid antenna

“…No energy transfer occurs between the common carotenoid of archaea, bacterioruberin, and BR [19,20] or even archaerhodopsin which interacts with this carotenoid [2,3,21]. The much-disputed explanation for the bilobe circular dichroism (CD) spectrum of the purple membrane by an exciton interaction within the BR trimer [22], which would result in energy transfer between the three retinal molecules, disagreed with a number of experimental results [23]. However, there are several cases when energy transfer from accessory pigments to retinal is involved in photoreception.…”

The reaction cycle of bacteriorhodopsin: an analysis using visible absorption, photocurrent and infrared techniques

“…The assumption proposing different population in the bR resting state was already discussed using independent observations (E1-Sayed et al 1989;Diller and Stockburger 1988). Specific azc and ~3C incorporation into Asp212 should provide a means of deciding between the possibilities and for the unequivocal assignment of the Asp212 carbonyl vibration.…”