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Using the mass-measuring capability of scanning transmission electron microscopy, we demonstrate that membrane crystals of the main light-harvesting complex of plants possess the ability to undergo light-induced dark-reversible disassociations, independently of the photochemical apparatus. This is the first direct visualization of light-driven reversible reorganizations in an isolated photosynthetic antenna. These reorganizations, identified earlier by circular dichroism (CD), can be accounted for by a biological thermo-optic transition: structural changes are induced by fast heat transients and thermal instabilities near the dissipation, and self-association of the complexes in the lipid matrix. A comparable process in native membranes is indicated by earlier findings of essentially identical kinetics, and intensity and temperature dependences of the ΔCD in granal thylakoids. [ABSTRACT FROM PUBLISHER]

We investigated the temperature dependence and inhibitor sensitivity of the light-induced reversible changes in the circular dichroism (ΔCD) of chloroplast thylakoid membranes. Earlier, these changes, which originate from structural changes affecting the chiral macroorganization of the chromophores, were thought to be driven by photochemically generated proton and/or ion gradients in the thylakoids [Garab et al. (1988) Biochemistry 27: 2430]. However, more recently, these changes have been shown to be largely independent of the photochemical activity of thylakoids, and ΔCD has been observed in lamellar aggregates of the light harvesting chlorophyll a/b complex (LHC II) of Photosystem II [Barzda et al. (1996) Biochemistry 35: 8981]. Here, we show that in thylakoids (i) ΔCD is gradually and substantially decelerated upon gradually decreasing the temperature from 33 °C to 2 °C, and abruptly disappears above 35–37 °C; (ii) ΔCD is inhibited with nigericin with I50≈ 1 μM, which is about 10 times higher than the I50for the transmembrane ΔpH; (iii) ΔCD can be inhibited with dicyclohexylcarbodiimide that blocks proton binding at the lumenal side of LHC II; (iv) quinone antagonists, such as antimycin-A and myxothiazol, inhibit ΔCD without noticeably affecting the electron and proton transport, and the chiral macroorganization of the chromophores in the dark. We conclude that ΔCD is conditioned but not driven by the photochemical activity of the membranes, and the structural changes are given rise by a physical mechanism previously unrecognized in thylakoids, thermooptic effect described for liquid crystals. We discuss the possible link between the deactivation(s) of the excess excitation energy and ΔCD, the light-induced changes in the chiral macroorganization of the chromophores of the photophysical apparatus in thylakoids. [ABSTRACT FROM AUTHOR]