Structure, function, spectroscopy and structural dynamics of lamellar aggregates of chlorophyll a/b light harvesting complexes. A model of highly organized molecular macroassemblies of biological origin

Molecular macroaggregates are found in many biological systems, e.g. DNA condensations, chromosomes, viruses, stacked membranes etc. These highly organized materials contain a very large number of chromophores, and usually form well defined structures with dimensions commensurate with the wavelength of the visible light. They exhibit unusual spectroscopic features which cannot be interpreted in terms of theories for small aggregates; in addition, the experimental approach is also often difficult but polarized spectroscopic methods carry important information (Tinoco et al., 1984, Ann. Rev. Phys. Chem. 35: 329; 1987, Ann. Rev Biophys. Biophys Chem. 16: 319). A theory has been elaborated to explain the anomalous circular dichroism (CD) in the so-called psi-type aggregates, macroaggregates with high density of chromophores with long-range chiral order (Keller and Bustamante, 1986, J. Chem Phys. 84: 2972) (psi, polymer or salt induced). Deeper understanding of these highly organized molecular macrostructures, however, require systematic studies on model systems.

Photosynthetic complexes and particularly the chlorophyll a/b light harvesting antenna complex of photosystem II (LHCII) constitute probably the most suitable model systems: (i) lamellar macroaggregates with long range order can readily be 'constructed' from small complexes of 25-27 kDa; (ii) the structure of LHCII is known at nearly atomic resolution (Kühlbrandt et al. 1994, Nature 367: 614); (iii) structural and light spectroscopic studies can be combined (e.g. Gülen et al., 1997, J. Phys. Chem. B 101: 7256); (iv) reactions can be triggered by light, and thus serve as ideal objects for studying (ultra)fast processes (e.g. Peterman et al., 1997, Chem. Phys. Lett. 264: 279); (v) the presence of this type macrostructures in thylakoids is of interest concerning their dynamics and function in energy utilization and regulation (Garab, 1996, NATO ASI 287, ed. Jennings et al., p. 125).

Earlier, we have shown that PSII particles in granal thylakoid membranes form chirally organized macroaggregates with dimensions commensurate with the wavelength of the visible light (Garab et al., 1988, Biochemistry 27: 2430); their formation is largely facilitated by LHCII, which also readily form lamellar aggregates with long range chiral order. The macrodomains in thylakoid membranes have been shown to be capable of undergoing light-induced, reversible structural reorganizations (Garab et al., 1988, Biochemistry 27: 2430).

A brief overview will be given on: (i) structural role of macrodomains, which explains the lateral segregation (sorting) of the two photosystems between the stroma and granum regions (Garab et al., 1991 Photochem Photobiol 54: 273); (ii) long distance energy migration in LHCII lamellae, which has been shown by singlet-singlet exciton annihilation experiments (Barzda et al., 1996 Biochim. Biophys. Acta 1273: 231); (iii) aggregation-dependent fluorescence quenching of Chl a in LHCII, which is reminiscent to the non-photochemical quenching in thylakoids and which appears to be governed mainly via interaction of Chls and carotenoids (Razi Naqvi et al., 1997, Spectrochim Acta 53: 2659); (iv) structural dynamics, light-induced reversible structural changes have been identified in lamellar aggregates of LHCII, accompanied by changes in the photophysical pathways (fluorescence vs dissipation) (Barzda et al., 1996, Biochemistry 35: 8981); the macroorganization and the structural flexibility of LHCII depend largely on the (added or associated) lipid content of the preparations (Simidjiev et al., 1997, Analyt. Biochem. 255: 167; 1998, Biochemistry 37: 4169). In thylakoids, the changes have been shown to be largely independent of the photochemical activity of the membranes and amplified in excess light (Istokovics et al., 1997, Photosynth. Res. 54: 45; Gussakovsky et al., 1997, Photosynth. Res, 51: 119). These data suggest that a hitherto unknown photophysical mechanism - most likely via thermal fluctuations in the domains - participates in the regulation of energy utilization/dissipation in low/high light in thylakoids membranes.