Refinement of the x-ray structure of the RC–LH1 core complex from Rhodopseudomonas palustris by single-molecule spectroscopy

Abstract

A unique combination of single-molecule spectroscopy with numerical simulations has allowed us to achieve a refined structural model for the bacteriochlorophyll a (BChl a) pigment arrangement in reaction center-light-harvesting 1 core complexes of Rhodopseudomonas palustris. Details in the optical spectra, such as spectral separation and mutual polarizations of spectral bands, are compared with results from numerical simulations for various models of the BChl a arrangement that were all well within the 4.8-Å limit of the accuracy of the available x-ray structure. The experimental data are consistent with a geometry where 15 BChl a dimers, each taken homologous to those from light-harvesting 2 complex from Rhodopseudomonas acidophila, are arranged in an overall elliptical structure featuring a gap on the long side of the ellipse.bacterial photosynthesis ͉ light harvesting ͉ supramolecular arrangement I n photosynthesis solar radiation is absorbed by the lightharvesting (LH) apparatus, and the excitation energy is then transferred efficiently to a reaction center (RC), where it is used to create a charge-separated state that ultimately drives all of the subsequent metabolic reactions. Most purple photosynthetic bacteria contain two types of antenna complexes, LH1 complex and LH2 complex (1, 2). The RC is closely associated with LH1, whereas LH2s are arranged around the perimeter of RC-LH1 in a 2D array, the structure of which depends on how the bacteria are grown (3-5). The progress made in high-resolution structural studies of the LH2s (6-9) has strongly stimulated research to understand the detailed mechanisms of the efficient energy transfer processes that take place in these antenna systems. The basic building block of LH2 is a protein heterodimer (␣␤), which accommodates three bacteriochlorophyll a (BChl a) pigments and one carotenoid molecule (8). Depending on the bacterial species LH2 consists either of eight or nine copies of these heterodimers, which are arranged in a ring-like structure. It has now been well established that the spatial arrangement of the pigments determines, to a large extent, the spectroscopic features of the complexes and that in these systems collective effects have to be considered to appropriately describe their electronically excited states (10-16). These effects lead to so-called Frenkel excitons, which arise from the interactions of the transition-dipole moments of the individual pigments and correspond to delocalized electronically excited states (17). Because the interaction strength between the individual pigments can be calculated on the basis of the available structural data, information about the pigment arrangement within the LH complexes becomes accessible via optical spectroscopy. From this perspective LH2 has served as a cornerstone for the development of a detailed understanding of structure-function relationships in such antenna systems (18).In contrast to LH2, where highly resolved x-ray structures are available, the discussion in the literature about the structural...

Low-temperature single-molecule spectroscopy on photosynthetic pigment–protein complexes from purple bacteria

“…The other traces are offset for clarity. Adapted from Richter et al (2007c) determined to a large extent by the geometrical arrangement of the BChl a chromophores with respect to each other. The two ring systems in LH2 feature strikingly different spectra which can be attributed to the differences in the intermolecular coupling strengths (V/DE) of the two assemblies.…”

Essential Genome of the Metabolically Versatile Alphaproteobacterium Rhodopseudomonas palustris

“…R. palustris also grows aerobically as a heterotroph, and some strains grow anaerobically in the dark by nitrate respiration. It has served as a model organism for studies of anaerobic aromatic compound degradation, hydrogen gas production, nitrogen fixation, and photosynthesis (13)(14)(15)(16)(17)(18)(19)(20)(21). R. palustris grows by budding in which a motile daughter swarmer cell is pinched off from the pole of a sessile mother cell once chromosome replication is complete (22).…”

Chlorophylls, Symmetry, Chirality, and Photosynthesis

“…Specifically, LHC2 consists of two BChl rings denoted B800 and B850 containing 9 monomeric BChls and 9 pairs of BChl pseudo dimers, respectively, with Mg-Mg distances of ~21 and 9 Å, also respectively [229][230][231]. The RC-LHC1 complex contains the B875 ring of 30 BChls composed of 15 BChl a dimers with similar Mg-Mg separations to B850 [232,233]. The energetic hierarchy of the bacterial light-harvesting complexes suggests excitation energy transfer occurs in a stepwise sequence: (LHC3 →) LHC2 → LHC1 → RC [234,235].…”