Atomic-level structural and functional model of a bacterial photosynthetic membrane vesicle.

The photosynthetic unit (PSU) of purple photosynthetic bacteria consists of a network of bacteriochlorophyll-protein complexes that absorb solar energy for eventual conversion to ATP. Because of its remarkable simplicity, the PSU can serve as a prototype for studies of cellular organelles. In the purple bacterium Rhodobacter sphaeroides the PSU forms spherical invaginations of the inner membrane, approximately 70 nm in diameter, composed mostly of light-harvesting complexes, LH1 and LH2, and reaction centers (RCs). Atomic force microscopy studies of the intracytoplasmic membrane have revealed the overall spatial organization of the PSU. In the present study these atomic force microscopy data were used to construct three-dimensional models of an entire membrane vesicle at the atomic level by using the known structure of the LH2 complex and a structural model of the dimeric RC-LH1 complex. Two models depict vesicles consisting of 9 or 18 dimeric RC-LH1 complexes and 144 or 101 LH2 complexes, representing a total of 3,879 or 4,464 bacteriochlorophylls, respectively. The in silico reconstructions permit a detailed description of light absorption and electronic excitation migration, including computation of a 50-ps excitation lifetime and a 95% quantum efficiency for one of the model membranes, and demonstration of excitation sharing within the closely packed RC-LH1 dimer arrays.

Comparison of the light-harvesting networks of plant and cyanobacterial photosystem I.

With the availability of structural models for photosystem I (PSI) in cyanobacteria and plants it is possible to compare the excitation transfer networks in this ubiquitous photosystem from two domains of life separated by over one billion years of divergent evolution, thus providing an insight into the physical constraints that shape the networks' evolution. Structure-based modeling methods are used to examine the excitation transfer kinetics of the plant PSI-LHCI supercomplex. For this purpose an effective Hamiltonian is constructed that combines an existing cyanobacterial model for structurally conserved chlorophylls with spectral information for chlorophylls in the Lhca subunits. The plant PSI excitation migration network thus characterized is compared to its cyanobacterial counterpart investigated earlier. In agreement with observations, an average excitation transfer lifetime of approximately 49 ps is computed for the plant PSI-LHCI supercomplex with a corresponding quantum yield of 95%. The sensitivity of the results to chlorophyll site energy assignments is discussed. Lhca subunits are efficiently coupled to the PSI core via gap chlorophylls. In contrast to the chlorophylls in the vicinity of the reaction center, previously shown to optimize the quantum yield of the excitation transfer process, the orientational ordering of peripheral chlorophylls does not show such optimality. The finding suggests that after close packing of chlorophylls was achieved, constraints other than efficiency of the overall excitation transfer process precluded further evolution of pigment ordering.

Excitation migration in trimeric cyanobacterial photosystem I.

A structure-based description of excitation migration in multireaction center light harvesting systems is introduced. The description is an extension of the sojourn expansion, which decomposes excitation migration in terms of repeated detrapping and recapture events. The approach is applied to light harvesting in the trimeric form of cyanobacterial photosystem I (PSI). Excitation is found to be shared between PSI monomers and the chlorophylls providing the strongest respective links are identified. Excitation sharing is investigated by computing cross-monomer excitation trapping probabilities. It is seen that on the average there is a nearly 40% chance of excitation cross transfer and trapping, indicating efficient coupling between monomers. The robustness and optimality of the chlorophyll network of trimeric PSI is examined.

General random matrix approach to account for the effect of static disorder on the spectral properties of light harvesting systems.

We develop a random matrix model approach to study static disorder in pigment-protein complexes in photosynthetic organisms. As a case study, we examine the ring of B850 bacteriochlorophylls in the peripheral light-harvesting complex of Rhodospirillum molischianum, formulated in terms of an effective Hamiltonian describing the collective electronic excitations of the system. We numerically examine and compare various models of disorder and observe that both the density of states and the absorption spectrum of the model show remarkable spectral universality. For the case of unitary disorder, we develop a method to analytically evaluate the density of states of the ensemble using the supersymmetric formulation of random matrix theory. Succinct formulas that can be readily applied in future studies are provided in an appendix.