The dynamics of pigment-pigment and pigment-protein interactions in light-harvesting complexes is studied with a novel approach that combines molecular dynamics simulations with quantum chemistry calculations and a polaron model analysis. The molecular dynamics simulation of lightharvesting complexes was performed on an 87,055 atom system comprised of an LH-II complex of Rhodospirillum molischianum embedded in a lipid bilayer and surrounded with appropriate water layers. The simulation provided information about the extent and timescales of geometrical deformations of pigment and protein residues at physiological temperatures, revealing also a pathway of a water molecule into the B800 binding site, as well as increased dimerization within the B850 BChl ring, as compared to the dimerization found for the crystal structure. For each of the 16 B850 BChls we performed 400 ab initio quantum chemistry calculations on geometries that emerged from the molecular dynamical simulations, determining the fluctuations of pigment excitation energies as a function of time. From the results of these calculations we construct a time-dependent Hamiltonian of the B850 exciton system from which we determine within linear response theory the absorption spectrum. Finally, a polaron model is introduced to describe both the excitonic and coupled phonon degrees of freedom by quantum mechanics. The exciton-phonon coupling that enters into the polaron model, and the corresponding phonon spectral function are derived from the molecular dynamics and quantum chemistry simulations. The model predicts that excitons in the B850 bacteriochlorophyll ring are delocalized over five pigments at room temperature. Also, the polaron model permits the calculation of the absorption spectrum of the B850 excitons from the sole knowledge of the autocorrelation function of the excitation energies of individual BChls, which is readily available from the combined molecular dynamics and quantum chemistry simulations. The obtained result is found to be in good agreement with the experimentally measured absorption spectrum. PACS number(s): 87.15. Aa, 87.15.Mi, 87.16.Ac

1. Introduction 22. Structure of the bacterial PSU 52.1 Organization of the bacterial PSU 52.2 The crystal structure of the RC 92.3 The crystal structures of LH-II 112.4 Bacteriochlorophyll pairs in LH-II and the RC 132.5 Models of LH-I and the LH-I-RC complex 152.6 Model for the PSU 173. Excitation transfer in the PSU 183.1 Electronic excitations of BChls 22 3.1.1 Individual BChls 22 3.1.2 Rings of BChls 22 3.1.2.1 Exciton states 22 3.1.3 Effective Hamiltonian 24 3.1.4 Optical properties 25 3.1.5 The effect of disorder 263.2 Theory of excitation transfer 29 3.2.1 General theory 29 3.2.2 Mechanisms of excitation transfer 32 3.2.3 Approximation for long-range transfer 34 3.2.4 Transfer to exciton states 353.3 Rates for transfer processes in the PSU 37 3.3.1 Car→BChl transfer 37 3.3.1.1 Mechanism of Car→BChl transfer 39 3.3.1.2 Pathways of Car→BChl transfer 40 3.3.2 Efficiency of Car→BChl transfer 40 3.3.3 B800-B850 transfer 44 3.3.4 LH-II→LH-II transfer 44 3.3.5 LH-II→LH-I transfer 45 3.3.6 LH-I→RC transfer 45 3.3.7 Excitation migration in the PSU 46 3.3.8 Genetic basis of PSU assembly 494. Concluding remarks 535. Acknowledgments 556. References 55Life as we know it today exists largely because of photosynthesis, the process through which light energy is converted into chemical energy by plants, algae, and photosynthetic bacteria (Priestley, 1772; Barnes, 1893; Wurmser, 1925; Van Niel, 1941; Clayton & Sistrom, 1978; Blankenship et al. 1995; Ort & Yocum, 1996). Historically, photosynthetic organisms are grouped into two classes. When photosynthesis is carried out in the presence of air it is called oxygenic photosynthesis (Ort & Yocum, 1996). Otherwise, it is anoxygenic (Blankenship et al. 1995). Higher plants, algae and cyanobacteria perform oxygenic photosynthesis, which involves reduction of carbon dioxide to carbohydrate and oxidation of water to produce molecular oxygen. Some photosynthetic bacteria, such as purple bacteria, carry out anoxygenic photosynthesis that involves oxidation of molecules other than water. In spite of these differences, the general principles of energy transduction are the same in anoxygenic and oxygenic photosynthesis (Van Niel, 1931, 1941; Stanier, 1961; Wraight, 1982; Gest, 1993). The primary processes of photosynthesis involve absorption of photons by light-harvesting complexes (LHs), transfer of excitation energy from LHs to the photosynthetic reaction centers (RCs), and the primary charge separation across the photosynthetic membrane (Sauer, 1975; Knox, 1977; Fleming & van Grondelle, 1994; van Grondelle et al. 1994). In this article, we will focus on the anoxygenic photosynthetic process in purple bacteria, since its photosynthetic system is the most studied and best characterized during the past 50 years.

Photosynthetic organisms fuel their metabolism with light energy and have developed for this purpose an efficient apparatus for harvesting sunlight. The atomic structure of the apparatus, as it evolved in purple bacteria, has been constructed through a combination of x-ray crystallography, electron microscopy, and modeling. The detailed structure and overall architecture reveals a hierarchical aggregate of pigments that utilizes, as shown through femtosecond spectroscopy and quantum physics, elegant and efficient mechanisms for primary light absorption and transfer of electronic excitation toward the photosynthetic reaction center.The prevalent color green in Earth's biosphere is testimony to the important role that chlorophylls play in harnessing the energy of the Sun to fuel the metabolism of photosynthetic life forms. Chlorophylls are assisted in their light-harvesting role by carotenoids, also widely known through their coloration of petals and fruits in plants. Photosynthetic organisms have evolved intricate aggregates of chlorophylls and carotenoids for efficient light harvesting and exploit in subtle ways the laws of quantum mechanics. This role of chlorophylls and carotenoids has emerged in full detail only recently, when the atomic structures of proteins involved in bacterial photosynthetic light harvesting have been solved by a combination of x-ray crystallography, electron microscopy, and molecular modeling.However, the conceptual foundation for our present understanding of light harvesting was laid long ago, when Emerson and Arnold demonstrated that it required hundreds of chlorophylls to reduce one molecule of CO 2 under saturating flash light intensity (1, 2). To explain the cooperative action of these chlorophylls, Emerson and Arnold postulated that only very few chlorophylls in the primary reaction site, termed the photosynthetic reaction center (RC), directly take part in photochemical reactions; most chlorophylls serve as lightharvesting antennae by capturing the sunlight and funneling electronic excitation toward the RC. This notion gave rise to the definition of the photosynthetic unit (PSU) as an ensemble of an RC with associated light-harvesting complexes containing up to 250 chlorophylls, and became widely accepted only when Duysens carried out a critical experiment in which energy transfer between different chlorophylls was observed (3).A wealth of accumulated evidence proves that the organization of PSUs, to surround an RC with aggregates of chlorophylls and associated carotenoids, is universal in both photosynthetic bacteria and higher plants (2,(4)(5)(6).Of the known photosynthetic systems, the PSU of purple bacteria is the most studied and best characterized. Fig. 1 depicts schematically the intracytoplasmic membrane of purple bacteria with its primary photosynthetic apparatus. In the PSU, an array of light-harvesting complexes captures light and transfers the excitation energy to the photosynthetic RC. This article focuses on the primary processes of light harvesting and elec...

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The Q y excitation energies of the 96 chlorophyll molecules in photosystem I of Synechococcus elongatus, both in and out of their protein environments, were obtained by using the semiempirical INDO/S method and the crystal structure geometries. The dipole-dipole approximation was used to calculate the coupling between the Q y states of chlorophylls; in the case of closely separated chlorophylls INDO/S dimer calculations were used to determine the couplings. The effective Hamiltonian for chlorophyll Q y excitations was constructed, enabling tentative assignment of red chlorophylls and calculation of the absorption spectrum of PSI.

In photosynthetic light-harvesting systems carotenoids and chlorophylls jointly absorb light and transform its energy within about a picosecond into electronic singlet excitations of the chlorophylls only. This paper investigates this process for the light-harvesting complex II of the purple bacterium Rhodospirillum molischianum, for which a structure and, hence, the exact arrangement of the participating bacteriochlorophylls and carotenoids have recently become known. Based on this structure and on CI expansions of the electronic states of individual chromophores ͑bacteriochlorophylls and carotenoids͒ as well as on an exciton description of a circular aggregate of bacteriochlorophylls, the excitation transfer between carotenoids and bacteriochlorophylls is described by means of Fermi's golden rule. The electronic coupling between the various electronic excitations is determined for all orders of multipoles ͑Coulomb mechanism͒ and includes the electron exchange ͑Dexter mechanism͒ term. The rates and efficiencies for different pathways of excitation transfer, e.g., 1 1 B u ϩ (carotenoid)→bacteriochlorophyll aggregate and 2 1 A g Ϫ (carotenoid)→ bacteriochlorophyll aggregate, are compared. The results show that in LH-II the Coulomb mechanism is dominant for the transfer of singlet excitations. The 1 1 B u ϩ →Q x pathway appears to be partially efficient, while the 2 1 A g Ϫ →Q y pathway, in our description, which does not include vibrational levels, is inefficient. An improved treatment of the excitation transfer from the 2 1 A g Ϫ state is required to account for observed transfer rates. Exciton splitting of bacteriochlorophyll Q y excitations slightly accelerates the excitation transfer from the 2 1 A g Ϫ state, while it plays a crucial role in accelerating the transfer from the B800 BChl Q y state. Photoprotection of bacteriochlorophylls through triplet quenching is investigated, too. The results suggest that eight of the 16 B850 bacteriochlorophylls in LH-II of Rhodospirillum molischianum are protected well by eight carotenoids observed in the x-ray structure of the protein. The remaining eight B850 bacteriochlorophylls can transfer their triplet excitation energy efficiently to their neighboring protected bacteriochlorophylls. Eight B800 bacteriochlorophylls appear not to be protected well by the observed carotenoids. ͓S1063-651X͑98͒11007-3͔

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