Light-harvesting mechanism of bacteria exploits a critical interplay between the dynamics of transport and trapping.

Light-harvesting bacteria Rhodospirillum photometricum were recently found to adopt strikingly different architectures depending on illumination conditions. We present analytic and numerical calculations which explain this observation by quantifying a dynamical interplay between excitation transfer kinetics and reaction center cycling. High light-intensity membranes exploit dissipation as a photoprotective mechanism, thereby safeguarding a steady supply of chemical energy, while low light-intensity membranes efficiently process unused illumination intensity by channeling it to open reaction centers. More generally, our analysis elucidates and quantifies the trade-offs in natural network design for solar energy conversion.

Dynamics and diffusion in photosynthetic membranes from rhodospirillum photometricum.

Photosynthetic organisms drive their metabolism by converting light energy into an electrochemical gradient with high efficiency. This conversion depends on the diffusion of quinones within the membrane. In purple photosynthetic bacteria, quinones reduced by the reaction center (RC) diffuse to the cytochrome bc(1) complex and then return once reoxidized to the RC. In Rhodospirillum photometricum the RC-containing core complexes are found in a disordered molecular environment, with fixed light-harvesting complex/core complex ratio but without a fixed architecture, whereas additional light-harvesting complexes synthesized under low-light conditions pack into large paracrystalline antenna domains. Here, we have analyzed, using time-lapse atomic force microscopy, the dynamics of the protein complexes in the different membrane domains and find that the disordered regions are dynamic whereas ordered antennae domains are static. Based on our observations we propose, and analyze using Monte Carlo simulations, a model for quinone diffusion in photosynthetic membranes. We show that the formation of large static antennae domains may represent a strategy for increasing electron transfer rates between distant complexes within the membrane and thus be important for photosynthetic efficiency.

Theoretical prediction of spectral and optical properties of bacteriochlorophylls in thermally disordered LH2 antenna complexes.

A general approach for calculating spectral and optical properties of pigment-protein complexes of known atomic structure is presented. The method, that combines molecular dynamics simulations, quantum chemistry calculations, and statistical mechanical modeling, is demonstrated by calculating the absorption and circular dichroism spectra of the B800-B850 bacteriochlorophylls of the LH2 antenna complex from Rs. molischianum at room temperature. The calculated spectra are found to be in good agreement with the available experimental results. The calculations reveal that the broadening of the B800 band is mainly caused by the interactions with the polar protein environment, while the broadening of the B850 band is due to the excitonic interactions. Since it contains no fitting parameters, in principle, the proposed method can be used to predict optical spectra of arbitrary pigment-protein complexes of known structure.

Circular dichroism of carotenoids in bacterial light-harvesting complexes: experiments and modeling.

In this work we investigate the origin and characteristics of the circular dichroism (CD) spectrum of rhodopin glucoside and lycopene in the light-harvesting 2 complex of Rhodopseudomonas acidophila and Rhodospirillum molischianum, respectively. We successfully model their absorption and CD spectra based on the high-resolution structures. We assume that these spectra originate from seven interacting transition dipole moments: the first corresponds to the 0-0 transition of the carotenoid, whereas the remaining six represent higher vibronic components of the S2 state. From the absorption spectra we get an estimate of the Franck-Condon factors of these transitions. Furthermore, we investigate the broadening mechanisms that lead to the final shape of the spectra and get an insight into the interaction energy between carotenoids. Finally, we examine the consequences of rotations of the carotenoid transition dipole moment and of deformations in the light-harvesting 2 complex rings. Comparison of the modeled carotenoid spectra with modeled spectra of the bacteriochlorophyll QY region leads to a refinement of the modeling procedure and an improvement of all calculated results. We therefore propose that the combined carotenoid and bacteriochlorophyll CD can be used as an accurate reflection of the overall structure of the light-harvesting complexes.

Low-intensity pump-probe measurements on the B800 band of Rhodospirillum molischianum.

We have measured low-intensity, polarized one-color pump-probe traces in the B800 band of the light-harvesting complex LH2 of Rhodospirillum molischianum at 77 K. The excitation/detection wavelength was tuned through the B800 band. A single-wavelength and a global target analysis of the data were performed with a model that accounts for excitation energy transfer among the B800 molecules and from B800 to B850. By including the anisotropy of the signals into the fitting procedure, both transfer processes could be separated. It was estimated in the global target analysis that the intra-B800 energy transfer, i.e., the hopping of the excitation from one B800 to another B800 molecule, takes approximately 0.5 ps at 77 K. This transfer time increases with the excitation/detection wavelength from 0.3 ps on the blue side of the B800 band to approximately 0.8 ps on the red side. The residual B800 anisotropy shows a wavelength dependence as expected for energy transfer within an inhomogeneously broadened cluster of weakly coupled pigments. In the global target analysis, the transfer time from B800 to B850 was determined to be approximately 1.7 ps at 77 K. In the single-wavelength analysis, a speeding-up of the B800 --> B850 energy transfer rate toward the blue edge of the B800 band was found. This nicely correlates with the proposed position of the suggested high-exciton component of the B850 band acting as an additional decay channel for B800 excitations.

Photoresponses of the purple nonsulfur bacteria Rhodospirillum centenum and Rhodobacter sphaeroides.

We have measured the photoresponse of two purple nonsulfur bacteria, Rhodobacter sphaeroides and Rhodospirillum centenum, under defined conditions in a light beam propagating at 90 degrees to the optical axis of the microscope. This beam presented cells with a steep gradient of intensity perpendicular to the direction of propagation and a shallow gradient in the direction of light propagation. R. centenum, a species that reverses to change direction, accumulated in the light beam, as expected for a "scotophobic" response, while R. sphaeroides, which stops rather than reverses, accumulated outside the light beam. We also compared the behavior of liquid-grown R. centenum, which swims by using a single polar flagellum, to that of surface-grown R. centenum, which swarms over agar by using many lateral flagella and has been shown to move as colonies toward specific wavelengths of light. When suspended in liquid medium, both liquid- and surface-grown R. centenum showed similar responses to the light gradient. In all cases, free-swimming cells responded to the steep gradient of intensity but not to the shallow gradient, indicating they cannot sense the direction of light propagation but only its intensity. In a control experiment, the known phototactic alga Chlamydamonas reinhardtii was shown to swim in the direction of light propagation.