Richard J. Cogdell

Carotenoids in photosynthesis

Carotenoids are usually considered to perform two major functions in photosynthesis. They serve as accessory light harvesting pigments, extending the range of wavelengths over which light can drive photosynthesis, and they act to protect the chlorophyllous pigments from the harmful photodestructive reaction which occurs in the presence of oxygen. Drawing upon recent work with photosynthetic bacteria, evidence is presented as to how the carotenoids are organized within both portions of the photosynthetic unit (the light harvesting antenna and the reaction centre) and how they discharge both their functions. The accessory pigment role is a singlet-singlet energy transfer from the carotenoid to the bacteriochlorophyll, while the protective role is a triplet-triplet energy transfer from the bacteriochlorophyll to the carotenoid.

Quantum control of energy flow in light harvesting

Coherent light sources have been widely used in control schemes that exploit quantum interference effects to direct the outcome of photochemical processes. The adaptive shaping of laser pulses is a particularly powerful tool in this context: experimental output as feedback in an iterative learning loop refines the applied laser field to render it best suited to constraints set by the experimenter. This approach has been experimentally implemented to control a variety of processes, but the extent to which coherent excitation can also be used to direct the dynamics of complex molecular systems in a condensed-phase environment remains unclear. Here we report feedback-optimized coherent control over the energy-flow pathways in the light-harvesting antenna complex LH2 from Rhodopseudomonas acidophila, a photosynthetic purple bacterium. We show that phases imprinted by the light field mediate the branching ratio of energy transfer between intra- and intermolecular channels in the complexs donor–acceptor system. This result illustrates that molecular complexity need not prevent coherent control, which can thus be extended to probe and affect biological functions.

The photochemistry of carotenoids

Preface. Color Plates. Part I: Biosynthetic Pathways and the Distribution of Carotenoids in Photosynthetic Organisms. 1. Carotenoids in Photosynthesis: An Historical Perspective Govindjee. 2. Carotenoid Synthesis and Function in Plants: Insights from Mutant Studies in Arabidopsis thaliana D. DellaPenna. 3. Carotenoids and Carotenogenesis in Anoxygenic Photosynthetic Bacteria S. Takaichi. Part II: Structure of Carotenoid-Chlorophyll Protein Complexes. 4. The Structure and Function of the LH2 Complex from Rhodopseudomonas acidophila Strain 10050, with Special Reference to the Bound Carotenoid R.J. Cogdell, et al. 5. Carotenoids as Components of the Light-harvesting Proteins of Eukaryotic Algae R.G. Hiller. 6. The Structure of Reaction Centers from Purple Bacteria G. Fritzsch, A. Kuglstatter. 7. Carotenoids and the Assembly of Light-Harvesting Complexes H. Paulsen. Part III: Electronic Structure, Stereochemistry, Spectroscopy, Dynamics and Radicals. 8. The Electronic States of Carotenoids R.L. Christensen. 9. Cis-Trans Carotenoids in Photosynthesis: Configurations, Excited-State Properties and Physiological Functions Y. Koyama, R. Fujii. 10. The Electronic Structure, Stereochemistry and Resonance Raman Spectroscopy of Carotenoids B. Robert. 11. Electron Magnetic Resonance of Carotenoids A. Angerhofer. 12. Carotenoid Radicals and the Interaction of Carotenoids with Active Oxygen Species R. Edge, T.G. Truscott. 13. Incorporation of Carotenoids into ReactionCenter and Light-Harvesting Pigment-protein Complexes H.A. Frank. Part IV: Ecophysiology and the Xanthophyll Cycle. 14. Ecophysiology of the Xanthophyll Cycle B. Demmig-Adams, et al. 15. Regulation of the Structure and Function of the Light-Harvesting Complexes of Photosystem II by the Xanthophyll Cycle P. Horton, et al. 16. Biochemistry and Molecular Biology of the Xanthophyll Cycle H.Y. Yamamoto, et al. 17. Relationships Between Antioxidant Metabolism and Carotenoids in the Regulation of Photosynthesis C.H. Foyer, J. Harbinson. Part V: Model Systems. 18. Novel and Biomimetic Functions of Carotenoids in Artificial Photosynthesis T.A. Moore, et al. 19. Physical Properties of Carotenoids in the Solid State H. Hashimoto. 20. Carotenoids in Membranes W.I. Gruszecki. Index.

How carotenoids function in photosynthetic bacteria

Carotenoids are essential for the survival of photosynthetic organisms. They function as light-harvesting molecules and provide photoprotection. In this review, the molecular features which determine the efficiencies of the various photophysical and photochemical processes of carotenoids are discussed. The behavior of carotenoids in photosynthetic bacterial reaction centers and light-harvesting complexes is correlated with data from experiments carried out on carotenoids and model systems in vitro. The status of the carotenoid structural determinations in vivo is reviewed.

The Structure and Thermal Motion of the B800–850 LH2 Complex from Rps. acidophila at 2.0 Å Resolution and 100 K: New Structural Features and Functionally Relevant Motions

The structure at 100K of integral membrane light-harvesting complex II (LH2) from Rhodopseudomonas acidophila strain 10050 has been refined to 2.0A resolution. The electron density has been significantly improved, compared to the 2.5A resolution map, by high resolution data, cryo-cooling and translation, libration, screw (TLS) refinement. The electron density reveals a second carotenoid molecule, the last five C-terminal residues of the alpha-chain and a carboxy modified alpha-Met1 which forms the ligand of the B800 bacteriochlorophyll. TLS refinement has enabled the characterisation of displacements between molecules in the complex. B850 bacteriochlorophyll molecules are arranged in a ring of 18 pigments composed of nine approximate dimers. These pigments are strongly coupled and at their equilibrium positions the excited state dipole interaction energies, within and between dimers, are approximately 370cm(-1) and 280cm(-1), respectively. This difference in coupling energy is similar in magnitude to changes in interaction energies arising from the pigment displacements described by TLS tensors. The displacements appear to be non-random in nature and appear to be designed to optimise the modulation of pigment energy interactions. This is the first time that LH2 pigment displacements have been quantified experimentally. The calculated energy changes indicate that there may be significant contributions to inter-pigment energy interactions from molecular displacements and these may be of importance to photosynthetic energy transfer.

An unusual pathway of excitation energy deactivation in carotenoids: Singlet-to-triplet conversion on an ultrafast timescale in a photosynthetic antenna

Carotenoids are important biomolecules that are ubiquitous in nature and find widespread application in medicine. In photosynthesis, they have a large role in light harvesting (LH) and photoprotection. They exert their LH function by donating their excited singlet state to nearby (bacterio)chlorophyll molecules. In photosynthetic bacteria, the efficiency of this energy transfer process can be as low as 30%. Here, we present evidence that an unusual pathway of excited state relaxation in carotenoids underlies this poor LH function, by which carotenoid triplet states are generated directly from carotenoid singlet states. This pathway, operative on a femtosecond and picosecond timescale, involves an intermediate state, which we identify as a new, hitherto uncharacterized carotenoid singlet excited state. In LH complex-bound carotenoids, this state is the precursor on the reaction pathway to the triplet state, whereas in extracted carotenoids in solution, this state returns to the singlet ground state without forming any triplets. We discuss the possible identity of this excited state and argue that fission of the singlet state into a pair of triplet states on individual carotenoid molecules constitutes the mechanism by which the triplets are generated. This is, to our knowledge, the first ever direct observation of a singlet-to-triplet conversion process on an ultrafast timescale in a photosynthetic antenna.

Structure‐Based Calculations of the Optical Spectra of the LH2 Bacteriochlorophyll‐Protein Complex from Rhodopseudomonas acidophila

Abstract— The molecular structure of the light‐harvesting complex 2 (LH2) bacteriochlorophyll‐protein antenna complex from the purple non‐sulfur photosynthetic bacterium Rhodopseudomonas acidophila, strain 10050 provides the positions and orientations of the 27 bacteriochlorophyll (BChl) molecules in the complex. Our structure‐based model calculations of the distinctive optical properties (absorption, CD, polarization) of LH2 in the near‐infrared region use a point‐monopole approximation to represent the BChl Qy transition moment. The results of the calculations support the assignment of the ring of 18 closely coupled BChl to B850 (BChl absorbing at 850 nm) and the larger diameter, parallel ring of 9 weakly coupled BChl to B800. All of the significantly allowed transitions in the near infrared are calculated to be perpendicular to the C9 symmetry axis, in agreement with polarization studies of this membrane‐associated complex. To match the absorption maxima of the B800 and B850 components using a relative permittivity (dielectric constant) of 2.1, we assign different site energies (12 500 and 12260 cm−1, respectively) for the Qy transitions of the respective BChl in their protein binding sites. Excitonic coupling is particularly strong among the set of B850 chromophores, with pairwise interaction energies nearly 300 cm between nearest neighbors, comparable with the experimental absorption bandwidths at room temperature. These strong interactions, for the full set of 18 B850 chromophores, result in an excitonic manifold that is 1200 cm−1 wide. Some of the upper excitonic states should result in weak absorption and perhaps stronger CD features. These predictions from the calculations await experimental verification.

Quantum Coherent Energy Transfer over Varying Pathways in Single Light-Harvesting Complexes

Coherence in Photosynthesis It is unclear how energy absorbed by pigments in antenna proteins is transferred to the central site of chemical catalysis during photosynthesis. Hildner et al. (p. 1448) observed coherence—prolonged persistence of a quantum mechanical phase relationship—at the single-molecule level in light-harvesting complexes from purple bacteria. The results bolster conclusions from past ensemble measurements that coherence plays a pivotal role in photosynthetic energy transfer. Hayes et al. (p. 1431, published online 18 April) examined a series of small molecules comprised of bridged chromophores that also manifest prolonged coherence. A phase relation observed in ensemble measurements of photosynthetic proteins is borne out at the single-molecule level. The initial steps of photosynthesis comprise the absorption of sunlight by pigment-protein antenna complexes followed by rapid and highly efficient funneling of excitation energy to a reaction center. In these transport processes, signatures of unexpectedly long-lived coherences have emerged in two-dimensional ensemble spectra of various light-harvesting complexes. Here, we demonstrate ultrafast quantum coherent energy transfer within individual antenna complexes of a purple bacterium under physiological conditions. We find that quantum coherences between electronically coupled energy eigenstates persist at least 400 femtoseconds and that distinct energy-transfer pathways that change with time can be identified in each complex. Our data suggest that long-lived quantum coherence renders energy transfer in photosynthetic systems robust in the presence of disorder, which is a prerequisite for efficient light harvesting.

Two-dimensional electronic spectroscopy of the B800–B820 light-harvesting complex

Emerging nonlinear optical spectroscopies enable deeper insight into the intricate world of interactions and dynamics of complex molecular systems. 2D electronic spectroscopy appears to be especially well suited for studying multichromophoric complexes such as light-harvesting complexes of photosynthetic organisms as it allows direct observation of couplings between the pigments and charts dynamics of energy flow on a 2D frequency map. Here, we demonstrate that a single 2D experiment combined with self-consistent theoretical modeling can determine spectroscopic parameters dictating excitation energy dynamics in the bacterial B800–B820 light-harvesting complex, which contains 27 bacteriochlorophyll molecules. Ultrafast sub-50-fs dynamics dominated by coherent intraband processes and population transfer dynamics on a picosecond time scale were measured and modeled with one consistent set of parameters. Theoretical 2D spectra were calculated by using a Frenkel exciton model and modified Förster/Redfield theory for the calculation of dynamics. They match the main features of experimental spectra at all population times well, implying that the energy level structure and transition dipole strengths are modeled correctly in addition to the energy transfer dynamics of the system.

An alternative carotenoid-to-bacteriochlorophyll energy transfer pathway in photosynthetic light harvesting

Blue and green sunlight become available for photosynthetic energy conversion through the light-harvesting (LH) function of carotenoids, which involves transfer of carotenoid singlet excited states to nearby (bacterio)chlorophylls (BChls). The excited-state manifold of carotenoids usually is described in terms of two singlet states, S1 and S2, of which only the latter can be populated from the ground state by the absorption of one photon. Both states are capable of energy transfer to (B)Chl. We recently showed that in the LH1 complex of the purple bacterium Rhodospirillum rubrum, which is rather inefficient in carotenoid-to-BChl energy transfer, a third additional carotenoid excited singlet state is formed. This state, which we termed S*, was found to be a precursor on an ultrafast fission reaction pathway to carotenoid triplet state formation. Here we present evidence that S* is formed with significant yield in the LH2 complex of Rhodobacter sphaeroides, which has a highly efficient carotenoid LH function. We demonstrate that S* is actively involved in the energy transfer process to BChl and thus have uncovered an alternative pathway of carotenoid-to-BChl energy transfer. In competition with energy transfer to BChl, fission occurs from S*, leading to ultrafast formation of carotenoid triplets. Analysis in terms of a kinetic model indicates that energy transfer through S* accounts for 10–15% of the total energy transfer to BChl, and that inclusion of this pathway is necessary to obtain a highly efficient LH function of carotenoids.