Harry A. Frank

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.

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.

Photophysics of the carotenoids associated with the xanthophyll cycle in photosynthesis

Green plants use the xanthophyll cycle to regulate the flow of energy to chlorophylla within photosynthetic proteins. Under conditions of low light intensity violaxanthin, a carotenoid possessing nine conjugated double bonds, functions as an antenna pigment by transferring energy from its lowest excited singlet state to that of chlorophylla within light-harvesting proteins. When the light intensity increases, violaxanthin is biochemically transformed into zeaxanthin, a carotenoid that possesses eleven conjugated double bonds. The results presented here show that extension of the ⧄ conjugation of the polyene lowers the energy of the lowest excited singlet state of the carotenoid below that of chlorophylla. As a consequence zeaxanthin can act as a trap for the excess excitation energy on chlorophylla pigments within the protein, thus regulating the flow of energy within photosynthetic light-harvesting proteins.

Molecular Factors Controlling Photosynthetic Light Harvesting by Carotenoids

Carotenoids are naturally occurring pigments that absorb light in the spectral region in which the sun irradiates maximally. These molecules transfer this energy to chlorophylls, initiating the primary photochemical events of photosynthesis. Carotenoids also regulate the flow of energy within the photosynthetic apparatus and protect it from photoinduced damage caused by excess light absorption. To carry out these functions in nature, carotenoids are bound in discrete pigment-protein complexes in the proximity of chlorophylls. A few three-dimensional structures of these carotenoid complexes have been determined by X-ray crystallography. Thus, the stage is set for attempting to correlate the structural information with the spectroscopic properties of carotenoids to understand the molecular mechanism(s) of their function in photosynthetic systems. In this Account, we summarize current spectroscopic data describing the excited state energies and ultrafast dynamics of purified carotenoids in solution and bound in light-harvesting complexes from purple bacteria, marine algae, and green plants. Many of these complexes can be modified using mutagenesis or pigment exchange which facilitates the elucidation of correlations between structure and function. We describe the structural and electronic factors controlling the function of carotenoids as energy donors. We also discuss unresolved issues related to the nature of spectroscopically dark excited states, which could play a role in light harvesting. To illustrate the interplay between structural determinations and spectroscopic investigations that exemplifies work in the field, we describe the spectroscopic properties of four light-harvesting complexes whose structures have been determined to atomic resolution. The first, the LH2 complex from the purple bacterium Rhodopseudomonas acidophila, contains the carotenoid rhodopin glucoside. The second is the LHCII trimeric complex from higher plants which uses the carotenoids lutein, neoxanthin, and violaxanthin to transfer energy to chlorophyll. The third, the peridinin-chlorophyll-protein (PCP) from the dinoflagellate Amphidinium carterae, is the only known complex in which the bound carotenoid (peridinin) pigments outnumber the chlorophylls. The last is xanthorhodopsin from the eubacterium Salinibacter ruber. This complex contains the carotenoid salinixanthin, which transfers energy to a retinal chromophore. The carotenoids in these pigment-protein complexes transfer energy with high efficiency by optimizing both the distance and orientation of the carotenoid donor and chlorophyll acceptor molecules. Importantly, the versatility and robustness of carotenoids in these light-harvesting pigment-protein complexes have led to their incorporation in the design and synthesis of nanoscale antenna systems. In these bioinspired systems, researchers are seeking to improve the light capture and use of energy from the solar emission spectrum.

Energy transfer reactions involving carotenoids: quenching of chlorophyll fluorescence

Carotenoids have a key role in photosynthesis in photosynthetic systems, transferring excitation energy to chlorophyll (Chl) during light harvesting. These pigments also protect the photosynthetic apparatus from photodamage by quenching the Chl triplet state and singlet oxygen. In addition, in higher plants and some algae, a number of xanthophylls also have the ability to deactivate excited Chl under conditions of excess excitation via the operation of the xanthophyll cycle (violaxanthin<-->antheraxanthin<-->zeaxanthin or diadinoxanthin<-->diatoxanthin). The formation of zexanthin (or diatoxanthin) can be clearly correlated with the non-photochemical quenching of Chl fluorescence, and is now recognized as a major photoprotective process in higher plants and a number of algal genera. The interconversion of these xanthophylls in response to a changing light environment alters the extent of their carbon-carbon double bond conjugation, which, in turn, affects the excited state energies and lifetimes of the carotenoids and may also alter their structure/conformation and hydrophobicity. The possible roles of these photophysical and physicochemical changes in the mechanism(s) of xanthophyll-mediated energy dissipation via quenching of Chl fluorescence are discussed.

Femtosecond energy-transfer processes in the B800-850 light-harvesting complex of Rhodobacter sphaeroides 2.4.1

The B800-to-B850 energy transfer time in the purified B800-850 light-harvesting complex of Rhodobacter sphaeroides 2.4.1 is determined to be 0.7 ps at room temperature. The electronic state dynamics of the principal carotenoid of this species, spheroidene, are examined, both in vivo and in vitro, by direct femtosecond time-resolved experiments and by fluorescence emission yield studies. Evidence is presented which suggests that carotenoid-to-bacteriochlorophyll energy transfer may occur directly from the initially excited carotenoid S2 state, as well as from the carotenoid S1 state. Further support for this conjecture is obtained from calculations of energy transfer rates from the carotenoid S2 state. Previous measurements of in vivo carotenoid and B800 dynamics are discussed in light of the new results, and currently unresolved issues are described.

The application of the energy gap law to the S1 energies and dynamics of carotenoids

Abstract The energy gap law for radiationless transitions set forth by Englman and Jortner (Mol. Phys. 18 (1970) 145) has been evaluated for use in deducing the S 1 energies of carotenoids. A simultaneous knowledge of the dynamics and energies of the S 1 states of carotenoids are available for only a few of these molecules owing to the lack of detectable S 1 state fluorescence in many cases. All the available data where the S 1 dynamics and energies of carotenoids are simultaneously known were fit by the energy gap law expression in its full exponential form. The parameters derived from the computer optimization suggest that the weak coupling limit form of the energy gap law is valid for describing the relationship between the dynamics and energetics of carotenoid molecules. The optimal fitting parameters were then used in conjunction with the energy gap law expression to calculate the S 1 energies of several biologically important carotenoids from the lifetimes of their S 1 states. Particularly important is the S 1 energy of β-carotene determined in this analysis to be 14 100 cm −1 .

Low-lying electronic states of carotenoids

Four all-trans carotenoids, spheroidene, 3,4-dihydrospheroidene, 3,4,5,6-tetrahydrospheroidene, and 3,4,7,8-tetrahydrospheroidene, have been purified using HPLC techniques and analyzed using absorption, fluorescence and fluorescence excitation spectroscopy of room temperature solutions. This series of molecules, for which the extent of pi-electron conjugation decreases from 10 to seven carbon-carbon double bonds, exhibits a systematic crossover from S2----S0 (1(1)Bu----1(1)Ag) to S1----S0 (2(1)Ag----1(1)Ag) emission with decreasing chain length. Extrapolation of the S1----S0 transition energies indicates that the 2(1)Ag states of longer carotenoids have considerably lower energies than previously thought. The energies of the S1 states of spheroidenes and other long carotenoids are correlated with the S1 energies of their chlorophyll partners in antenna complexes of photosynthetic systems. Implications for energy transfer in photosynthetic antenna are discussed.

Zeaxanthin protects plant photosynthesis by modulating chlorophyll triplet yield in specific light-harvesting antenna subunits

Background: The plant carotenoid zeaxanthin is accumulated under excess light. Results: Zeaxanthin induces a red shift in the carotenoid triplet excited state spectrum and reveals a higher efficiency in controlling chlorophyll triplet formation. Conclusion: Binding of zeaxanthin to specific proteins modulates the yield of dangerous chlorophyll excited states and protects photosynthesis from over-excitation. Significance: Functional dissection of zeaxanthin-dependent photoprotective mechanisms is crucial for understanding how plants avoid photoinhibition. Plants are particularly prone to photo-oxidative damage caused by excess light. Photoprotection is essential for photosynthesis to proceed in oxygenic environments either by scavenging harmful reactive intermediates or preventing their accumulation to avoid photoinhibition. Carotenoids play a key role in protecting photosynthesis from the toxic effect of over-excitation; under excess light conditions, plants accumulate a specific carotenoid, zeaxanthin, that was shown to increase photoprotection. In this work we genetically dissected different components of zeaxanthin-dependent photoprotection. By using time-resolved differential spectroscopy in vivo, we identified a zeaxanthin-dependent optical signal characterized by a red shift in the carotenoid peak of the triplet-minus-singlet spectrum of leaves and pigment-binding proteins. By fractionating thylakoids into their component pigment binding complexes, the signal was found to originate from the monomeric Lhcb4–6 antenna components of Photosystem II and the Lhca1–4 subunits of Photosystem I. By analyzing mutants based on their sensitivity to excess light, the red-shifted triplet-minus-singlet signal was tightly correlated with photoprotection in the chloroplasts, suggesting the signal implies an increased efficiency of zeaxanthin in controlling chlorophyll triplet formation. Fluorescence-detected magnetic resonance analysis showed a decrease in the amplitude of signals assigned to chlorophyll triplets belonging to the monomeric antenna complexes of Photosystem II upon zeaxanthin binding; however, the amplitude of carotenoid triplet signal does not increase correspondingly. Results show that the high light-induced binding of zeaxanthin to specific proteins plays a major role in enhancing photoprotection by modulating the yield of potentially dangerous chlorophyll-excited states in vivo and preventing the production of singlet oxygen.