Resonance Raman Spectra and Electronic Transitions in Carotenoids: A Density Functional Theory Study

Mačernis, Mindaugas; Šulskus, Juozas; Malickaja, Svetlana; Robert, Bruno; Valkūnas, Leonas

doi:10.1021/jp406449c

Cited by 65 publications

(95 citation statements)

References 44 publications

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“…The Raman spectra and relative intensities of Raman peaks were simulated at the same levels of theory on corresponding optimized geometries. This approach was successfully applied in previous studies to model substituent effects on the Raman spectra of carotenoid molecules (45,46). The ultrafine grid keyword was specified for all DFT calculations and the Raman and Wiberg bond order calculations (47) were carried out in Gaussian 09.…”

Section: Methodsmentioning

confidence: 99%

Triplet–triplet energy transfer in artificial and natural photosynthetic antennas

Kish

Méndez-Hernández

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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In photosynthetic organisms, protection against photooxidative stress due to singlet oxygen is provided by carotenoid molecules, which quench chlorophyll triplet species before they can sensitize singlet oxygen formation. In anoxygenic photosynthetic organisms, in which exposure to oxygen is low, chlorophyll-to-carotenoid triplet-triplet energy transfer (T-TET) is slow, in the tens of nanoseconds range, whereas it is ultrafast in the oxygen-rich chloroplasts of oxygen-evolving photosynthetic organisms. To better understand the structural features and resulting electronic coupling that leads to T-TET dynamics adapted to ambient oxygen activity, we have carried out experimental and theoretical studies of two isomeric carotenoporphyrin molecular dyads having different conformations and therefore different interchromophore electronic interactions. This pair of dyads reproduces the characteristics of fast and slow T-TET, including a resonance Raman-based spectroscopic marker of strong electronic coupling and fast T-TET that has been observed in photosynthesis. As identified by density functional theory (DFT) calculations, the spectroscopic marker associated with fast T-TET is due primarily to a geometrical perturbation of the carotenoid backbone in the triplet state induced by the interchromophore interaction. This is also the case for the natural systems, as demonstrated by the hybrid quantum mechanics/molecular mechanics (QM/MM) simulations of light-harvesting proteins from oxygenic (LHCII) and anoxygenic organisms (LH2). Both DFT and electron paramagnetic resonance (EPR) analyses further indicate that, upon T-TET, the triplet wave function is localized on the carotenoid in both dyads.artificial photosynthesis | photoprotection | DFT calculations | triplet-triplet energy transfer | resonance Raman P hotoprotection is central to the maintenance of photosynthesis. Under certain circumstances, chlorophyll excited triplet states may form from intersystem crossing and from electron-hole recombination reactions in reaction centers. Chlorophyll triplet species can sensitize the formation of singlet oxygen, a deleterious reactive oxygen species (1). In photosynthetic complexes, this sensitization reaction is precluded by sufficiently rapid transfer of the triplet excited state from chlorophyll (Chl) or bacteriochlorophyll (BChl) to carotenoid molecules. The triplet states of carotenoids involved in photoprotection are well below the energy of singlet oxygen and therefore do not sensitize singlet oxygen. This quenching reaction reduces the lifetime of the Chl or BChl triplet state by many orders of magnitude (1) and renders it kinetically incompetent to sensitize singlet oxygen. Moreover, carotenoids can quench singlet oxygen directly in the event that it is inadvertently formed.In the light-harvesting (LH) proteins from most (anoxygenic) purple bacteria, triplet-triplet energy transfer (T-TET) from BChl to carotenoid molecules occurs on the nanosecond timescale (2, 3). By contrast, in light-harvesting complexes (LHCs) from...

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Section: Methodsmentioning

confidence: 99%

Triplet–triplet energy transfer in artificial and natural photosynthetic antennas

Kish

Méndez-Hernández

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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“…In solvent, ␤-carotene displays an effective conjugation length of 9.6, shorter than its 11 CϭC-conjugated chain, and this was attributed to out-of-plane positions of its conjugated end-cycles due to torsional twisting of the terminal rings of carotenoids that contain conjugated CϭC bonds (43,44). We may thus further conclude that ␤-Car 1 in Ycf39-HliD displays a configuration close to that observed in solvents, and is bound in a moderate polarizability binding site, whereas ␤-Car 2 have its C-5,6 (and C-5Ј,6Ј) double bonds in the ␤-rings clearly more conjugated to the electronic system, and thus that its rings must be maintained close to the plane of the conjugated carbon chain.…”

Section: Twisting a ␤-Carotene For Photoprotectionmentioning

confidence: 99%

“…Its effective conjugation is close to that of its theoretically maximum (n ϭ 11), and it is furthermore, bound to a binding site of high polarizability (comparable with carbon disulfide). It is well known that for terminal conjugated rings, the interaction of end groups with the polyene chain leads to steric deformations of around 45°for ␤-carotene (44). This deformation at the ends of the polyene chains together with the influence of end CH 3 groups or ␤-rings in carotenes causes smaller participation of orbitals from C 5 and C 6 atoms in HOMO and LUMO of the polyene chain, diminishing the effective conjugation length (44) as we observe for ␤-Car 1 .…”

Section: Twisting a ␤-Carotene For Photoprotectionmentioning

confidence: 99%

Twisting a β-Carotene, an Adaptive Trick from Nature for Dissipating Energy during Photoprotection

Llansola-Portolés

Sobotka

Kish

et al. 2017

Journal of Biological Chemistry

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Edited by James N. SiedowCyanobacteria possess a family of one-helix high light-inducible proteins (Hlips) that are homologous to light-harvesting antenna of plants and algae. An Hlip protein, high light-inducible protein D (HliD) purified as a small complex with the Ycf39 protein is evaluated using resonance Raman spectroscopy. We show that the HliD binds two different ␤-carotenes, each present in two non-equivalent binding pockets with different conformations, having their (0,0) absorption maxima at 489 and 522 nm, respectively. Both populations of ␤-carotene molecules were in all-trans configuration and the absorption position of the farthest blue-shifted ␤-carotene was attributed entirely to the polarizability of the environment in its binding pocket. In contrast, the absorption maximum of the red-shifted ␤-carotene was attributed to two different factors: the polarizability of the environment in its binding pocket and, more importantly, to the conformation of its ␤-rings. This second ␤-carotene has highly twisted ␤-rings adopting a flat conformation, which implies that the effective conjugation length N is extended up to 10.5 modifying the energetic levels. This increase in N will also result in a lower S 1 energy state, which may provide a permanent energy dissipation channel. Analysis of the carbonyl stretching region for chlorophyll a excitations indicates that the HliD binds six chlorophyll a molecules in five non-equivalent binding sites, with at least one chlorophyll a presenting a slight distortion to its macrocycle. The binding modes and conformations of HliD-bound pigments are discussed with respect to the known structures of LHCII and CP29.In nature, photosynthetic organisms obtain their energy by collecting solar photons, using complex arrays of pigments known as antennas. Subsequently, the energy harvested by the antennas is transferred to reaction centers to be transduced into electrochemical potential. Finally after a cascade of molecular steps, this energy is stored as potential chemical energy that is easy to store and transport (1). To accomplish this process, these organisms have developed a large number of different protein antenna assemblies, a notable subgroup of which are the light-harvesting complexes (LHCs) 3 of green plants and algae. LHCs constitute a large family of proteins, which can exist as monomers, dimers, or trimers in the membrane, and have related amino acid sequences. It is hypothesized that in the evolution of photosynthesis there was, and continues to be, a selective advantage for the organism to make optimum use of low light conditions to drive the relatively slow downstream metabolic reactions of legacy biochemistry (2). Plants, algae, and cyanobacteria are oxygenic photosynthetic organisms that are exposed to random fluctuations in light intensity. In the case of low light requiring large antennas, during high light exposure, most of the energy absorbed is in excess of that required to drive downstream metabolism. If excess light energy is not dealt with properly, i...

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“…However, in solution β-carotene and lutein exhibit a shorter effective conjugation length than expected when counting the number of C_C double bonds in their isoprene chain, including the terminal β-cycles [9]. This shorter conjugation length is likely to be due to an s-cis configuration of the β-cycles due to steric hindrance, such that they are twisted slightly out of the conjugated plane [24]. It was thus proposed that, in both PSII reaction centers and LHCII, the pigment binding site of the redabsorbing carotenoid brings the conjugated cycle(s) back into the plane of the molecule through steric hindrance, red-shifting its absorption by increasing its effective conjugation length [9].…”

Section: Tuning Carotenoid Absorption In Photosynthetic Proteinsmentioning

confidence: 93%

“…In addition, progress in DFT and time-dependent DFT, which now result in reasonable modeling of the vibrational spectra of molecules as complex as the photosynthetic pigments (see e.g. [24]), should in the next decade become an unavoidable support to formalize the data obtained by vibrational spectroscopy.…”

Section: Final Wordmentioning

confidence: 99%

Vibrational techniques applied to photosynthesis: Resonance Raman and fluorescence line-narrowing

Gall

Pascal

Robert

2015

Biochimica et Biophysica Acta (BBA) - Bioenergetics

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Resonance Raman spectroscopy may yield precise information on the conformation of, and the interactions assumed by, the chromophores involved in the first steps of the photosynthetic process. Selectivity is achieved via resonance with the absorption transition of the chromophore of interest. Fluorescence line-narrowing spectroscopy is a complementary technique, in that it provides the same level of information (structure, conformation, interactions), but in this case for the emitting pigment(s) only (whether isolated or in an ensemble of interacting chromophores). The selectivity provided by these vibrational techniques allows for the analysis of pigment molecules not only when they are isolated in solvents, but also when embedded in soluble or membrane proteins and even, as shown recently, in vivo. They can be used, for instance, to relate the electronic properties of these pigment molecules to their structure and/or the physical properties of their environment. These techniques are even able to follow subtle changes in chromophore conformation associated with regulatory processes. After a short introduction to the physical principles that govern resonance Raman and fluorescence line-narrowing spectroscopies, the information content of the vibrational spectra of chlorophyll and carotenoid molecules is described in this article, together with the experiments which helped in determining which structural parameter(s) each vibrational band is sensitive to. A selection of applications is then presented, in order to illustrate how these techniques have been used in the field of photosynthesis, and what type of information has been obtained. This article is part of a Special Issue entitled: Vibrational spectroscopies and bioenergetic systems.

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Resonance Raman Spectra and Electronic Transitions in Carotenoids: A Density Functional Theory Study

Cited by 65 publications

References 44 publications

Triplet–triplet energy transfer in artificial and natural photosynthetic antennas

Triplet–triplet energy transfer in artificial and natural photosynthetic antennas

Twisting a β-Carotene, an Adaptive Trick from Nature for Dissipating Energy during Photoprotection

Vibrational techniques applied to photosynthesis: Resonance Raman and fluorescence line-narrowing

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