A minimal mathematical model of nonphotochemical quenching of chlorophyll fluorescence

Copyright © 2010 Elsevier Ireland Ltd. All rights reserved.Peer reviewedPreprin

Excitation Energy Transfer between Higher Excited States of Photosynthetic Pigments: 1. Carotenoids Intercept and Remove B Band Excitations

Chlorophylls (Chls) are known for fast, subpicosecond internal conversion (IC) from ultraviolet/blue-absorbing (“B” or “Soret” states) to the energetically lower, red light-absorbing Q states. Consequently, excitation energy transfer (EET) in photosynthetic pigment–protein complexes involving the B states has so far not been considered. We present, for the first time, a theoretical framework for the existence of B–B EET in tightly coupled Chl aggregates such as photosynthetic pigment–protein complexes. We show that according to a Förster resonance energy transport (FRET) scheme, unmodulated B–B EET has an unexpectedly high range. Unsuppressed, it could pose an existential threat: the damage potential of blue light for photochemical reaction centers (RCs) is well-known. This insight reveals so far undescribed roles for carotenoids (Crts, this article) and Chl b (next article in this series) of possibly vital importance. Our model system is the photosynthetic antenna pigment–protein complex (CP29). Here, we show that the B → Q IC is assisted by the optically allowed Crt state (S2): The sequence is B → S2 (Crt, unrelaxed) → S2 (Crt, relaxed) → Q. This sequence has the advantage of preventing ∼39% of Chl–Chl B–B EET since the Crt S2 state is a highly efficient FRET acceptor. The B–B EET range and thus the likelihood of CP29 to forward potentially harmful B excitations toward the RC are thus reduced. In contrast to the B band of Chls, most Crt energy donation is energetically located near the Q band, which allows for 74/80% backdonation (from lutein/violaxanthin) to Chls. Neoxanthin, on the other hand, likely donates in the B band region of Chl b, with 76% efficiency. Crts thus act not only in their currently proposed photoprotective roles but also as a crucial building block for any system that could otherwise deliver harmful “blue” excitations to the RCs

Excitation Energy Transfer between Higher Excited States of Photosynthetic Pigments: 2. Chlorophyll b is a B Band Excitation Trap

Chlorophylls (Chls) are known for fast, subpicosecond internal conversion (IC) from ultraviolet/blue absorbing (“B” or “Soret” states) to the energetically lower, red light-absorbing Q states. Consequently, excitation energy transfer (EET) in photosynthetic pigment–protein complexes involving the B states has so far not been considered. We present, for the first time, a theoretical framework for the existence of B–B EET in tightly coupled Chl aggregates such as photosynthetic pigment–protein complexes. We show that according to a Förster resonance energy transport (FRET) scheme, unmodulated B–B EET has an unexpectedly high range. Unsuppressed, it could pose an existential threat-the damage potential of blue light for photochemical reaction centers (RCs) is well-known. This insight reveals so-far undescribed roles for carotenoids (Crts, cf. previous article in this series) and Chl b (this article) of possibly vital importance. Our model system is the photosynthetic antenna pigment–protein complex (CP29). The focus of the study is on the role of Chl b for EET in the Q and B bands. Further, the initial excited pigment distribution in the B band is computed for relevant solar irradiation and wavelength-centered laser pulses. It is found that both accessory pigment classes compete efficiently with Chl a absorption in the B band, leaving only 40% of B band excitations for Chl a. B state population is preferentially relocated to Chl b after excitation of any Chls, due to a near-perfect match of Chl b B band absorption with Chl a B state emission spectra. This results in an efficient depletion of the Chl a population (0.66 per IC/EET step, as compared to 0.21 in a Chl a-only system). Since Chl b only occurs in the peripheral antenna complexes of plants and algae, and RCs contain only Chl a, this would automatically trap potentially dangerous B state population in the antennae, preventing forwarding to the RCs

Spectrally selective fluorescence imaging of Chlorobaculum tepidum reaction centers conjugated to chelator-modified silver nanowires

A polyhistidine tag (His-tag) present on Chlorobaculum tepidum reaction centers (RCs) was used to immobilize photosynthetic complexes on a silver nanowire (AgNW) modified with nickel-chelating nitrilo-triacetic acid (Ni-NTA). The optical properties of conjugated nanostructures were studied using wide-field and confocal fluorescence microscopy. Plasmonic enhancement of RCs conjugated to AgNWs was observed as their fluorescence intensity dependence on the excitation wavelength does not follow the excitation spectrum of RC complexes in solution. The strongest effect of plasmonic interactions on the emission intensity of RCs coincides with the absorption spectrum of AgNWs and is observed for excitation into the carotenoid absorption. From the absence of fluorescence decay shortening, we attribute the emission enhancement to increase of absorption in RC complexes

Light-harvesting antenna function of phycoerythrin in Prochlorococcus marinus

AbstractProchlorococcus marinus strain CCMP 1375 is the sole prokaryote to possess phycoerythrin in addition to (divinyl-)chlorophyll a/b binding antenna complexes. Here we demonstrate, employing a spectrofluorimetric assay, that phycoerythrin serves a light-harvesting antenna function (transfers energy to chlorophylls)

Inactivation of the geranylgeranyl reductase (ChlP) gene in the cyanobacterium Synechocystis sp. PCC 6803

AbstractGeranylgeranyl reductase catalyses the reduction of geranylgeranyl pyrophosphate to phytyl pyrophosphate required for synthesis of chlorophylls, phylloquinone and tocopherols. The gene chlP (ORF sll1091) encoding the enzyme has been inactivated in the cyanobacterium Synechocystis sp. PCC 6803. The resulting ΔchlP mutant accumulates exclusively geranylgeranylated chlorophyll a instead of its phytylated analogue as well as low amounts of α-tocotrienol instead of α-tocopherol. Whereas the contents of chlorophyll and total carotenoids are decreased, abundance of phycobilisomes is increased in ΔchlP cells. The mutant assembles functional photosystems I and II as judged from 77 K fluorescence and electron transport measurements. However, the mutant is unable to grow photoautotrophically due to instability and rapid degradation of the photosystems in the absence of added glucose. We suggest that instability of the photosystems in ΔchlP is directly related to accumulation of geranylgeranylated chlorophyll a. Increased rigidity of the chlorophyll isoprenoid tail moiety due to three additional CC bonds is the likely cause of photooxidative stress and reduced stability of photosynthetic pigment–protein complexes assembled with geranylgeranylated chlorophyll a in the ΔchlP mutant

Vibronic coupling explains the ultrafast carotenoid-to-bacteriochlorophyll energy transfer in natural and artificial light harvesters

The initial energy transfer in photosynthesis occurs between the light-harvesting pigments and on ultrafast timescales. We analyze the carotenoid to bacteriochlorophyll energy transfer in LH2 Marichromatium purpuratum as well as in an artificial light-harvesting dyad system by using transient grating and two-dimensional electronic spectroscopy with 10 fs time resolution. We find that F\"orster-type models reproduce the experimentally observed 60 fs transfer times, but overestimate coupling constants, which leads to a disagreement with both linear absorption and electronic 2D-spectra. We show that a vibronic model, which treats carotenoid vibrations on both electronic ground and excited state as part of the system's Hamiltonian, reproduces all measured quantities. Importantly, the vibronic model presented here can explain the fast energy transfer rates with only moderate coupling constants, which are in agreement with structure based calculations. Counterintuitively, the vibrational levels on the carotenoid electronic ground state play a central role in the excited state population transfer to bacteriochlorophyll as the resonance between the donor-acceptor energy gap and vibrational ground state energies is the physical basis of the ultrafast energy transfer rates in these systems

Homologous NF-YC2 Subunit from Arabidopsis and Tobacco Is Activated by Photooxidative Stress and Induces Flowering

The transcription factor NF-Y consists of the three subunits A, B and C, which are encoded in Arabidopsis in large gene families. The multiplicity of the genes implies that NF-Y may act in diverse combinations of each subunit for the transcriptional control. We aimed to assign a function in stress response and plant development to NF-YC subunits by analyzing the expression of NF-Y genes and exploitation of nf-y mutants. Among the subunit family, NF-YC2 showed the strongest inducibility towards oxidative stress, e.g. photodynamic, light, oxidative, heat and drought stress. A tobacco NF-YC homologous gene was found to be inducible by photooxidative stress generated by an accumulation of the tetrapyrrole metabolite, coproporphyrin. Despite the stress induction, an Arabidopsis nf-yc2 mutant and NF-YC2 overexpressors did not show phenotypical differences compared to wild-type seedlings in response to photooxidative stress. This can be explained by the compensatory potential of other members of the NF-YC family. However, NF-YC2 overexpression leads to an early flowering phenotype that is correlated with increased FLOWERING LOCUS T-transcript levels. It is proposed that NF-YC2 functions in floral induction and is a candidate gene among the NF-Y family for the transcriptional activation upon oxidative stress

Photoprotection in Plants Involves a Change in Lutein 1 Binding Domain in the Major Light-harvesting Complex of Photosystem II

Nonphotochemical quenching (NPQ) is the fundamental process by which plants exposed to high light intensities dissipate the potentially harmful excess energy as heat. Recently, it has been shown that efficient energy dissipation can be induced in the major light-harvesting complexes of photosystem II (LHCII) in the absence of protein-protein interactions. Spectroscopic measurements on these samples (LHCII gels) in the quenched state revealed specific alterations in the absorption and circular dichroism bands assigned to neoxanthin and lutein 1 molecules. In this work, we investigate the changes in conformation of the pigments involved in NPQ using resonance Raman spectroscopy. By selective excitation we show that, as well as the twisting of neoxanthin that has been reported previously, the lutein 1 pigment also undergoes a significant change in conformation when LHCII switches to the energy dissipative state. Selective two-photon excitation of carotenoid (Car) dark states (Car