The wavelength of the incident light determines the primary charge separation pathway in Photosystem II

Pavlou, Andrea; Jacques, Julien; Ahmadova, Nigar; Mamedov, Fikret; Styring, Stenbjörn

doi:10.1038/s41598-018-21101-w

Cited by 14 publications

(18 citation statements)

References 59 publications

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“…Our results are also in very good agreement with the suggestion that Y Z becomes the preferred electron donor under far-red light at 5 K. The migration of the Chl D1 hole to the special pair would require a reorganization of the protein environment that is probably inhibited at cryogenic temperature, resulting in Y Z becoming an electron donor to Chl D1 . Further EPR experiments 39 showed that charge separation upon light excitation is wavelength-dependent, leading to the hypothesis that P D1 is excited with visible light (532 nm), whereas Chl D1 is excited with far-red light. 39 Our results on the P D1 –P D2 –Chl D1 trimer do not support the presence of any energetically accessible CT state that could lead directly to productive charge separation along the D1 branch, but the conditions under which the special pair may function as the primary donor will need further studies to be clarified.…”

Section: Resultsmentioning

confidence: 99%

“…Further EPR experiments 39 showed that charge separation upon light excitation is wavelength-dependent, leading to the hypothesis that P D1 is excited with visible light (532 nm), whereas Chl D1 is excited with far-red light. 39 Our results on the P D1 –P D2 –Chl D1 trimer do not support the presence of any energetically accessible CT state that could lead directly to productive charge separation along the D1 branch, but the conditions under which the special pair may function as the primary donor will need further studies to be clarified.…”

Section: Resultsmentioning

confidence: 99%

“… 39 An important fact is that although the working threshold of PSII is typically considered to be 680 nm, charge separation in the reaction center can be initiated with far-red light (700–780 nm) either by direct excitation of a low-lying charge transfer state in Chl a RCs or by excitation of far-red chlorophylls (Chl d and f ). 38 , 39 , 41 − 50 These observations highlight the significance of low-energy charge-transfer states for RC function. 17 Remarkably, no quantum chemical study has so far identified interpigment CT excited states low enough in energy to be consistent with these observations.…”

Section: Introductionmentioning

confidence: 99%

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Protein Matrix Control of Reaction Center Excitation in Photosystem II

2020

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Photosystem II (PSII) is a multisubunit pigment–protein complex that uses light-induced charge separation to power oxygenic photosynthesis. Its reaction center chromophores, where the charge transfer cascade is initiated, are arranged symmetrically along the D1 and D2 core polypeptides and comprise four chlorophyll (P D1 , P D2 , Chl D1 , Chl D2 ) and two pheophytin molecules (Pheo D1 and Pheo D2 ). Evolution favored productive electron transfer only via the D1 branch, with the precise nature of primary excitation and the factors that control asymmetric charge transfer remaining under investigation. Here we present a detailed atomistic description for both. We combine large-scale simulations of membrane-embedded PSII with high-level quantum-mechanics/molecular-mechanics (QM/MM) calculations of individual and coupled reaction center chromophores to describe reaction center excited states. We employ both range-separated time-dependent density functional theory and the recently developed domain based local pair natural orbital (DLPNO) implementation of the similarity transformed equation of motion coupled cluster theory with single and double excitations (STEOM-CCSD), the first coupled cluster QM/MM calculations of the reaction center. We find that the protein matrix is exclusively responsible for both transverse (chlorophylls versus pheophytins) and lateral (D1 versus D2 branch) excitation asymmetry, making Chl D1 the chromophore with the lowest site energy. Multipigment calculations show that the protein matrix renders the Chl D1 → Pheo D1 charge-transfer the lowest energy excitation globally within the reaction center, lower than any pigment-centered local excitation. Remarkably, no low-energy charge transfer states are located within the “special pair” P D1 –P D2 , which is therefore excluded as the site of initial charge separation in PSII. Finally, molecular dynamics simulations suggest that modulation of the electrostatic environment due to protein conformational flexibility enables direct excitation of low-lying charge transfer states by far-red light.

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Protein Matrix Control of Reaction Center Excitation in Photosystem II

2020

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“…2). Many photons are beyond 680 nm, wavelengths that are not used or used far less efficiently by PSII, because the primary donor of PSII (P 680 ) is not formed (Pavlou et al 2018). As a result, red light could cause an imbalance in photosynthetic electron transport.…”

Section: Phycoerythrin Concentrationmentioning

confidence: 99%

Effect of light quality and quantity on productivity and phycoerythrin concentration in the cryptophyte Rhodomonas sp.

et al. 2021

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The cryptophyte Rhodomonas sp. is a potential feed source for aquaculture live feed and resource for phycoerythrin (PE) production. This research investigates the influence of light, both quality and quantity, on the biomass productivity, composition and growth rate of Rhodomonas sp. The incident light intensity used in the experiments was 50 μmolphotons m−2 s−1, irrespective of the colour of the light, and cultivation took place in lab-scale flat-panel photobioreactors in turbidostat mode. The highest productivity in volumetric biomass (0.20 gdry weight L−1 day−1), measured under continuous illumination, was observed under green light conditions. Blue and red light illumination resulted in lower productivities, 0.11 gdry weight L−1 day−1 and 0.02 g L−1 day−1 respectively. The differences in production are ascribed to increased absorption of green and blue wavelength by phycoerythrin, chlorophyll and carotenoids, causing higher photosynthetically usable radiation (PUR) from equal photosynthetically absorbed irradiance (PAR). Moreover, phycoerythrin concentration (281.16 mg gDW−1) was stimulated under red light illumination. Because photosystem II (PSII) absorbs poorly red light, the algae had to induce more pigments in order to negate the lower absorption per unit pigment of the incident available photons. The results of this study indicate that green light can be used in the initial growth of Rhodomonas sp. to produce more biomass and, at a later stage, red light could be implemented to stimulate the synthesis of PE. Fourier-transform infrared spectroscopy (FTIR) analysis demonstrated a significant difference between the cells under different light quality, with higher contents of proteins for samples of Rhodomonas sp. cultivated under green light conditions. In comparison, higher carbohydrate contents were observed for cells that were grown under red and blue light.

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“…One of the two CT pathways may be favored due to the specific conformation of the protein ( 7 ) or the wavelength of incident light ( 8 ). Vibronic coupling between states has been identified ( 9 ), which facilitates switching between the two available pathways ( 10 ) to further assist efficient CS.…”

mentioning

confidence: 99%

A TDDFT investigation of the Photosystem II reaction center: Insights into the precursors to charge separation

Kavanagh

Karlsson

Colburn

et al. 2020

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

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Photosystem II (PS II) captures solar energy and directs charge separation (CS) across the thylakoid membrane during photosynthesis. The highly oxidizing, charge-separated state generated within its reaction center (RC) drives water oxidation. Spectroscopic studies on PS II RCs are difficult to interpret due to large spectral congestion, necessitating modeling to elucidate key spectral features. Herein, we present results from time-dependent density functional theory (TDDFT) calculations on the largest PS II RC model reported to date. This model explicitly includes six RC chromophores and both the chlorin phytol chains and the amino acid residues <6 Å from the pigments’ porphyrin ring centers. Comparing our wild-type model results with calculations on mutant D1-His-198-Ala and D2-His-197-Ala RCs, our simulated absorption-difference spectra reproduce experimentally observed shifts in known chlorophyll absorption bands, demonstrating the predictive capabilities of this model. We find that inclusion of both nearby residues and phytol chains is necessary to reproduce this behavior. Our calculations provide a unique opportunity to observe the molecular orbitals that contribute to the excited states that are precursors to CS. Strikingly, we observe two high oscillator strength, low-lying states, in which molecular orbitals are delocalized over ChlD1 and PheD1 as well as one weaker oscillator strength state with molecular orbitals delocalized over the P chlorophylls. Both these configurations are a match for previously identified exciton–charge transfer states (ChlD1+PheD1−)* and (PD2+PD1−)*. Our results demonstrate the power of TDDFT as a tool, for studies of natural photosynthesis, or indeed future studies of artificial photosynthetic complexes.

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The wavelength of the incident light determines the primary charge separation pathway in Photosystem II

Cited by 14 publications

References 59 publications

Protein Matrix Control of Reaction Center Excitation in Photosystem II

Protein Matrix Control of Reaction Center Excitation in Photosystem II

Effect of light quality and quantity on productivity and phycoerythrin concentration in the cryptophyte Rhodomonas sp.

A TDDFT investigation of the Photosystem II reaction center: Insights into the precursors to charge separation

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