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Characterization of fluorescent chlorophyll charge-transfer states as intermediates in the excited state quenching of light-harvesting complex II

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Abstract

Light-harvesting complex II (LHCII) is the major antenna complex in higher plants and green algae. It has been suggested that a major part of the excited state energy dissipation in the so-called “non-photochemical quenching” (NPQ) is located in this antenna complex. We have performed an ultrafast kinetics study of the low-energy fluorescent states related to quenching in LHCII in both aggregated and the crystalline form. In both sample types the chlorophyll (Chl) excited states of LHCII are strongly quenched in a similar fashion. Quenching is accompanied by the appearance of new far-red (FR) fluorescence bands from energetically low-lying Chl excited states. The kinetics of quenching, its temperature dependence down to 4 K, and the properties of the FR-emitting states are very similar both in LHCII aggregates and in the crystal. No such FR-emitting states are found in unquenched trimeric LHCII. We conclude that these states represent weakly emitting Chl–Chl charge-transfer (CT) states, whose formation is part of the quenching process. Quantum chemical calculations of the lowest energy exciton and CT states, explicitly including the coupling to the specific protein environment, provide detailed insight into the chemical nature of the CT states and the mechanism of CT quenching. The experimental data combined with the results of the calculations strongly suggest that the quenching mechanism consists of a sequence of two proton-coupled electron transfer steps involving the three quenching center Chls 610/611/612. The FR-emitting CT states are reaction intermediates in this sequence. The polarity-controlled internal reprotonation of the E175/K179 aa pair is suggested as the switch controlling quenching. A unified model is proposed that is able to explain all known conditions of quenching or non-quenching of LHCII, depending on the environment without invoking any major conformational changes of the protein.

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Notes

  1. The crystal structure of LHCII (Standfuss et al. 2005) as deposited in file ID 2BHW in the protein database has been used as structural basis.

  2. We note here that the three-state model used by Chmeliov et al. (two fluorescing components, plus one non-fluorescent “dark state”) (Chmeliov et al. 2016) is kinetically indistinguishable in fluorescence data from a simpler two-state model with two fluorescent components since presence or absence of the “dark state” has no influence on the fluorescence kinetics. The proposal of the “dark state” in the kinetic model is thus an unproven assumption lacking experimental evidence.

  3. Due to the pronounced CT state relaxation at higher temperatures this system does not show the temperature dependence of reaction rates expected for a normal Boltzmann equilibrium.

  4. The authors (Gelzinis et al. 2018) claim that they have tested our Chl–Chl CT state kinetic model (Miloslavina et al. 2008; Müller et al. 2010) and found it to be inconsistent with their fluorescence kinetic data on LHCII aggregates. We note that their interpretation is a gross misinterpretation of our CT state model, since they modeled an energy transfer process as populating the “red state”. In contrast in our Chl–Chl CT state kinetic model an electron transfer process from the excited LHCII state to the Chl–Chl CT state, residing in the same LHCII monomer as the formed CT state, populates the “red state”. state. Thus the interpretation used in their modeling (Chmeliov et al. 2016; Gelzinis et al. 2019) has no resemblance to and deviates fundamentally from our proposed kinetic model.

Abbreviations

LHCII:

Major light-harvesting complex of photosystem II

PSII:

Photosystem II

RC:

Reaction center

Chl:

Chlorophyll

Car:

Carotenoid

Lut:

Lutein

Vx:

Violaxanthin

Zx:

Zeaxanthin

Nx:

Neoxanthin

DAES:

Decay-associated emission spectrum

r.t:

Room temperature

NPQ:

Non-photochemical quenching

qE:

Energy-dependent quenching

CT (state):

Charge-transfer (state)

RP:

Radical pair

FR:

Far-red

HL:

High light

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Acknowledgements

This research was supported by grants to ARH from the Deutsche Forschungsgemeinschaft (DFG HO-924/3–1 and in part by SFB 663), and by the EU Training and Research Network “Harvest” of the European Union. PHL acknowledges support from the Hungarian National Research, Development and Innovation Fund (grants NN 124904, 2018–1.2.1-NKP-2018–00009). JPG is currently funded by the DFG, project no. 393271229. We thank Prof. W. Kühlbrandt and Dr. Tiago Barros (Max-Planck-Institute for Biophysics, Frankfurt a. Main, Germany) for providing the LHCII crystals. We also thank the Max-Planck-Institute for Chemical Energy Conversion for generous support.

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  1. Max-Planck-Institut für Chemische Energiekonversion, Stiftstrasse 34-36, 45470, Mülheim a. d. Ruhr, Germany

    Evgeny E. Ostroumov, Jan P. Götze, Michael Reus & Alfred R. Holzwarth

  2. Biological Research Centre, Temesvári krt. 62, Szeged, 6726, Hungary

    Petar H. Lambrev

  3. Quantum Matter Institute, University of British Columbia, 2355 East Mall, Vancouver, V6T 1Z1, Canada

    Evgeny E. Ostroumov

  4. Institut für Chemie und Biochemie, Freie Universität Berlin, Arnimallee 22, 14195, Berlin, Germany

    Jan P. Götze

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Ostroumov, E.E., Götze, J.P., Reus, M. et al. Characterization of fluorescent chlorophyll charge-transfer states as intermediates in the excited state quenching of light-harvesting complex II. Photosynth Res 144, 171–193 (2020). https://doi.org/10.1007/s11120-020-00745-8

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