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Decoupling of the processes of molecular oxygen synthesis and electron transport in Ca2+-depleted PSII membranes

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Abstract

Extraction of Ca2+ from the O2-evolving complex (OEC) of photosystem II (PSII) membranes with 2 M NaCl in the light (PSII(–Ca/NaCl)) results in 90% inhibition of the O2-evolution reaction. However, electron transfer from the donor to acceptor side of PSII, measured as the reduction of the exogenous acceptor 2,6-dichlorophenolindophenol (DCIP) under continuous light, is inhibited by only 30%. Thus, calcium extraction from the OEC inhibits the synthesis of molecular O2 but not the oxidation of a substrate we term X, the source of electrons for DCIP reduction. The presence of electron transfer across PSII(–Ca/NaCl) membranes was demonstrated using fluorescence induction kinetics, a method that does not require an artificial acceptor. The calcium chelator, EGTA (5 mM), when added to PSII(–Ca/NaCl) membranes, does not affect the inhibition of O2 evolution by NaCl but does inhibit DCIP reduction up to 92% (the reason why electron transport in Ca2+-depleted materials has not been noticed before). Another chelator, sodium citrate (citrate/low pH method of calcium extraction), also inhibits both O2 evolution and DCIP reduction. The role of all buffer components (including bicarbonate and sucrose) as possible sources of electrons for PSII(–Ca/NaCl) membranes was investigated, but only the absence of chloride anions strongly inhibited the rate of DCIP reduction. Substitution of other anions for chloride indicates that Cl− serves its well-known role as an OEC cofactor, but it is not substrate X. Multiple turnover flash experiments have shown a period of four oscillations of the fluorescence yield (both the maximum level, F max, and the fluorescence level measured 50 s after an actinic flash in the presence of DCMU) in native PSII membranes, reflecting the normal function of the OEC, but the absence of oscillations in PSII(–Ca/NaCl) samples. Thus, PSII(–Ca/NaCl) samples do not evolve O2 but do transfer electrons from the donor to acceptor sides and exhibit a disrupted S-state cycle. We explain these results as follows. In Ca2+-depleted PSII membranes, obtained without chelators, the oxidation of the OEC stops after the absorption of three quanta of light (from the S1 state), which should convert the native OEC to the S4 state. An one-electron oxidation of the water molecule bound to the Mn cluster then occurs (the second substrate water molecule is absent due to the absence of calcium), and the OEC returns to the S3 state. The appearance of a sub-cycle within the S-state cycle between S3-like and S4-like states supplies electrons (substrate X is postulated to be OH−), explains the absence of O2 production, and results in the absence of a period of four oscillation of the normal functional parameters, such as the fluorescence yield or the EPR signal from S2. Chloride anions probably keep the redox potential of the Mn cluster low enough for its oxidation by Y •Z .

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Abbreviations

Chl:

Chlorophyll

DCMU:

3-(3,4-Dichlorophenyl)-1,1-dimethylurea

DCIP:

2,6-Dichlorophenolindophenol

EGTA:

Ethylene glycol-bis(β-aminoethyl ether)-N,N,N′,N′-tetraacetic acid

EDTA:

Ethylenediaminetetraacetic acid

F o :

Minimal fluorescence of “open” reaction centers in dark-adapted samples

F max :

Maximum fluorescence yield

FIK:

Fluorescence induction kinetics

FYD:

Pulse-probe fluorescence yield decay kinetics

MES:

2-(N-morpholino)ethanesulfonic acid

OEC:

Oxygen-evolving complex

PSII:

Photosystem II

PSII(–Mn):

Mn-depleted photosystem II

PSII(–Ca/NaCl):

Photosystem II with Ca2+ extracted by treatment with 2 M NaCl

PSII(–Ca/NaCl + 50 μM EGTA):

Photosystem II with Ca2+ extracted by treatment with 2 M NaCl in the presence of 50 μM EGTA

PSII(–Ca/NaCl + 5 mM EGTA):

Photosystem II with Ca2+ extracted by treatment with 2 M NaCl in the presence of 5 mM EGTA

PSII(–Ca/NaCl + 5 mM EGTA→ –EGTA):

Photosystem II with Ca2+ extracted by treatment with 2 M NaCl in the presence of 5 mM EGTA and subsequent washing free of EGTA

PSII(–Ca/pH 3.0):

Photosystem II with Ca2+ extracted by treatment with citrate buffer (pH 3.0)

YZ :

Tyrosine 161 on the D1 protein in spinach, the first electron donor to P680+ in PSII

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Acknowledgments

This study was supported by the Russian Foundation for Basic Research, Project Numbers 08-04-00490a (BS, LD) and 08-04-00354 (AR), and by the Office of Basic Energy Sciences, Office of Science, U.S. Department of Energy (MS). BKS appreciates support from the Division of Energy Biosciences, Office of Science, U.S. Department of Energy while at NREL. We thank Professor R. Debus for many helpful suggestions.

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  1. Department of Biophysics, Faculty of Biology, Lomonosov Moscow State University, 119991, Moscow, Russia

    Boris K. Semin, Lira N. Davletshina, Il’ya I. Ivanov & Andrei B. Rubin

  2. Chemical and Biosciences Center, National Renewable Energy Laboratory, Golden, CO, 80401, USA

    Boris K. Semin & Michael Seibert

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  1. Boris K. Semin
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  2. Lira N. Davletshina
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Correspondence to Michael Seibert.

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Semin, B.K., Davletshina, L.N., Ivanov, I.I. et al. Decoupling of the processes of molecular oxygen synthesis and electron transport in Ca2+-depleted PSII membranes. Photosynth Res 98, 235–249 (2008). https://doi.org/10.1007/s11120-008-9347-5

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