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Electron transfer through the acceptor side of photosystem I: Interaction with exogenous acceptors and molecular oxygen

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Abstract

This review considers the state-of-the-art on mechanisms and alternative pathways of electron transfer in photosynthetic electron transport chains of chloroplasts and cyanobacteria. The mechanisms of electron transport control between photosystems (PS) I and II and the Calvin–Benson cycle are considered. The redistribution of electron fluxes between the noncyclic, cyclic, and pseudocyclic pathways plays an important role in the regulation of photosynthesis. Mathematical modeling of light-induced electron transport processes is considered. Particular attention is given to the electron transfer reactions on the acceptor side of PS I and to interactions of PS I with exogenous acceptors, including molecular oxygen. A kinetic model of PS I and its interaction with exogenous electron acceptors has been developed. This model is based on experimental kinetics of charge recombination in isolated PS I. Kinetic and thermodynamic parameters of the electron transfer reactions in PS I are scrutinized. The free energies of electron transfer between quinone acceptors A1A/A1B in the symmetric redox cofactor branches of PS I and iron–sulfur clusters FX, FA, and FB have been estimated. The second-order rate constants of electron transfer from PS I to external acceptors have been determined. The data suggest that byproduct formation of superoxide radical in PS I due to the reduction of molecular oxygen in the A1 site (Mehler reaction) can exceed 0.3% of the total electron flux in PS I.

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Abbreviations

A0A and A0B:

dimers of chlorophyll a molecules that are primary electron acceptors in cofactor A and B branches

A1A and A1B:

phylloquinone molecules that are secondary electron acceptors in A and B branches

Asc–•:

monodehydroascorbate

AscH–:

ascorbate anion (fully reduced state)

CBC:

Calvin–Benson cycle

Chl, chlorophyll:

Cl2NQ, 2,3-dichloro-1,4-naphthoquinone

DCPIP:

2,6-dichlorophenolindophenol

DMF:

dimethylformamide

E m :

midpoint potential

Fc:

ferrocene

Fc+:

ferrocenium cation

Fd:

ferredoxin

Fld:

flavodoxin

FNR:

ferredoxin:NADP oxidoreductase

FQR:

ferredoxin:quinone reductase

FX, FA, and FB:

iron–sulfur clusters

FX–core:

complexes depleted of iron–sulfur FA/FB clusters

ΔG:

free energy

K m :

Michaelis constant

menB :

mutant strain of Synechocystis sp. PCC 6803 cyanobacterium

MV:

methyl viologen

NDH:

NADH dehydrogenase

O •–2 :

superoxide anion radical

P700:

special pair of chlorophyll a molecules in PS I

Pc:

plastocyanin

PGR5 :

proton gradient regulation protein gene 5 (proton gradient regulation 5)

PGRL1 :

PGR5-like protein 1 gene (PGR5-like protein 1)

PhQ:

phylloquinone

PQ:

plastoquinone

PQH2:

plastoquinol

PS I (II):

photosystem I (II)

PSA:

photosynthetic apparatus

PsaA, PsaB, PsaC, PsaD and PsaE:

subunits within photosystem I

ROS:

reactive oxygen species

SCE:

saturated calomel electrode

SHE:

standard hydrogen electrode

WT:

wild-type Synechocystis sp. PCC 6803 cyanobacterium

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Authors and Affiliations

  1. Lomonosov Moscow State University, Belozersky Institute of Physico-Chemical Biology, 119992, Moscow, Russia

    D. A. Cherepanov, G. E. Milanovsky, A. A. Petrova & A. Yu. Semenov

  2. Semenov Institute of Chemical Physics, Russian Academy of Sciences, 119991, Moscow, Russia

    D. A. Cherepanov

  3. Lomonosov Moscow State University, Faculty of Physics, 119991, Moscow, Russia

    A. N. Tikhonov

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  1. D. A. Cherepanov
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  2. G. E. Milanovsky
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  3. A. A. Petrova
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  4. A. N. Tikhonov
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  5. A. Yu. Semenov
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Correspondence to D. A. Cherepanov, A. N. Tikhonov or A. Yu. Semenov.

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Published in Russian in Biokhimiya, 2017, Vol. 82, No. 11, pp. 1593–1614.

Originally published in Biochemistry (Moscow) On-Line Papers in Press, as Manuscript BM17-296, October 30, 2017.

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Cherepanov, D.A., Milanovsky, G.E., Petrova, A.A. et al. Electron transfer through the acceptor side of photosystem I: Interaction with exogenous acceptors and molecular oxygen. Biochemistry Moscow 82, 1249–1268 (2017). https://doi.org/10.1134/S0006297917110037

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