Multiple pathways of charge recombination revealed by the temperature dependence of electron transfer kinetics in cyanobacterial photosystem I

Georgy Milanovsky, Oksana Gopta, Anastasia Petrova, M. Mamedov, Michael Gorka, Dmitry Cherepanov, John H. Golbeck, Alexey Semenov

Research output: Contribution to journalArticle

Abstract

The kinetics of charge recombination in Photosystem I P700-FA/FB complexes and P700-FX cores lacking the terminal iron‑sulfur clusters were studied over a temperatures range of 310 K to 4.2 K. Analysis of the charge recombination kinetics in this temperature range allowed the assignment of backward electron transfer from the different electron acceptors to P700 +. The kinetic and thermodynamic parameters of these recombination reactions were determined. The kinetics of all electron transfer reactions were activation-less below 170 K, the glass transition temperature of the water-glycerol solution. Above this temperature, recombination from [FA/FB] in P700-FA/FB complexes was found to proceed along two pathways with different activation energies (Ea). The charge recombination via A1A has an Ea of ~290 meV and is dominant at temperatures above ~280 K, whereas the direct recombination from FX has an Ea of 22 meV and is prevalent in the 200 K to 270 K temperature range. Charge recombination from the FX cluster becomes highly heterogeneous at temperatures below 200 K. The conformational mobility of Photosystem I was studied by molecular dynamics simulations. The FX cluster was found to ‘swing’ by ~30° along the axis between the two sulfur atoms proximal to FA/FB. The partial rotation of FX is accompanied by significant changes of electric potential within the iron‑sulfur cluster, which may induce preferential electron localization at different atoms of the FX cluster. These effects may account for the partial arrest of forward electron transfer and for the heterogeneity of charge recombination observed at the glass transition temperature.

Original languageEnglish (US)
Pages (from-to)601-610
Number of pages10
JournalBiochimica et Biophysica Acta - Bioenergetics
Volume1860
Issue number8
DOIs
StatePublished - Aug 1 2019

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Photosystem I Protein Complex
Genetic Recombination
Electrons
Kinetics
Temperature
Transition Temperature
Glass
Atoms
Sulfur
Glycerol
Molecular dynamics
Molecular Dynamics Simulation
Activation energy
Chemical activation
Thermodynamics
Water
Computer simulation
Electric potential

All Science Journal Classification (ASJC) codes

  • Biophysics
  • Biochemistry
  • Cell Biology

Cite this

Milanovsky, Georgy ; Gopta, Oksana ; Petrova, Anastasia ; Mamedov, M. ; Gorka, Michael ; Cherepanov, Dmitry ; Golbeck, John H. ; Semenov, Alexey. / Multiple pathways of charge recombination revealed by the temperature dependence of electron transfer kinetics in cyanobacterial photosystem I. In: Biochimica et Biophysica Acta - Bioenergetics. 2019 ; Vol. 1860, No. 8. pp. 601-610.
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abstract = "The kinetics of charge recombination in Photosystem I P700-FA/FB complexes and P700-FX cores lacking the terminal iron‑sulfur clusters were studied over a temperatures range of 310 K to 4.2 K. Analysis of the charge recombination kinetics in this temperature range allowed the assignment of backward electron transfer from the different electron acceptors to P700 +. The kinetic and thermodynamic parameters of these recombination reactions were determined. The kinetics of all electron transfer reactions were activation-less below 170 K, the glass transition temperature of the water-glycerol solution. Above this temperature, recombination from [FA/FB]− in P700-FA/FB complexes was found to proceed along two pathways with different activation energies (Ea). The charge recombination via A1A has an Ea of ~290 meV and is dominant at temperatures above ~280 K, whereas the direct recombination from FX − has an Ea of 22 meV and is prevalent in the 200 K to 270 K temperature range. Charge recombination from the FX cluster becomes highly heterogeneous at temperatures below 200 K. The conformational mobility of Photosystem I was studied by molecular dynamics simulations. The FX cluster was found to ‘swing’ by ~30° along the axis between the two sulfur atoms proximal to FA/FB. The partial rotation of FX is accompanied by significant changes of electric potential within the iron‑sulfur cluster, which may induce preferential electron localization at different atoms of the FX cluster. These effects may account for the partial arrest of forward electron transfer and for the heterogeneity of charge recombination observed at the glass transition temperature.",
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Multiple pathways of charge recombination revealed by the temperature dependence of electron transfer kinetics in cyanobacterial photosystem I. / Milanovsky, Georgy; Gopta, Oksana; Petrova, Anastasia; Mamedov, M.; Gorka, Michael; Cherepanov, Dmitry; Golbeck, John H.; Semenov, Alexey.

In: Biochimica et Biophysica Acta - Bioenergetics, Vol. 1860, No. 8, 01.08.2019, p. 601-610.

Research output: Contribution to journalArticle

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T1 - Multiple pathways of charge recombination revealed by the temperature dependence of electron transfer kinetics in cyanobacterial photosystem I

AU - Milanovsky, Georgy

AU - Gopta, Oksana

AU - Petrova, Anastasia

AU - Mamedov, M.

AU - Gorka, Michael

AU - Cherepanov, Dmitry

AU - Golbeck, John H.

AU - Semenov, Alexey

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