Effect of Dehydrated Trehalose Matrix on the Kinetics of Forward Electron Transfer Reactions in Photosystem I

Ivan Shelaev; Michael Gorka; Anton Savitsky; Vasily Kurashov; Mahir Mamedov; Fedor Gostev; Klaus Möbius; Victor Nadtochenko; John Golbeck; Alexey Semenov

doi:10.1515/zpch-2016-0860

Published by De Gruyter (O) November 3, 2016

Effect of Dehydrated Trehalose Matrix on the Kinetics of Forward Electron Transfer Reactions in Photosystem I

Ivan Shelaev , Michael Gorka , Anton Savitsky , Vasily Kurashov , Mahir Mamedov , Fedor Gostev , Klaus Möbius , Victor Nadtochenko , John Golbeck and Alexey Semenov

From the journal Zeitschrift für Physikalische Chemie

https://doi.org/10.1515/zpch-2016-0860

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Abstract

The effect of dehydration on the kinetics of forward electron transfer (ET) has been studied in cyanobacterial photosystem I (PS I) complexes in a trehalose glassy matrix by time-resolved optical and EPR spectroscopies in the 100 fs to 1 ms time domain. The kinetics of the flash-induced absorption changes in the subnanosecond time domain due to primary and secondary charge separation steps were monitored by pump–probe laser spectroscopy with 20-fs low-energy pump pulses centered at 720 nm. The back-reaction kinetics of P₇₀₀ were measured by high-field time-resolved EPR spectroscopy and the forward kinetics of A1A•−/A1B•−→FX by time-resolved optical spectroscopy at 480 nm. The kinetics of the primary ET reactions to form the primary P700•+A0•− and the secondary P700•+A1•− ion radical pairs were not affected by dehydration in the trehalose matrix, while the yield of the P700•+A1•− was decreased by ~20%. Forward ET from the phylloquinone molecules in the A1A•− and A1B•− sites to the iron–sulfur cluster F_X slowed from ~220 ns and ~20 ns in solution to ~13 μs and ~80 ns, respectively. However, as shown by EPR spectroscopy, the ~15 μs kinetic phase also contains a small contribution from the recombination between A1B•− and P700•+. These data reveal that the initial ET reactions from P₇₀₀ to secondary phylloquinone acceptors in the A- and B-branches of cofactors (A_1A and A_1B) remain unaffected whereas ET beyond A_1A and A_1B is slowed or prevented by constrained protein dynamics due to the dry trehalose glass matrix.

Keywords: electron transfer; EPR; optical spectroscopy; photosystem I; trehalose matrix

Dedicated to: Kev Salikhov on the occasion of his 80th birthday.

Funding source: Russian Foundation for Basic Research

Award Identifier / Grant number: 15-04-04252

Funding source: Russian Science Foundation

Award Identifier / Grant number: 14-14-00789

Funding statement: This work was financially supported by the Russian Foundation for Basic Research, grant 15-04-04252 (to A.Yu.S.) and Russian Science Foundation, grant 14-14-00789 (to A.Yu.S. and V.N.), by the President of RF grant MK-6515.2015.4 (to I.S.), by the US National Science Foundation, grant MCB-1613022 (to J.G.) and by the Cluster of Excellence RESOLV (EXC 1069) funded by the Deutsche Forschungsgemeinschaft (to A.S.) and the Max Planck Society (to A.S. and K.M.). K.M. acknowledges sustaining support by the Free University of Berlin. We want to thank Giovanni Venturoli (University of Bologna) for stimulating and fruitful discussions, Dmitry Cherepanov and Georgy Milanovsky for their assistance in application of CONTIN software, and Anastasia Petrova for preparation of PS I complexes (all Moscow State University).

Acknowledgments

This work was financially supported by the Russian Foundation for Basic Research, grant 15-04-04252 (to A.Yu.S.) and Russian Science Foundation, grant 14-14-00789 (to A.Yu.S. and V.N.), by the President of RF grant MK-6515.2015.4 (to I.S.), by the US National Science Foundation, grant MCB-1613022 (to J.G.) and by the Cluster of Excellence RESOLV (EXC 1069) funded by the Deutsche Forschungsgemeinschaft (to A.S.) and the Max Planck Society (to A.S. and K.M.). K.M. acknowledges sustaining support by the Free University of Berlin. We want to thank Giovanni Venturoli (University of Bologna) for stimulating and fruitful discussions, Dmitry Cherepanov and Georgy Milanovsky for their assistance in application of CONTIN software, and Anastasia Petrova for preparation of PS I complexes (all Moscow State University).

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Received: 2016-7-18

Accepted: 2016-10-5

Published Online: 2016-11-3

Published in Print: 2017-2-1

Effect of Dehydrated Trehalose Matrix on the Kinetics of Forward Electron Transfer Reactions in Photosystem I

Abstract

Acknowledgments

References

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