Critical evaluation of electron transfer kinetics in P700–FA/FB, P700–FX, and P700–A1 Photosystem I core complexes in liquid and in trehalose glass

This work aims to fully elucidate the effects of a trehalose glassy matrix on electron transfer reactions in cyanobacterial Photosystem I (PS I). Forward and backward electron transfer rates from A1A− and A1B− to FX, and charge recombination rates from A0−, A1B−, A1A−, FX−, and [FA/FB]− to P700+ were measured in P700–FA/FB complexes, P700–FX cores, and P700–A1 cores, both in liquid and in a trehalose glassy matrix at 11% humidity. By comparing CONTIN-resolved kinetic events over 6 orders of time in increasingly simplified versions of PS I at 480 nm, a wavelength that reports primarily A1A−/A1B− oxidation, and over 9 orders of time at 830 nm, a wavelength that reports P700+ reduction and A0− oxidation, assignments could be made for nearly all of the resolved kinetic phases. Trehalose-embedded PS I samples demonstrated partially arrested forward electron transfer. The fractions of complexes in which electron transfer did not proceed beyond A0, A1 and FX were 53%, 16% and 22%, respectively, with only 10% of electrons reaching the terminal FA/FB clusters. The ~10 μs and ~150 μs components in both liquid and trehalose-embedded PS I were assigned to recombination between A1B− and P700+ and between A1A− and P700+, respectively. The kinetics and amplitudes of these resolved kinetic phases in liquid and trehalose-embedded PS I samples could be well-fitted by a kinetic model that allowed us to calculate the asymmetrical contribution of the A1A− and A1B− quinones to the electrochromic signal at 480 nm. Possible reasons for these effects are discussed. •Photosystem I embedded in trehalose glass demonstrates arrested electron transfer.•Forward rates from the A1A−/A1B− quinones to FX are slower than in liquid medium.•Recombination rates from the A1A−/A1B− quinones to P700+ are similar to liquid medium.•Recombination from FX− to P700+ is heterogeneous and splits into several components.•The kinetics and amplitudes of the reactions can be well-fitted by a kinetic model.