Kinetics and Energetics of Phylloquinone Reduction in Photosystem I: Insight From Modeling of the Site Directed Mutants

Abstract

Two phylloquinone molecules (A ₁), one being predominantly coordinated by PsaA subunit residues (A _1A) the other by those of PsaB (A _1B), act as intermediates in the two parallel electron transfer chains of Photosystem I. The oxidation kinetics of the two phyllosemiquinones by the iron-sulfur cluster F_X differ by approximately one order of magnitude, with $A_{1\text{A}}^{-}$ being oxidized in about 200 ns and $A_{1\text{B}}^{-}$ in about 20 ns. These differences are generally explained in terms of asymmetries in the driving force for F_X reduction on the two electron transfer chains. Site directed mutations of conserved amino acids composing the A ₁ binding site have been engineered on both reaction center subunits, and proved to affect selectively the oxidation lifetime of either $A_{1\text{A}}^{-}$ , for PsaA mutants, or $A_{1\text{B}}^{-}$ , for PsaB mutants. The mutation effects are here critically reviewed, also by novel modeling simulations employing the tunneling formalism to estimate the electron transfer rates. Three main classes of mutation effects are in particular addressed: (i) those leading to an acceleration, (ii) those leading to a moderated slowing (~5-folds), and (iii) those leading to a severe slowing (>20-folds) of the kinetics. The effect of specific amino acid perturbations contributing to the poising of the phylloquinones redox potential and, in turn, to PSI functionality, is discussed.

Keywords: bioenergetics; electron transfer; kinetic modeling; photosystem I; phylloquinone; redox tuning.