Thermodynamic Factors Controlling Electron Transfer among the Terminal Electron Acceptors of Photosystem I: Insights from Kinetic Modelling
Abstract
:1. Introduction
2. Results and Discussion
2.1. “Weak Driving Force” Scenario for Oxidation
2.2. “Large Driving Force” Scenario for Oxidation
2.3. Effect of Changing the Driving Force of Oxidation ()
2.4. Effect of Changing the Driving Force of Oxidation ()
3. Materials and Methods
3.1. Electron Transfer Dynamics Simulations
3.2. Electron Transfer Rates Description
3.3. Average and Mean Lifetimes
4. Conclusions
- (i).
- Tuning the redox potential, together with an alteration of the ET kinetics directly involving this redox centre, also affects the phyllosemiquinone oxidation kinetics, particularly the slow kinetic phase of this process that is dominated by the depopulation of . Significant kinetic perturbations are predicted within the “weak driving force” scenario for oxidation by . Tuning has instead a limited effect on oxidation kinetics when considering the “large driving force” energetic scheme for these cofactors’ oxidation reactions. Since both energetic schemes describe adequately several measured parameters, they can both be considered realistic. A more in-depth analysis of mutants affecting coordination in the PsaC subunit, some of which have already been reported (e.g., refs. [78,79,80,81,82,83,84]) but not studied with sufficient (ns) temporal resolution, is expected to shed further light on the energy gap between and , especially since the redox potential of the modified cofactor shall be accessible by direct electrochemistry and henceforth correlated to the kinetic perturbation. Similar approaches have already been explored and proven feasible (e.g., refs. [78,79,80]). However, as already discussed, the effect of the mutations on the kinetics of forward ET reactions has not been investigated in detail yet.
- (ii).
- Tuning the redox potential is predicted to affect almost exclusively ET involving the iron–sulphur clusters instead, especially the oxidation kinetics of and , without significantly impacting on the oxidation kinetics, regardless of the energetic scenario employed to describe the latter reaction.
- (iii).
- Alterations of the redox potential, which have also been reported for mutants affecting its coordination site in the PsaC subunit (e.g., refs. [76,77,78,79,80,81,82,83,84,85,86,87]), can, however, help in elucidating the actual energetics of ET between the terminal iron–sulphur clusters, which might be inferred from differences in both the recombination rates and forward ET to ferredoxin, in comparison with a similar perturbation of the redox potential.
- (iv).
- The ~180 ns kinetic phase experimentally retrieved in investigations of oxidation kinetics [30,33,34,62,63] appears to be associated principally with oxidation by , whereas it was previously assigned to oxidation by [30]. The ~180 ns lifetime appears to be a significant contribution also in the oxidation kinetics, indicating that oxidation by is not fully kinetically decoupled from upstream reactions. This lifetime is correctly predicted in the “weak driving force” oxidation scenario, whereas a slight overestimation (~300 ns) is obtained in the “large driving force” energetic scheme.
- (v).
- The need to consider ~ 1 eV in the “large driving force” oxidation scenario led to simulating a relatively slow oxidation, which couples to a small-amplitude oxidation phase in the μs windows. This phase has not been detected experimentally either because it is not present or not resolvable. Multiple pieces of evidence suggest that oxidation shall proceed in the sub-μs scale. This can be taken as an indication that ~ 1 eV represents an upper limit/overestimation of this parameter. The calculated recombination rates, which are limited by the back-population of , argue in the same direction, as they are overestimated, in general, by about an order of magnitude within the “large driving force” scenario (see Sections S2 and S3 of the Supplementary Materials for further discussion and simulations).
- (vi).
- Uphill ET from to can significantly slow down donation from the terminal electron acceptor(s) to diffusible carriers, at least when pre-bound complexes are formed, i.e., the speed of electron transfer to ferredoxin (or other acceptors) might not depend solely on the rate of transfer from to the redox-active centre in the acceptor molecules, particularly if the intrinsic rate constant for this reaction is as fast as, or comparable with, the electron transfer kinetics involving the terminal electron acceptors within the photosystem.
Supplementary Materials
Author Contributions
Funding
Data Availability Statement
Conflicts of Interest
References
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Rate Determining Parameters | Electron Transfer Simulated Parameters | ||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Reaction | (Å) | (eV) | (eV) | (eV/ cm−1) | (ns−1) | (ns) | Amplitudes | ||||||
9.1 | 0.01 | 0.700 | 0.022 (175) | 0.0181 | 5.26 | 0.0754 | 0.382 | −0.489 | 0.033 | 0.000 | 0.457 | −0.457 | |
9.0 | −0.05 | 0.700 | 0.046 (375) | 0.145 | 22.5 | −0.173 | 0.051 | 0.172 | −0.051 | 0.003 | −0.123 | 0.123 | |
11.6 | −0.15 | 0.700 | 0.034 (275) | 0.0126 | 136 | 0.0035 | 0.000 | 0.001 | −0.295 | 0.336 | 0.004 | 0.042 | |
9.5 | 0.025 | 0.900 | 0.034 (275) | 0.0019 | 243 | 0.587 | 0.067 | 0.312 | −0.489 | −0.628 | 0.654 | −0.806 | |
– | – | – | – | 0.00100 | 3808 | 0.0068 | 0.001 | 0.005 | 0.803 | 0.290 | 0.008 | 1.098 |
Rate Determining Parameters | Electron Transfer Simulated Parameters | ||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Reaction | (Å) | (eV) | (eV) | (eV/ cm−1) | (ns−1) | (ns) | Amplitudes | ||||||
9.1 | −0.05 | 1.0 | 0.022 (175) | 0.00270 | 8.15 | 0.002 | 0.500 | −0.504 | 0.0035 | 0.0000 | 0.501 | −0.501 | |
9.0 | −0.22 | 1.0 | 0.046 (375) | 0.12249 | 294.7 | 0.0020 | 0.000 | −0.003 | 0.3891 | −0.550 | 0.002 | −0.164 | |
11.6 | −0.15 | 1.0 | 0.034 (275) | 0.00085 | 307.3 | 0.307 | 0.000 | −0.414 | −0.343 | 0.650 | 0.307 | −0.107 | |
9.5 | 0.025 | 1.0 | 0.034 (275) | 0.00077 | 1411 | 0.187 | 0.001 | 0.912 | −1.292 | −0.468 | 0.188 | −0.847 | |
– | – | – | – | 0.00100 | 4415 | 0.002 | 0.000 | 0.001 | 1.242 | 0.367 | 0.002 | 1.619 |
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Santabarbara, S.; Casazza, A.P. Thermodynamic Factors Controlling Electron Transfer among the Terminal Electron Acceptors of Photosystem I: Insights from Kinetic Modelling. Int. J. Mol. Sci. 2024, 25, 9795. https://doi.org/10.3390/ijms25189795
Santabarbara S, Casazza AP. Thermodynamic Factors Controlling Electron Transfer among the Terminal Electron Acceptors of Photosystem I: Insights from Kinetic Modelling. International Journal of Molecular Sciences. 2024; 25(18):9795. https://doi.org/10.3390/ijms25189795
Chicago/Turabian StyleSantabarbara, Stefano, and Anna Paola Casazza. 2024. "Thermodynamic Factors Controlling Electron Transfer among the Terminal Electron Acceptors of Photosystem I: Insights from Kinetic Modelling" International Journal of Molecular Sciences 25, no. 18: 9795. https://doi.org/10.3390/ijms25189795