Inverted-region electron transfer as a mechanism for enhancing photosynthetic solar energy conversion efficiency

Abstract

In all photosynthetic organisms, light energy is used to drive electrons from a donor chlorophyll species via a series of acceptors across a biological membrane. These light-induced electron-transfer processes display a remarkably high quantum efficiency, indicating a near-complete inhibition of unproductive charge recombination reactions. It has been suggested that unproductive charge recombination could be inhibited if the reaction occurs in the so-called inverted region. However, inverted-region electron transfer has never been demonstrated in any native photosynthetic system. Here we demonstrate that the unproductive charge recombination in native photosystem I photosynthetic reaction centers does occur in the inverted region, at both room and cryogenic temperatures. Computational modeling of light-induced electron-transfer processes in photosystem I demonstrate a marked decrease in photosynthetic quantum efficiency, from 98% to below 72%, if the unproductive charge recombination process does not occur in the inverted region. Inverted-region electron transfer is therefore demonstrated to be an important mechanism contributing to efficient solar energy conversion in photosystem I. Inverted-region electron transfer does not appear to be an important mechanism in other photosystems; it is likely because of the highly reducing nature of photosystem I, and the energetic requirements placed on the pigments to operate in such a regime, that the inverted-region electron transfer mechanism becomes important.

Modelling electron transfer in photosystem I: limits and perspectives

“…However, for the recombination reactions, the reorganisation energy had to be lowered to 0.58 eV to adequately describe P 700 + reduction with a lifetime of ∼80 ms. The calculations undertaken by Makita and Hastings (, ) could not be reconciled with λ = 0.4 eV for forward ET processes, in agreement with the conclusions of Santabarbara and Zucchelli (), that λ = 0.5 eV should be considered as a lower limit for this parameter.…”

“…Fig. C shows the results of simulations similar to those undertaken by Makita and Hastings (, ) based on ET rates calculated using Eqn , but considering also an electron drain from F B (Fig. B).…”

“…In the simulations presented here, all the backward ET rates are calculated using the so‐called ‘detailed balance equation’ given by the Boltzmann distribution (Eqn ): which is valid when the high‐temperature approximation holds. However if is sufficiently large, deviations from the classic equilibrium occur (discussion in Makita and Hastings ).…”

“…Calculations were performed employing the ET ruler (Eqn ), including corrections for protein packing density. In estimating ΔG 0 and setting the parameters, the authors also took into account the effect on all the ET reactions (both at RT and 77 K) of the incorporation of eight foreign quinones into the A 1 binding site that modify the system bioenergetics by modulating the reactions driving forces (Makita and Hastings , Makita and Hastings ). The authors focused on reproducing the average reaction lifetime ( τ av ) rather than the specific ones associated with the PsaA and PsaB coordinated quinones.…”

“…D shows the same simulations without the drain allowing P 700 + reduction by recombination reactions. To allow a direct comparison with Eqn , the parameters used by Makita and Hastings (, ) would be equivalent to = 56 meV for all ET reactions and coupling matrix elements, |V 0 | 2 , of ∼0.57 × 10 −3 eV 2 (|V 0 |∼23 meV) at RT. Moreover, the β parameter associated to each ET reaction considered is related to the specific packing densities, which were taken from Moser and Dutton () and corresponds to β in the 1.3–1.4 Å −1 range.…”