Redesigning the QA binding site of Photosystem II allows reduction of exogenous quinones

Han-Yi Fu,Manon Guille-Collignon,Fabrice Rappaport,Francis-André Wollman,Frédéric Lemaître,Daniel Picot,Adnan Sayegh,Jérôme Delacotte,Guillaume Longatte,Yves Choquet

doi:10.1038/ncomms15274

Abstract

Strategies to harness photosynthesis from living organisms to generate electrical power have long been considered, yet efficiency remains low. Here, we aimed to reroute photosynthetic electron flow in photosynthetic organisms without compromising their phototrophic properties. We show that 2,6-dimethyl-p-benzoquinone (DMBQ) can be used as an electron mediator to assess the efficiency of mutations designed to engineer a novel electron donation pathway downstream of the primary electron acceptor QA of Photosystem (PS) II in the green alga Chlamydomonas reinhardtii. Through the use of structural prediction studies and a screen of site-directed PSII mutants we show that modifying the environment of the QA site increases the reduction rate of DMBQ. Truncating the C-terminus of the PsbT subunit protruding in the stroma provides evidence that shortening the distance between QA and DMBQ leads to sustained electron transfer to DMBQ, as confirmed by chronoamperometry, consistent with a bypass of the natural QA°− to QB pathway.

Highlights

Strategies to harness photosynthesis from living organisms to generate electrical power have long been considered, yet efficiency remains low
To assess the relative efficiency of various quinones to accept electrons from PSII, we used a mutant strain of C. reinhardtii lacking cytochrome b6f (DpetA), a protein complex which acts as a quinol:plastocyanin oxidoreductase
The ability of exogenous quinones to accept electron from PSII, that is, to restore the electron flow downstream of PSII, is witnessed by a decrease in the steady-state fluorescence level reached under continuous illumination with sub-saturating light

Summary

Introduction

Strategies to harness photosynthesis from living organisms to generate electrical power have long been considered, yet efficiency remains low. Extracting electrons from these photosystems to generate a photocurrent requires the establishment of sustained flux that will be determined by the intrinsic rate constant of light-independent reactions. These kinetic limitations are such that the yield of biophotovoltaics is still far lower than the theoretical limit of conversion efficiency[2]. To circumvent these limitations, attempts were made to optimize the electrical connectivity between isolated photosystems and the electrode that eventually collects the reducing equivalents they produce under illumination.

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