A variant of the MenB strain of Synechocystis sp. PCC 6803 disrupts a stress response pathway allowing DMPBQ to occupy the A₁ sites of photosystem I

Phylloquinone (PhQ) plays a unique role in photosynthesis as the A_1A and A_1B intermediates in light-driven electron transfer in Photosystem I (PSI). When PhQ biosynthesis is inhibited by deletion of the menB gene in the cyanobacterium Synechocystis sp. PCC 6803, previous studies have shown that plastoquinone-9 (PQ-9) occupies the A₁ sites. However, a recent cryo-electron microscopy structure of a strain of ΔmenB from the year 2023 revealed an unusual quinone in the A₁ sites with a benzoquinone headgroup similar to PQ-9 and a phytyl tail similar to PhQ. Here, we investigate its biosynthesis and binding properties. Mass spectrometry confirms that PSI from the 2023 ΔmenB strain contains 2,3-dimethyl-5-phytyl-1,4-benzoquinone (DMPBQ), while PSI from the original strain contains PQ-9. Whole genome sequencing reveals that a mutation in slr1737 (tocopherol cyclase) leads to the accumulation of DMPBQ, an intermediate in the tocopherol biosynthetic pathway. Transient optical and electron paramagnetic resonance spectroscopy studies show that when DMPBQ occupies the A₁ sites, it does not exchange with exogenously supplied PhQ, in contrast to PQ-9, which exchanges readily. We propose that the slr1737 mutation in the 2023 ΔmenB strain is a likely candidate for the source of the phenotype. This new strain has sacrificed tocopherol synthesis, the absence of which is known not to affect growth under low stress conditions, resulting in the incorporation of DMPBQ in the A₁ sites. The tighter binding and function of DMPBQ likely allow this ΔmenB strain to outcompete its peers under optimal growth conditions and thus dominate the population.