BPS2026 – A variant of the menB strain of Synechocystis sp. PCC 6803 disrupts a stress response pathway, incorporating an unusual quinone in the electron transfer pathway 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 showed that plastoquinone-9 (PQ-9) occupies the A 1 sites. However, a recent cryo-electron microscopy structure of PSI from a Δ menB strain from the year 2023 revealed an unusual quinone in the A 1 sites with a benzoquinone headgroup similar to PQ-9 and a phytyl tail similar to PhQ. Mass spectrometry confirms that PSI from the 2023 Δ menB strain contains 2,3-dimethyl-5-phytyl-1,4-benzoquinone (DMPBQ). Whole genome sequencing reveals that this difference is the result of a mutation in slr1737 (tocopherol cyclase) that leads to the accumulation of DMPBQ, an intermediate in the tocopherol biosynthetic pathway. Time-resolved optical and EPR spectroscopy studies show that when DMPBQ occupies the A 1A and A 1B 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 Δ menB strain is the source of the phenotype. This new strain has sacrificed a stress response pathway under low stress laboratory growth conditions, resulting in the incorporation of DMPBQ in the A 1A and A 1B sites. The tighter quinone binding and function of DMPBQ allow this Δ menB strain to outcompete its peers under optimal growth conditions. ∗ This work is supported by the U.S. DOE, Photosynthetic Systems Program under the contract DE-FG02-07ER15903 (KVL), DE-SC0010575 (JHG), DE-SC0025359 (DJV), NSF GRFP (PL) and Discovery Grant No. 2015-04021 from the NSERC (AvdE).