Response of the thylakoid proteome of Synechocystis sp. PCC 6803 to photohinibitory intensities of orange-red light

Photoautotrophic growth of Synechocystis sp. PCC 6803 in a flat-panel photobioreactor, run in turbidostat mode under increasing intensities of orange-red light (636 nm), showed a maximal growth rate (0.12 h⁻¹) at 300 μmol_photons m⁻² s⁻¹, whereas first signs of photoinhibition were detected above 800 μmol_photons m⁻² s⁻¹. To investigate the dynamic modulation of the thylakoid proteome in response to photoinhibitory light intensities, quantitative proteomics analyses by SWATH mass spectrometry were performed by comparing thylakoid membranes extracted from Synechocystis grown under low-intensity illumination (i.e. 50 μmol_photons m⁻² s⁻¹) with samples isolated from cells subjected to photoinhibitory light regimes (800, 950 and 1460 μmol_photons m⁻² s⁻¹). We identified and quantified 126 proteins with altered abundance in all three photoinhibitory illumination regimes. These data reveal the strategies by which Synechocystis responds to photoinibitory growth irradiances of orange-red light. The accumulation of core proteins of Photosystem II and reduction of oxygen-evolving-complex subunits in photoinhibited cells revealed a different turnover and repair rates of the integral and extrinsic Photosystem II subunits with variation of light intensity. Furthermore, Synechocystis displayed a differentiated response to photoinhibitory regimes also regarding Photosystem I: the amount of PsaD, PsaE, PsaJ and PsaM subunits decreased, while there was an increased abundance of the PsaA, PsaB, Psak2 and PsaL proteins. Photoinhibition with 636 nm light also elicited an increased capacity for cyclic electron transport, a lowering of the amount of phycobilisomes and an increase of the orange carotenoid protein content, all presumably as a photoprotective mechanism against the generation of reactive oxygen species.