Enhanced carotenoid photoprotection in Far-Red light acclimated Chroococcidiopsis thermalis

Oxygenic photosynthesis is mainly driven by visible light in most photosynthetic organisms. However, some cyanobacteria strains can reversibly remodel their photosynthetic apparatus in order to rely exclusively on far-red photons. This acclimation, known as FaRLiP, requires the synthesis of red-shifted pigments, chlorophyll d , chlorophyll f and far-red allophycocyanin, that are incorporated in paralog subunits of the main photosynthetic complexes, namely photosystem II and photosystem I as well as phycobilisomes. In addition, some far-red–acclimating strains were also observed to show a rise in the carotenoid content and in the expression of genes involved in the biosynthesis of UV-shielding molecules, suggesting a counterintuitive photoprotective response concomitant with acclimation to lower energy wavelengths. In this work we investigated the response of Chroococcidiopsis thermalis to far-red light, and identified a robust set of photoprotective mechanisms associated with acclimation. Enhanced carotenoid/chlorophyll content ratios correlated with stronger carotenoid–chlorophyll triplet quenching, particularly pronounced for red-shifted chlorophylls. Non-photochemical quenching was higher and activated more rapidly than in cells grown under simulated solar light, and this was accompanied by enhanced antioxidant activity. Collectively, these findings indicate that the far-red acclimated cells, whose photosynthetic apparatus is not optimal under visible light, exhibit a strong photoprotected state, that we propose to be crucial under fluctuating irradiance conditions and during transitions from shaded to non-shaded environments. Highlights Far-red light photoacclimation (FaRLiP) in Chroococcidiopsis thermalis is associated with an increased carotenoid-to-chlorophyll ratio. The relative abundance of myxol-2’ fucoside, echinenone and β-carotene increased in cells acclimated to far-red light compared with cells acclimated to simulated solar irradiation. Upon establishment of FaRLiP an exceptionally strong chlorophyll triplet quenching by carotenoids was observed, and it was specifically involving red-shifted chlorophylls. When exposed to the same light treatment, non-photochemical quenching was higher in far-red-acclimated cells than in solar-acclimated. Moreover, following high visible-light stress, far-red-acclimated cells exhibited lower levels of reactive oxygen species. The FaRLiP photosynthetic apparatus is safeguarded by robust mechanisms of photoprotection.