Abstract

Oxygenic phototrophs have evolved a remarkable plethora of strategies to react to changes in light intensity and spectral range, which allows them to thrive in a wide range of environmental conditions. Varying light quality and quantity influences the balance between solar energy capture and utilisation in photosynthesis, affecting concomitantly the downstream processes of central carbon and nitrogen metabolism as well as cellular growth and division. Here, we performed a comprehensive analysis of the mechanisms of long-term photoacclimation of an extremophilic red alga Cyanidioschyzon merolae that grows in sulphuric hot springs at high temperatures and low pH. By using spectroscopic, confocal fluorescence microscopy, photosynthetic performance measurements and global transcriptome analyses, we identified several molecular mechanisms underlying the long-term adaptation of this acido-thermophilic red alga to varying light intensity and spectral quality. These include: (1) remodelling of the functional antenna size of both photosystems; (2) rearrangement of the PSB/PSII/PSI microdomains within thylakoids; (3) modulation of the photosynthetic performance parameters, especially at the level of non-photochemical quenching, and (4) transcriptional regulation of photosynthesis and its regulatory components as well as downstream metabolic pathways related to ROS detoxification, cell/organelle division, and central carbon and nitrogen metabolism. Such an intricate network of interplay between light-driven reactions and downstream metabolic pathways provides the necessary basis for maintaining the highest photosynthetic performance under light-limiting conditions.