Temperature-dependent photostasis and nitrogen limitation in streamlined-genome red algae Cyanidiophyceae from natural habitats

Photosynthetic microorganisms must continuously balance light energy absorption with metabolic demand to maintain photostasis under fluctuating environments. Cyanidiophyceae, unicellular red algae from acidic hot springs with highly streamlined genomes (9-18 Mb), nevertheless thrive across a wide temperature range (20-56°C), posing the question of how such minimalist eukaryotic cells sustain photostasis in nature. Here, we combined field observations of natural mats in sulfuric hot springs in Japan with laboratory experiments under habitat-mimicking conditions. Spring-water chemistry remained nearly constant year-round, characterized by low nitrogen availability (<30 μM), whereas temperature varied spatially and seasonally. Growth increased with temperature (up to 47°C) and nearly ceased at 20-25°C, yet photosynthetic pigment levels and apparatus components remained largely unchanged, indicating sustained light absorption even under conditions of minimal growth. At low temperatures, photosystem efficiency and regulated energy dissipation decreased, whereas non-regulated dissipation and reactive oxygen species (ROS) increased, indicating excess excitation energy was mainly dissipated through non-regulated pathways. Proteomic and transcriptomic analyses showed accumulation of ROS scavengers and chromosome maintenance/repair proteins at low temperature, suggesting that excess reducing power/ATP, even after partial energy dissipation, was redirected toward stress mitigation rather than growth. At higher temperatures, nitrogen-deficiency responses emerged, reflecting nitrogen limitation relative to elevated demand for rapid growth. Together, these results reveal a temperature-dependent trade-off in Cyanidiophyceae in natural habitats: oxidative stress at low temperature versus nitrogen limitation at high temperature. Overall, our findings highlight a simple yet robust photostasis strategy and provide environmental and omics resources for studies of this model lineage.