Integrated photochemical and transcriptomic responses reveal an adaptive strategy of the Antarctic snow alga Chlorominima collina (Chlorophyta) for surviving freezing and darkness

Snow algae represent important primary producers and carbon sinks in the cryosphere. Disentangling the physiological and molecular responses that these organisms display in the face of acute abiotic stress caused by snow dynamics is key to revealing survival strategies and monitoring climate change effects. Here, we examine the tolerance to a short-term (4 h) freezing condition (-20°C) in darkness, followed by a recovery period, in the Antarctic snow alga Chlorominima collina. The responses were analyzed in contrast to a light control (2 °C) by integrating of chlorophyll fluorescence of PSII, mRNA-sequencing and oxidative stress detection. The treated cells reduce PSII photochemical efficiency and suppress the light harvesting process. Simultaneously abiotic stress-responsive genes were expressed, suggested a reprograming of metabolism and process, orchestrated by key signaling pathways and transcription factors. This profile revealed common elements of states prior to hypometabolism such as, the fuel switch from carbohydrate to lipid catabolism, improved defenses, repression of biosynthetic processes, induction of mitophagy and autophagy, and regulation of transcription and translation. These adjustments promoted the maintenance of cellular homeostasis, as evidenced by enrichment of this process and the recovery of PSII efficiency. Therefore, we proposed that the integration of the reduction of efficiency with which PSII captures energy and the regulation of genes involved in the induction of hypometabolism constitutes an adaptive strategy that confers at snow algae freezing and darkness tolerance. Collectively, the observed functional changes may be relevant for understanding the survival and subsequent adaptation of Chlorophyta to the Antarctic snow environment.