Light is a key environmental regulator in all photosynthetic organisms. Many studies focused on the physiologic response to changes in light availability of species from the Zygnematophyceae, but the impact of the absence of light and the molecular acclimation process on the other side have been poorly understood. Here we present transcriptomic analyses of Cosmarium crenatum from a polar habitat exposed to darkness. The algae were cultured in dark for one week; cell number and quantum yield of photosystem II (Fv/Fm) were monitored. Cell number was stable, but the Fv/Fm decreased in both groups, darkness-treated and control. Gene expression analysis revealed a strong repression of transcripts associated with photosynthesis, photorespiration and cell wall development. General carbohydrate and lipid metabolism were differentially regulated, but starch is shown to be the primary energy source in these conditions. Additionally, C. crenatum induced mRNA responsible for epigenetic modifications which may be a specific response to an adaption and acclimation to polar conditions. Our study sheds light on the molecular acclimation process to darkness and provides ecological implications for new perspectives in this specialized group of green algae.