The archaea Cuniculiplasma divulgatum are abundant in acidic environments with low to moderate temperatures. However, the molecular mechanisms underlying its ability to thrive at low temperatures remain unexplored. Using mass spectrometry (MS)-based proteomics, we analysed the effect of short-term (3 h) exposure to cold shock. The C. divulgatum genome encodes 2,016 protein-coding genes, from which 819 proteins were identified in the cells grown under optimal conditions. In line with the peptidolytic lifestyle of C. divulgatum, its intracellular proteome revealed the abundance of proteases, ABC transporters and cytochrome C oxidase. From 747 quantifiable polypeptides, the levels of 582 proteins showed no change after the cold shock (the core proteome), whereas 104 proteins were upregulated suggesting that they might be contributing to cold adaptation. The highest increase in protein levels was found for the metal-dependent hydrolase, FAD-dependent oxidoreductase, aspartate carbamoyltransferase regulatory chain proteins, 2-oxoacid ferredoxin oxidoreductase and ATPase-V type ATP synthase. Furthermore, the cold shock induced a substantial increase (3.5 % and 9.0 %) in the levels of two most abundant intracellular proteins, chaperonin and glutamate dehydrogenase. This study has outlined potential mechanisms of environmental fitness of Cuniculiplasma spp. allowing them to colonise and survive in acidic settings at low/ moderate temperatures.