Polar winter waters are one of the least studied marine ecosystems with regard to microbial life and Thaumarchaeota are key microorganisms in this environment. We collected data on abundance and metabolic activity of Thaumarchaeota in Arctic and Antarctic waters in different seasons, including the wintertime. As previously observed, Arctic Thaumarchaeota grew throughout the winter, increasing their abundances one order of magnitude from January to March 2008. Yet, paradoxically, in situ single-cell measurements revealed an unexpected low metabolic activity for this group in both polar systems, i.e., less than 5% of archaeal cells taking up leucine or bicarbonate, inconsistent with known heterotrophic or autotrophic archaeal lifestyles. To resolve how archaea obtain energy and carbon for growth, we analyzed a metagenome collected during the Arctic winter, when the Thaumarchaeota population was at its maximum of abundance (18% of cell counts). Metagenomics and quantitative PCR showed that archaeal amoA genes were abundant in Arctic and Antarctic waters, indicating that polar Thaumarchaeota have the potential for ammonia oxidation. The presence of a large number of archaeal genes involved in urea transport and degradation together with detectable uptake of 14C-labeled urea by the prokaryotic assemblage, suggest that the products of urea hydrolysis (NH3 and CO2) may be sources of both energy and carbon for polar ammonia oxidizing archaea. This hypothesis, consistent with the idea of polar archaea growing as nitrifiers but with apparent low incorporation of bicarbonate, would provide the molecular basis for the recurrent archaeal growth in polar winter waters.