The discovery of Archaea carrying an amoA gene coding for the A-subunit of ammonia monooxygenase gave a boost to studies aimed at detecting this gene under diverse conditions. Despite numerous studies describing the archaeal amoA gene abundance and richness in different habitats, the understanding of the freshwater ecology of potentially archaeal ammonia oxidizers, recently positioned in the phylum Thaumarchaeota, is still lacking. In a seasonal and vertical study of deep oligotrophic Lake Lucerne, Switzerland, with high Thaumarchaeota-specific crenarchaeol concentrations, we showed that all archaeal 16S rRNA genes found belong to the thaumarchaeotal phylum. The abundances of archaeal 16S rRNA and amoA genes remained in the same order of magnitude (average 6 × mL−1) and displayed matching seasonal dynamics within 16 monthly collected samples at three different water depths (r2 = 0.80, slope of 1.06). The Thaumarchaeota in this lake form a distinct cluster in both the 16S rRNA and amoA gene phylogenies, are affiliated to other thaumarchaeotal freshwater sequences within group 1.1a Archaea, and fall in the low saline cluster of the amoA phylogeny. In accordance with temperature and conductivity, the Thaumarchaeota in the surface water showed a significantly different seasonality and lower abundance than their counterparts in the deeper waters. This study indicates that the ecology of Thaumarchaeota, with their potential in nitrogen cycling, may differ per water depth in deep freshwater ecosystems.