Soil microorganisms require metabolic strategies to cope with the significant variations in oxygen availability that occur in soil over a range of time scales. Characterised ammonia-oxidisers within Thaumarchaeota Groups 1.1a and 1.1b are aerobic, but the oxygen preference and metabolic potential of deeply-rooted Thaumarchaeota remain unknown, with several studies providing evidence for both aerobic and anaerobic metabolisms. This study therefore aimed to determine the influence of oxygen on the mesophilic Group 1.1c and Group 1.3 thaumarchaeotal community in controlled microcosm experiments conducted using oxic and anoxic Scottish pine forest soils, incubated under oxic or anoxic conditions. While we expected more anaerobic growth metabolism in those peatland soils, we demonstrated growth of multiple aerobic clusters within Group 1.1c Thaumarchaeota and anaerobic growth within Group 1.3 Thaumarchaeota. These findings extend our understanding of the physiology of deeply-rooted mesophilic Thaumarchaeota and provide the first detailed qualitative and quantitative assessment of their growth in soil.