Thaumarchaeota are the most globally significant archaea in the nitrogen cycle, and one of the most numerically abundant phyla today. The first thaumarchaeote to be isolated was a marine ammonia-oxidizing archaeon (AOA; Könneke, et al. 2005). Although thaumarchaeotal catabolism requires molecular oxygen, AOA retain activity at low oxygen levels, and peak in abundance at oxic-anoxic interfaces where ammonia and oxygen are available, albeit at low concentrations. AOA produce elevated levels of gaseous N compounds (NO, a toxic yet vital metabolic intermediate, and N2O, a potent greenhouse gas) under oxygen depletion (Kozlowski et al., 2016), although the mechanism of archaeal N2O production remains debated. The discovery of numerous genes encoding copper-containing enzymes in AOA genomes is particularly intriguing because ammonia-oxidizing bacteria (AOB), which commonly dominate in ecosystems with plentiful ammonia, rely on a multitude of iron-based proteins for their metabolism. It has thus been hypothesized that AOA evolved after the Great Oxidation Event (~2.4 billion years ago) and a concurrent rise in environmental copper levels under more oxidizing conditions (Klotz & Stein, 2008). Many unanswered questions remain about the timing of marine AOA evolution and the consequences of AOA diversification and ocean oxygenation for nitrogen and greenhouse gas cycling. This talk will address AOA metabolism, phylogeny, and evolution in the context of changing seawater iron and copper availability over Earth history, as well as depth-and oxygen-dependent correlations between iron and copper concentrations, and environmental genes and transcripts encoding archaeal iron and copper proteins, in modern seawater samples (Glass et al., 2015). This research was supported by the NASA Astrobiology Institute Alternative Earths team (NNA15BB03A).