Hydrogen peroxide detoxification is a key mechanism for growth of ammonia-oxidizing archaea

Ammonia-oxidizing archaea (AOA), that is, members of the Thaumarchaeotaphylum, occur ubiquitously in the environment and areof major significance for global nitrogen cycling. However, controls oncell growth and organic carbon assimilation by AOA are poorlyunderstood. We isolated an ammonia-oxidizing archaeon (designatedstrain DDS1) from seawater and used this organism to study the physiologyof ammonia oxidation. These findings were confirmed usingfour additional Thaumarchaeota strains from both marine and terrestrialhabitats. Ammonia oxidation by strain DDS1 was enhanced incoculture with other bacteria, as well as in artificial seawater mediasupplemented with a-keto acids (e.g., pyruvate, oxaloacetate). a-Ketoacid-enhanced activity of AOA has previously been interpreted as evidenceof mixotrophy. However, assays for heterotrophic growth indicatedthat incorporation of pyruvate into archaeal membrane lipidswas negligible. Lipid carbon atoms were, instead, derived from dissolvedinorganic carbon, indicating strict autotrophic growth. a-Ketoacids spontaneously detoxify H2O2 via a nonenzymatic decarboxylationreaction, suggesting a role of a-keto acids as H2O2 scavengers.Indeed, agents that also scavenge H2O2, such as dimethylthiourea andcatalase, replaced the a-keto acid requirement, enhancing growth ofstrain DDS1. In fact, in the absence of a-keto acids, strain DDS1 andother AOA isolates were shown to endogenously produce H2O2 (upto ~4.5 µM), which was inhibitory to growth. Genomic analyses indicatedcatalase genes are largely absent in the AOA. Our resultsindicate that AOA broadly feature strict autotrophic nutrition andimplicate H2O2 as an important factor determining the activity, evolution,and community ecology of AOA ecotypes