The discovery of ammonia oxidation by mesophilic and thermophilic Crenarchaeota and the widespread distribution of these organisms in marine and terrestrial environments indicated an important role for them in the global nitrogen cycle. However, very little is known about their physiology or their contribution to nitrification. Here we report oligotrophic ammonia oxidation kinetics and cellular characteristics of the mesophilic crenarchaeon `Candidatus Nitrosopumilus maritimus' strain SCM1. Unlike characterized ammonia-oxidizing bacteria, SCM1 is adapted to life under extreme nutrient limitation, sustaining high specific oxidation rates at ammonium concentrations found in open oceans. Its half-saturation constant (Km = 133nM total ammonium) and substrate threshold (<=10nM) closely resemble kinetics of in situ nitrification in marine systems and directly link ammonia-oxidizing Archaea to oligotrophic nitrification. The remarkably high specific affinity for reduced nitrogen (68,700l per g cells per h) of SCM1 suggests that Nitrosopumilus-like ammonia-oxidizing Archaea could successfully compete with heterotrophic bacterioplankton and phytoplankton. Together these findings support the hypothesis that nitrification is more prevalent in the marine nitrogen cycle than accounted for in current biogeochemical models.