To elucidate the potential coupling of nitrification and denitrification processes in seasonal oxygen minimum zones, we linked the abundance and community composition of the main microbial players in the aerobic and anaerobic (anammox) ammonium oxidation and denitrification processes in the Gulf of Alaska throughout the water column. Furthermore, the abundance of functional marker genes for ammonia-oxidation and archaeal and bacterial denitrification was determined. Archaeal ammonia oxidizers (AOA) dominated the microbial community involved in the nitrogen cycle. Two AOA ecotypes, characterized by distinct genes for aerobic ammonia oxidation (amoA) and for denitrification (nirK), exhibited a distinct distribution pattern related to depth and ammonia concentrations. Bacterial denitrifiers were probably associated to particles and anaerobic ammonia oxidizers were low in abundance under the oxygen conditions in the Gulf of Alaska. Taken together, our results indicate that nitrification and denitrification in the oxygenic but also microaerobic and oxygen limited ocean is partitioned between two archaeal ammonia oxidizers ecotypes, with distinct metabolic characteristics. However, the widespread distribution of bacterial denitrifiers and anaerobic ammonia oxidizers in low abundances, reveals a reservoir of genetic and metabolic potential ready to colonize the environment under the predicted increase of oxygen minimum zones in the ocean.