Niche Differentiation of Aerobic and Anaerobic Ammonia Oxidizers in a High Latitude Deep Oxygen Minimum Zone

To elucidate the potential for nitrification and denitrification processes in a high latitude deep oxygen minimum zone (OMZ) we determined 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. Within the dominant bacterial groups, Flavobacterales, Rhodobacterales, Actinomarinales, and SAR86 were more abundant in epipelagic waters and decreased with depth, whereas SAR11, SAR324, Marinimicrobia, and Thiomicrospirales increased their contribution to the bacterial community with depth. Nitrosopumilaceae also increased with depth and dominated the OMZ and bathypelagic archaeal communities. Euryarchaeota Marine Group II exhibited an opposite depth pattern to Nitrosopumilaceae, whereas Marine Group III and Woesearchaeota were more abundant in the bathypelagic realm. Candidatus Brocadia contributed 70-100% of the anammox bacterial community throughout the water column. Archaeal ammonia oxidizers (AOA) dominated the microbial community involved in the nitrogen cycle. Two AOA ecotypes, the high ammonia (HAC) and low ammonia (LAC)-AOA, characterized by distinct genes for aerobic ammonia oxidation (amoA) and for denitrification (nirK), exhibited a distinct distribution pattern related to depth and ammonia concentrations. HAC-AOA dominated in epipelagic (80.5 +/- 28.3% of total AOA) oxygenated and ammonia-rich waters, and LAC-AOA dominated in the OMZ (90.9 +/- 5.1%) and bathypelagic waters (85.5 +/- 13.5%), characterized by lower oxygen and ammonia concentrations. Bacterial denitrifiers (3.7 +/- 6.9 bacterial nirK gene mL(-1)) and anaerobic ammonia oxidizers (78 +/- 322 anammox 16S rRNA genes L-1) were low in abundance under the oxygen conditions in the Gulf of Alaska throughout the water column. 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 OMZs in the ocean. Taken together, our results reinforce the niche partitioning of archaeal ammonia oxidizers based on their distinct metabolic characteristics resulting in the dominance of LAC-AOA in a high latitude deep OMZ. Considering the different ecological roles and functions of the two archaeal ecotypes, the expansion of the zones dominated by the LAC-ecotype might have implications for the nitrogen cycle in the future ocean.