Prevalence of Metalloenzymes in Oxygen Minimum Zones Extremities: Implicit Widespread Mesopelagic Nitrogen Cycling Activity and Potential Impacts of Deoxygenation on Nitrogen and Iron Biogeochemical Cycles

The major oxygen minimum zones (OMZs) of the oceans are regions where chemical transformations of nitrogen are thought to be particularly important. While OMZ studies have typically focused on the prevalence and controls of chemical reactions in close vicinity to coastal regions where oxygen is strongly depleted, less attention has been paid to the offshore extremities of OMZs. Using targeted metaproteomic techniques, we identified abundant microbial nitrogen cycle metalloenzymes within the outer limits of Pacific OMZ water column regions. Nitrite oxidoreductase was one of the most abundant proteins detected in the Central North Pacific Oxygen Minimum Zone (OMZ) and offshore from the Peru Upwelling Region. Extrapolating this enzyme’s concentrations and metal stoichiometry to the suboxic ocean volume implies it is likely one of the most abundant iron enzymes in the ocean. Consistent with these observations, this enzyme was also observed to be highly abundant within the proteomes of nitrifying bacterial cultures. Additional metalloenzymes ammonia monooxygenase and nitrite reductase were present throughout this region from Archaeal and bacterial microbial populations. Potential maximal reaction rates were calculated using measured enzyme concentrations and literature specific activities and provided oceanographically reasonable values. With future deoxygenation of the oceans, the distributions of these nitrogen cycle metalloenzymes found in the OMZ extremities will likely expand, with a concomitant increase in mesopelagic microbial metal demand and biogeochemical activities.