Copepod-associated anaerobic nitrogen cycling across ecosystems and taxonomic groups

Organic aggregates sinking through marine and freshwater water bodies are increasingly perceived as abundant hotspots of anaerobic microbial metabolism that cannot take place in the surrounding oxygenated water. While the research focus is often on phytoplankton-derived aggregates, zooplankton may also provide anoxic microenvironments, such as guts, fecal pellets, and carcasses of copepods. We tested therefore, if anaerobic nitrogen cycling is associated with copepods collected from polar, temperate, and tropical marine or freshwater ecosystems and belonging to different taxonomic groups and size classes. Dissimilatory nitrogen transformations were quantified using 15N tracing with living and dead copepods and with fecal pellets at different ambient oxygen levels to mimic conditions prevailing in the respective ecosystem. Significant anaerobic nitrogen cycling was without exception associated with copepod carcasses and was also evident in living specimens and fecal pellets of Calanus hyperboreus, a key component of Arctic marine zooplankton. In this large copepod species, denitrification was the dominant pathway of anaerobic nitrogen cycling and correlated with the presence or absence of food particles in the gut, but not with ambient oxygen levels. In contrast, the carcasses of the much smaller tropical marine and temperate freshwater copepods displayed high rates of dissimilatory nitrate reduction to ammonium or nitrite that were boosted by low ambient oxygen levels. Extrapolated to their in situ carcass abundance, copepods contribute up to 28% to the total fixed-nitrogen loss in oxic/hypoxic settings and up to 14% in anoxic settings. Overall, copepods greatly expand the water volume in which anaerobic nitrogen cycling is possible.