Nitrogen cycling in strong redox gradients of marine environments: Oceanic oxygen minimum zones and salt marsh sediments

Abstract

Essential for all known living organisms, nitrogen is often the limiting nutrient in most of the open ocean and other types of marine environments. Therefore it is important to understand the budget and cycling of nitrogen, which supports primary production. Nitrogen takes multiple forms with different reduction-oxidation (redox) states, and the transformation between them controls the biological availability of nitrogen. Strong redox gradients in the environment are hotspots of nitrogen cycling, which is largely mediated by microorganisms. This thesis reports investigations of microbial nitrogen cycling in two types of marine environments characterized by sharp oxygen gradients: oceanic oxygen minimum zones (OMZs) and salt marsh sediments.

Nitrification, the oxidation of ammonia to nitrite and then nitrate, links the most reduced and the most oxidized forms nitrogen. It was recently discovered that ammonia-oxidizing archaea (AOA) are one of the most abundant groups of picoplankton in the ocean. Although AOA are considered to be obligate aerobes, high abundances of AOA functional genes were reported at anoxic depths of OMZs. I analyzed the AOA community composition in OMZs using a DNA microarray, and found that the AOA assemblages at anoxic depths were not different from those at oxic depths. This suggests that AOA might possess some unknown metabolism that allows them to survive at anoxic conditions.

Nitrification produces substrates for denitrification, the sequential reduction of nitrate to dinitrogen gas, which is highly active in both OMZs and salt marsh sediments. The depth and spatial distribution of ammonia and nitrite oxidation rates were determined using incubations with 15N labeled substrates in two major OMZs: eastern tropical North and South Pacific. While organic matter flux exerts a first-order control on nitrification rates in OMZs, my study revealed that light, in situ concentrations of oxygen and ammonium are all strongly correlated with ammonia oxidation rates. High rates of nitrite oxidation were measured at anoxic depths, and this remains unexplained.

Situated between the land and the sea, salt marshes provide numerous valuable ecological services. Among them nitrogen removal alleviates nitrogen loading entering the coastal ocean and hence reduces the chance of eutrophication, which has increased due to high anthropogenic sources of nitrogen (“fertilization”). The effect of long-term fertilization on nitrogen cycling was examined in experimental plots established in a New England salt marsh. Using slurry incubations with 15N labeled substrates, I found that nitrification and denitrification rates have increased by more than ten-fold due to long-term fertilization. On the other hand, dissimilatory nitrate reduction to ammonium, which retains nitrogen in the system, was high in unfertilized plots but not detected in fertilized plots. These results suggest that long-term fertilization shifted nitrogen cycling in salt marsh sediments from predominantly retention to removal.