Evidence and a conceptual model for the co-occurrence of nitrogen fixation and denitrification in heterotrophic marine sediments

Marine waters are often nitrogen (N) limited. Denitrification, the microbial conversion of nitrate to dinitrogen (N-2) gas, is responsible for significant N removal from the coastal ocean. In contrast, nitrogen fixation, the microbial transformation of N-2 to ammonium, is typically regarded as an inconsequential N source. The imbalance between these 2 processes is responsible, at least in part, for N limitation in the coastal ocean. Organic matter quality and quantity has been shown to determine rates of these critical N cycling processes. We hypothesized that the timing of organic matter deposition to the benthos might also be important in determining which process dominates. We tested this hypothesis using a coupled biogeochemical-molecular approach. We report directly measured net sediment denitrification rates and corresponding expression of nirS, a gene in the denitrification pathway, with the simultaneous expression of nifH, a gene associated with nitrogen fixation. The timing of organic matter deposition determined the magnitude of the net sediment N-2 fluxes. Highest rates of denitrification occurred soon after deposition, and the lowest rates occurred over 200 d after the last deposition event concomitant with increased nifH expression. Phylogenetic evidence suggests that sulfur and sulfate reducers are responsible for the nitrogen fixation. Globally, warming water temperatures, changes in light, and reduced nutrient loads through management intervention have been linked to decreases and/or altered phenology of water column productivity. Based on a conceptual model developed here, we suggest that in these systems, heterotrophic sediment nitrogen fixation may become an important component of the nitrogen budget.