Nitrogen cycling in the deep sedimentary biosphere: nitrate isotopes in porewaters underlying the oligotrophic North Atlantic

Nitrogen (N) is a key component of fundamental biomolecules. Hence, its cycling and availability are central factors governing the extent of ecosystems across the Earth. In the organic-lean sediment porewaters underlying the oligotrophic ocean, where low levels of microbial activity persist despite limited organic matter delivery from overlying water, the extent and modes of nitrogen transformations have not been widely investigated. Here we use the N and oxygen (O) isotopic composition of porewater nitrate (NO3-) from a site in the oligotrophic North Atlantic (Integrated Ocean Drilling Program - IODP) to determine the extent and magnitude of microbial nitrate production (via nitrification) and consumption (via denitrification). We find that NO3- accumulates far above bottom seawater concentrations ( 21 mu M) throughout the sediment column (up to 50 mu M) down to the oceanic basement as deep as 90 m b.s.f. (below sea floor), reflecting the predominance of aerobic nitrification/remineralization within the deep marine sediments. Large changes in the delta N-15 and delta O-18 of nitrate, however, reveal variable influence of nitrate respiration across the three sites. We use an inverse porewater diffusion-reaction model, constrained by the N and O isotope systematics of nitrification and denitrification and the porewater NO3- isotopic composition, to estimate rates of nitrification and denitrification throughout the sediment column. Results indicate variability of reaction rates across and within the three boreholes that are generally consistent with the differential distribution of dissolved oxygen at this site, though not necessarily with the canonical view of how redox thresholds separate nitrate regeneration from dissimilative consumption spatially. That is, we provide stable isotopic evidence for expanded zones of co-occurring nitrification and denitrification. The isotope biogeochemical modeling also yielded estimates for the delta N-15 and delta O-18 of newly produced nitrate (delta N-15(NTR) (NTR, referring to nitrification) and delta O-18(NTR)), as well as the isotope effect for denitrification ((15)epsilon(DNF)) (DNF, referring to denitrification), parameters with high relevance to global ocean models of N cycling. Estimated values of delta N-15(NTR) were generally lower than previously reported delta N-15 values for sinking particulate organic nitrogen in this region. We suggest that these values may be, in part, related to sedimentary N-2 fixation and remineralization of the newly fixed organic N. Values of delta O-18(NTR) generally ranged between -2.8 and 0.0 parts per thousand, consistent with recent estimates based on lab cultures of nitrifying bacteria. Notably, some delta O-18(NTR) values were elevated, suggesting incorporation of O-18-enriched dissolved oxygen during nitrification, and possibly indicating a tight coupling of NH4+ and NO2- oxidation in this metabolically sluggish environment. Our findings indicate that the production of organic matter by in situ autotrophy (e.g., nitrification, nitrogen fixation) supplies a large fraction of the biomass and organic substrate for heterotrophy in these sediments, supplementing the small organic-matter pool derived from the overlying euphotic zone. This work sheds new light on an active nitrogen cycle operating, despite exceedingly low carbon inputs, in the deep sedimentary biosphere.