Mixed layer nitrogen cycling in the Southern Ocean: seasonality, kinetics, and biogeochemical implications

The alternation between summertime nitrate drawdown and wintertime nitrate recharge is central to the role of the Southern Ocean in setting atmospheric CO2. However, active cycling of nitrogen (N) in the seasonally-varying mixed layer – including the production of ammonium and its subsequent removal via phytoplankton uptake and nitrification (i.e., the oxidation of ammonium to nitrite and then nitrate) – remains poorly understood. Following the “new production paradigm”, phytoplankton production fueled by ammonium (“regenerated production”) results in no net drawdown of CO2 to the deep ocean, while growth supported by nitrate (“new production”) can be equated to CO2 removal provided that mixed-layer nitrification is negligible. While non-zero mixed-layer nitrification has been measured in many ocean regions, very few data exist for the Southern Ocean. This thesis presents new N cycle data collected across the Southern Ocean south of Africa in winter and summer that emphasize the integral role of mixed-layer N transformations in Southern Ocean productivity and biological CO2 drawdown. To evaluate the new production paradigm as a framework for quantifying Southern Ocean carbon export potential, rates of net primary production (NPP), N uptake (as ammonium and nitrate) and nitrification (ammonium and nitrite oxidation) were measured across the Atlantic sector in winter and summer. Winter mixed-layer NPP and total N (i.e., ammonium + nitrate) uptake were strongly decoupled, likely due to elevated heterotrophic bacterial consumption of ammonium. In summer, NPP and total N were generally well-coupled, although dissolved organic N apparently supported more than a third of NPP at some stations. Nitrification accounted for >100% of the nitrate consumed by phytoplankton in winter, rendering the new production paradigm ill-suited for quantifying carbon export in this season. By contrast, of the >50% of summertime NPP fueled by nitrate, 115-245 nM, suggesting that nitrite oxidizers require a minimum (i.e., “threshold”) nitrite concentration to produce nitrate. Low derived Km values (134-403 nM) that increased with increasing ambient nitrite indicate a high affinity of nitrite oxidizers for substrate, in contrast to results from culture experiments. Throughout the Southern Ocean mixed layer, ambient nitrite concentrations are rarely less than 150 nM, regardless of season. Coincident measurements of ammonium and nitrite oxidation in the mixed layer suggest that nitrite oxidation is the rate-limiting step for nitrification in the winter Southern Ocean. This, combined with a possible nitrite concentration threshold for nitrite oxidation, may explain the perennial non-zero mixed-layer nitrite. A possible explanation for the apparent threshold nitrite requirement of nitrite oxidizers is undersaturation of the hemerich nitrite oxidoreductase enzyme, perhaps driven by the limited availability of iron in Southern Ocean surface waters. The findings described in this thesis yield new insights into the active cycling of N within the Southern Ocean's mixed layer, and particularly emphasize the need for seasonally-resolved parallel N- and iron cycle investigations to fully understand the role of nitrification in biological CO2 removal and N supply. Climate change-driven warming and acidification of Southern Ocean surface waters is already driving changes in microbial community composition, nutrient supply, and primary productivity. If we are to better predict the Southern Ocean's future role in CO2 sequestration and global ocean fertility, an improved understanding of the controls on mixed layer N cycling, particularly nitrification, is essential

Database of nitrification and nitrifiers in the global ocean

As a key biogeochemical pathway in the marine nitrogen cycle, nitrification (ammonia oxidation and nitrite oxidation) converts the most reduced form of nitrogen – ammonium–ammonia (NH4+–NH3) – into the oxidized species nitrite (NO2-) and nitrate (NO3-). In the ocean, these processes are mainly performed by ammonia-oxidizing archaea (AOA) and bacteria (AOB) and nitrite-oxidizing bacteria (NOB). By transforming nitrogen speciation and providing substrates for nitrogen removal, nitrification affects microbial community structure; marine productivity (including chemoautotrophic carbon fixation); and the production of a powerful greenhouse gas, nitrous oxide (N2O). Nitrification is hypothesized to be regulated by temperature, oxygen, light, substrate concentration, substrate flux, pH and other environmental factors. Although the number of field observations from various oceanic regions has increased considerably over the last few decades, a global synthesis is lacking, and understanding how environmental factors control nitrification remains elusive. Therefore, we have compiled a database of nitrification rates and nitrifier abundance in the global ocean from published literature and unpublished datasets. This database includes 2393 and 1006 measurements of ammonia oxidation and nitrite oxidation rates and 2242 and 631 quantifications of ammonia oxidizers and nitrite oxidizers, respectively. This community effort confirms and enhances our understanding of the spatial distribution of nitrification and nitrifiers and their corresponding drivers such as the important role of substrate concentration in controlling nitrification rates and nitrifier abundance. Some conundrums are also revealed, including the inconsistent observations of light limitation and high rates of nitrite oxidation reported from anoxic waters. This database can be used to constrain the distribution of marine nitrification, to evaluate and improve biogeochemical models of nitrification, and to quantify the impact of nitrification on ecosystem functions like marine productivity and N2O production. This database additionally sets a baseline for comparison with future observations and guides future exploration (e.g., measurements in the poorly sampled regions such as the Indian Ocean and method comparison and/or standardization). The database is publicly available at the Zenodo repository: https://doi.org/10.5281/zenodo.8355912 (Tang et al., 2023).</p

The kinetics of ammonium uptake and oxidation across the Southern Ocean

International audienceCentral to the Southern Ocean's role in setting atmospheric CO2 is the seasonal alternation between upward mixing of nutrients and their subsequent consumption by phytoplankton. Active nutrient cycling within the mixed layer, including the release of ammonium (NH4+) and its removal by phytoplankton and nitrifiers, also affects Southern Ocean CO2 drawdown, yet remains poorly understood. We conducted kinetics experiments across the Southern Ocean south of Africa to investigate the dependence of NH4+ uptake (summer, winter) and oxidation (winter) on NH4+ concentration. NH4+ uptake followed a Michaelis–Menten function in both seasons, with the maximum rate (Vmax) decreasing poleward, apparently controlled mainly by light in winter and temperature in summer. The half-saturation constant (Km) increased poleward with increasing ambient NH4+ ([NH4+]amb) and was threefold higher in winter (150–405 nM) than in summer (41–115 nM), suggesting that summertime phytoplankton are adapted to low-NH4+ conditions while winter communities typically receive a higher NH4+ supply. NH4+ oxidation showed a high affinity for NH4+ (Km = 28–137 nM), suggesting a dominant role for ammonia-oxidizing archaea, and followed a Michaelis–Menten curve only when [NH4+]amb was ≤ 90 nM. Vmax was near-constant across the region regardless of [NH4+]amb, temperature, or light. From coincident mixed-layer NH4+ oxidation and iron measurements, we hypothesize that iron availability may (co-)limit the Vmax of NH4+ oxidation. If verified, this suggestion has implications for models that parameterize nitrification as a linear function of [NH4+]amb. Additionally, iron depletion may limit the role of mixed-layer nitrification, which is dominant in the winter Southern Ocean, in offsetting phytoplankton CO2 drawdown annually