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

Doctoral Thesis


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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, < 4% on average derived from mixed-layer nitrification. While the near-zero mixed-layer nitrification rates measured in summer could be taken as confirmation that nitrate uptake is a good proxy for Southern Ocean carbon export potential, a portion of the nitrate consumed in the summertime euphotic zone was produced in the winter mixed layer and will thus not support net carbon dioxide removal on an annual basis. Despite the high rates of ammonium uptake and oxidation measured in winter Southern Ocean surface waters, mixed-layer ammonium concentrations remain fairly high, indicating an imbalance between ammonium production and consumption. Kinetics experiments conducted across the Indian sector (37-62ºS) reveal a seasonal switch from a phytoplankton community with a high affinity for ammonium in summer to one with a lower affinity in winter, even though phytoplankton at similar latitudes achieved a comparable maximum specific ammonium uptake rate in summer and winter. Rates of ammonium oxidation showed a Michaelis-Menten response to substrate availability only when the ambient ammonium concentration was ≤90 nM. This, coupled with half-saturation constants (Km values) of 28-137 nM (i.e., indicating a very high affinity for ammonium) suggest a dominant role for ammonia oxidizing archaea in mixed-layer nitrification. The maximum rate of ammonium oxidation was near-constant across the transect (37-62ºS), despite a significant gradient in sea surface temperature, light availability and ammonium concentration, perhaps due to iron limitation of ammonium oxidation, which has been hypothesized from culture experiments but not yet shown in the environment. It is possible that iron depletion in the surface Southern Ocean may limit the role of winter mixed-layer nitrification in offsetting phytoplankton CO2 drawdown annually. To better understand the controls on nitrifier ecology in the surface Southern Ocean, a series of nitrite oxidation kinetics experiments were conducted across the Indian sector (37- 62ºS) in winter. All experiments yielded a Michaelis-Menten relationship with substrate concentration, yet the nitrite oxidation rates only increased significantly at nitrite concentrations >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.