Ammonium and nitrite oxidation at nanomolar oxygen concentrations in oxygen minimum zone waters

Abstract

A major percentage of fixed nitrogen (N) loss in the oceans occurs within nitrite-rich oxygen minimum zones (OMZs) via denitrification and anammox. It remains unclear to what extent ammonium and nitrite oxidation co-occur, either supplying or competing for substrates involved in nitrogen loss in the OMZ core. Assessment of the oxygen (O 2 ) sensitivity of these processes down to the O 2 concentrations present in the OMZ core (<10 nmol·L −1 ) is therefore essential for understanding and modeling nitrogen loss in OMZs. We determined rates of ammonium and nitrite oxidation in the seasonal OMZ off Concepcion, Chile at manipulated O 2 levels between 5 nmol·L −1 and 20 μmol·L −1 . Rates of both processes were detectable in the low nanomolar range (5-33 nmol·L −1 O 2 ), but demonstrated a strong dependence on O 2 concentrations with apparent half-saturation constants (K m s) of 333 ± 130 nmol·L −1 O 2 for ammonium oxidation and 778 ± 168 nmol·L −1 O 2 for nitrite oxidation assuming one-component Michaelis-Menten kinetics. Nitrite oxidation rates, however, were better described with a two-component Michaelis-Menten model, indicating a high-affinity component with a K m of just a few nanomolar. As the communities of ammonium and nitrite oxidizers were similar to other OMZs, these kinetics should apply across OMZ systems. The high O 2 affinities imply that ammonium and nitrite oxidation can occur within the OMZ core whenever O 2 is supplied, for example, by episodic intrusions. These processes therefore compete with anammox and denitrification for ammonium and nitrite, thereby exerting an important control over nitrogen loss.is a key factor regulating biogeochemical cycling in the marine environment (1). Although the vast majority of the ocean remains well oxygenated, subsurface regions of extreme oxygen depletion can persist along eastern boundaries of the world's ocean basins. These regions are known as oxygen minimum zones (OMZs) and are located within the eastern tropical North and South Pacific, the Arabian Sea, and off the coast of Namibia, where oxygen depletion results from poor ventilation and a high export of organic matter from productive surface waters, generating high rates of subsurface oxygen consumption (2, 3).Oceanic waters characterized by oxygen-deficient conditions (<4.5 μmol·L −1 O 2 ) account for <0.1% of total ocean volume but for >30% of fixed nitrogen (N) loss (3-6) due to the onset of anaerobic processes, including denitrification and anammox (7-10). Both field and modeling observations point to the expansion of low oxygen regions as a result of global warming (11). Thus, to evaluate the biogeochemical impact of these regions, it is imperative to understand fully how oxygen controls the cycling of substrates involved in nitrogen loss pathways.Recent studies have quantified the oxygen sensitivity of anaerobic OMZ nitrogen transformations, finding that denitrification has relatively low oxygen tolerance with a half-inhibition concentration (IC 50 ) of 0.3 μmol·L −1 , compared with higher values for...

Cryptic oxygen cycling in anoxic marine zones

“…Our results show that the photosynthetic community of the SCM produces significant amounts of O 2 , sufficient to maintain an aerobic community in an otherwise anoxic environment. Rates of O 2 production and carbon fixation in the SCM in both ETNP and ETSP AMZs are comparable to previously measured rates of aerobic processes like nitrite and ammonium oxidation (8,17), as well as anaerobic AMZ processes like denitrification, anammox, and sulfate reduction (7,8). Although the measured metabolic rates exhibit large spatial and temporal variability, our data collectively suggest a significant effect of local photosynthesis on the biogeochemical cycling in Pacific Ocean AMZs.…”

Vertical segregation among pathways mediating nitrogen loss (N&lt;sub&gt;2&lt;/sub&gt; and N&lt;sub&gt;2&lt;/sub&gt;O production) across the oxygen gradient in a coastal upwelling ecosystem

“…On the other hand, the detection of nitrification during anoxic incubations has been attributed to the persistence of traces of O 2 in the samples (e.g. Bristow et al, 2016;Ganesh et al, 2015), although those studies exhibited caution to O 2 contamination that was similar to this study (see Sect. 2.5 in Methods).…”

“…However, a dominance of bacterial AO 4808 A. Galán et al: Vertical segregation among pathways mediating nitrogen loss does not correspond to recent molecular and biogeochemical observations from the study area, particularly during the upwelling season, when a high abundance of Thaumarchaeota (previously Crenarchaeota; an archaeon that sustains itself chemolithoautotrophically through aerobic oxidization of NH + 4 ) account for a significant fraction of the microbial assemblage, while ammonium-oxidizing bacteria are scarce or undetectable (Levipan et al, 2007;Quiñones et al, 2009;Bristow et al, 2016). Likewise, the relative contribution to ammonium oxidation, quantified by the ammonia monooxygenase subunit A gene (Molina et al, 2010), and dark carbon assimilation rates (Farías et al, 2009), showed that archaea had a greater potential activity relative to the homologous bacteria in the system.…”

Determination of Respiration Rates in Water with Sub-Micromolar Oxygen Concentrations

“…Element transformations in Oxygen Minimum Zones (OMZs) are very dependent on the local O 2 concentrations, and it has for example been shown that O 2 concentrations below 0.5 µmol L −1 may be strongly inhibitory for denitrification (Dalsgaard et al, 2014;Bristow et al, 2016), but that sub-micromolar O 2 concentrations still allow for high rates of ammonium and nitrite oxidation (Kalvelage et al, 2011(Kalvelage et al, , 2015Füssel et al, 2012;Beman et al, 2013;Bristow et al, 2016). It is thus crucial for our study and understanding of element transformations in OMZ waters that we know exactly which O 2 regime is found in situ, and that we can reproduce this in the laboratory when analyzing rates of element transformations.…”