Anaerobic Nitrogen Turnover by Sinking Diatom Aggregates at Varying Ambient Oxygen Levels

Abstract

In the world’s oceans, even relatively low oxygen levels inhibit anaerobic nitrogen cycling by free-living microbes. Sinking organic aggregates, however, might provide oxygen-depleted microbial hotspots in otherwise oxygenated surface waters. Here, we show that sinking diatom aggregates can host anaerobic nitrogen cycling at ambient oxygen levels well above the hypoxic threshold. Aggregates were produced from the ubiquitous diatom Skeletonema marinoi and the natural microbial community of seawater. Microsensor profiling through the center of sinking aggregates revealed internal anoxia at ambient 40% air saturation (∼100 μmol O2 L-1) and below. Accordingly, anaerobic nitrate turnover inside the aggregates was evident within this range of ambient oxygen levels. In incubations with 15N-labeled nitrate, individual Skeletonema aggregates produced NO2- (up to 10.7 nmol N h-1 per aggregate), N2 (up to 7.1 nmol N h-1), NH4+ (up to 2.0 nmol N h-1), and N2O (up to 0.2 nmol N h-1). Intriguingly, nitrate stored inside the diatom cells served as an additional, internal nitrate source for dinitrogen production, which may partially uncouple anaerobic nitrate turnover by diatom aggregates from direct ambient nitrate supply. Sinking diatom aggregates can contribute directly to fixed-nitrogen loss in low-oxygen environments in the ocean and vastly expand the ocean volume in which anaerobic nitrogen turnover is possible, despite relatively high ambient oxygen levels. Depending on the extent of intracellular nitrate consumption during the sinking process, diatom aggregates may also be involved in the long-distance export of nitrate to the deep ocean.

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

“…Assuming that these aerobic processes also occur in association with the particles, it is proposed that aerobic metabolisms occurring at the periphery of the oxygenated particle fuel the internal anaerobic pathways by the diffusion of their products (e.g. nitrite produced by AO) to the respiration-mediated anoxic core, similarly to the scenarios described for various other microbial aggregates in wastewater treatment plants (Nielsen et al, 2005), man-made model systems (Stief et al, 2016) and natural environments (Klawonn et al, 2015). 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.…”

“…This leads to an active removal of fixed N and greenhouse gas production (Farías et al, 2009;Galán et al, 2014). Likewise, the dense upwelled waters cause increased stratification in the water column, decelerating the downward flux of organic particles formed at the surface (Charpentier et al, 2007), facilitating their accumulation, and thus creating anoxic microbial hotspots within the oxycline that favour the N-based anaerobic microbial metabolisms (Klawonn et al, 2015;Stief et al, 2016).…”

Fixed-Nitrogen Loss Associated with Sinking Zooplankton Carcasses in a Coastal Oxygen Minimum Zone (Golfo Dulce, Costa Rica)

“…The 15 N-incubations were prepared on the next day using acid-washed, sample-rinsed glass bottles (25 mL) equipped with optode spots for contactless O 2 measurements (PyroScience, Germany) and sealed with butyl stoppers to enable sample extraction. Preparation, incubation, and sampling of the glass bottles were made as described by Stief et al (2016). Briefly, the bottles were filled with the appropriate mixture of oxygen-and helium-flushed seawater (for 15 min each) to arrive at the desired air saturation level of O 2 .…”

“…On the basis of the preceding O 2 measurement, the O 2 concentration in the replacement water was adjusted to a level that would compensate any observed concentration decrease. Oxygen consumption rates were calculated according to Stief et al (2016).…”

“…Thus, in pelagic ecosystems, copepods and other mesozooplankton represent vastly abundant "microbial hotspots" with unique biogeochemical features (Tang, 2005;Tang et al, 2010;Nuester et al, 2014). In this sense, zooplankters, and in particular their carcasses, resemble sinking phytodetritus aggregates that host dense microbial communities within a low-oxygen microenvironment (Ploug et al, 1997;Glud et al, 2015;Klawonn et al, 2015;Stief et al, 2016). The presence of zooplankton carcasses in the water column results from nonconsumptive mortality, caused by e.g., parasitism or turbulences, which allows extensive microbial degradation of carcasses during their descent to the seabed (Tang et al, 2011).…”