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.
Highlights
Marine snow comprises a variety of organic aggregates, larger than 500 μm in diameter, that are suspended in the ocean’s water column (Simon et al, 2002; Turner, 2015)
Diatom aggregates were produced on a plankton wheel from axenic cultures of S. marinoi and the natural microbial community of coastal seawater
The microscale O2 distribution inside dark-incubated, sinking Skeletonema aggregates was determined with O2 microsensors in a net-jet flow system (Ploug and Jørgensen, 1999)
Summary
Marine snow comprises a variety of organic aggregates, larger than 500 μm in diameter, that are suspended in the ocean’s water column (Simon et al, 2002; Turner, 2015). Anoxic centers have been directly traced with O2 microsensors only in relatively large organic aggregates, such as fecal pellets (Alldredge and Cohen, 1987), laboratory-made aggregates (Ploug et al, 1997; Ploug and Bergkvist, 2015), zooplankton carcasses (Glud et al, 2015), and cyanobacterial colonies (Paerl and Bebout, 1988; Klawonn et al, 2015) Even in such aggregates, anoxia may be short-lived due to carbon limitation (Ploug et al, 1997), the distribution of O2 may be patchy (Paerl and Bebout, 1988), and low-oxygen conditions may quickly alternate with high-oxygen conditions in photosynthetically active aggregates (Alldredge and Cohen, 1987). A higher abundance of hypoxic and anoxic aggregates can be assumed to occur in low-oxygen than in high-oxygen environments (Ploug et al, 1997; Ploug, 2001; Klawonn et al, 2015)
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