Sediments From a Seasonally Euxinic Coastal Ecosystem Show High Nitrogen Cycling Potential

Abstract

Coastal ecosystems are susceptible to eutrophication and deoxygenation, which may alter their nitrogen cycle dynamics. Here, we investigated the microbial nitrogen cycling potential in the sediment of a seasonally euxinic coastal ecosystem (Lake Grevelingen, NL) in winter and summer. Activity tests revealed ammonium (NH₄ ⁺) oxidation potential with maximum potential rates up to 53 μmol g^-1 day^-1, even in anoxic sediment layers. A nitrifying microbial community was present in both oxic and anoxic sediment sections (up to 1.4% relative abundance). Nitrate (NO₃ ^-), nitrite (NO₂ ^-), and nitrous oxide (N₂O) reduction potential were prominent across all sediment sections, with the highest potential rates (167 μmol NO₃ ^-∙g^-1 day^-1) in the surface sediment in summer. Denitrification (79.3%-98.4%) and dissimilatory nitrate reduction to ammonium (DNRA; 1.6%-20.7%) were the major NO₃ ^- removal pathways, as supported by the detection of the narG/napA, nirK/nirS, norB, nosZ and nrfA/otr genes in all sediment sections. The DNRA contribution increased with depth and with the addition of electron donors, such as monomethylamine. Anaerobic ammonium oxidation (anammox) was not detected in these eutrophic sediments. Combined, our results show that there is high potential for nitrogen removal in eutrophic coastal ecosystems, which may help further restoration measures.

Keywords: DNRA; coastal; denitrification; euxinic; nitrification; nitrogen cycle; sediment.

FIGURE 1

Concentrations of dissolved NH₄ ⁺ (green), NO₂ ⁻ (orange), NO₃ ⁻ (red) and headspace N₂O (blue) over time in bottle incubations with sediment from Lake Grevelingen from March at a depth of 10–15 cm supplemented with (A) no substrate (treatment 1) and (B) 0.5 mM NH₄Cl (treatment 2) after exposure to ambient air. Error bars indicate the standard deviation of the triplicate measurements for each sediment‐treatment combination.

FIGURE 2

Maximum potential rates (μmol g⁻¹ day⁻¹) of NH₄ ⁺ (green) and NO₂ ⁻ (orange) oxidation at different sediment depths in March and September, as measured in duplicate bottles amended with 0.5 mM NH₄Cl and 0.25 mM NaNO₂ (treatments 2 and 3, respectively). The maximum potential rate of NO₂ ⁻ oxidation was calculated based on the formation of NO₃ ⁻. NA: Treatment not included for incubations with this sediment section.

FIGURE 3

Concentrations of dissolved NH₄ ⁺ (green), NO₂ ⁻ (orange), NO₃ ⁻ (red), and headspace N₂O (blue) over time in incubations with sediment from Lake Grevelingen from March at a depth of 10–15 cm supplemented with (A) no substrate (treatment 7) and (B) 0.5 mM NaNO₃ (treatment 8). Error bars indicate the standard deviation of the triplicate measurements for each sediment‐treatment combination.

FIGURE 4

Maximum potential rates (μmol g⁻¹ day⁻¹) of NO₃ ⁻ (red), NO₂ ⁻ (orange) and N₂O (blue) reduction at different sediment depths in March and September, as measured in duplicate incubation bottles amended with 0.5–1 mM NaNO₃ (treatment 8), 0.25 mM NaNO₂ + 0.5 mM NH₄Cl + 2% CO₂ (treatment 9), and 0.5% N₂O (treatment 10), respectively. NA: Treatment not included for incubations with this sediment section.

FIGURE 5

Relative contribution of DNRA and denitrification to NO₃ ⁻ reduction at different sediment depths in March and September as measured in bottles amended with 0.5–1 mM NaNO₃ (treatment 8). Error bars indicate the standard deviation between duplicate bottles.

FIGURE 6

The relative abundance of genes belonging to the nitrification, denitrification, DNRA and anammox processes in reads per million (RPM) at the different depths and seasons studied as determined by metagenome sequencing. Left panel: March. Right panel: September.