Controls of H2S, Fe2 +, and Mn2 + on Microbial NO3–-Reducing Processes in Sediments of an Eutrophic Lake

Abstract

Understanding the biogeochemical controls on the partitioning between nitrogen (N) removal through denitrification and anaerobic ammonium oxidation (anammox), and N recycling via dissimilatory nitrate (NO 3 −) reduction to ammonium (DNRA) is crucial for constraining lacustrine N budgets. Besides organic carbon, inorganic compounds may serve as electron donors for NO 3 − reduction, yet the significance of lithotrophic NO 3 − reduction in the environment is still poorly understood. Conducting incubation experiments with additions of 15 N-labeled compounds and reduced inorganic substrates (H 2 S, Fe 2+ , Mn 2+), we assessed the role of alternative electron donors in regulating the partitioning between the different NO 3 −-reducing processes in ferruginous surface sediments of Lake Lugano, Switzerland. In sediment slurry incubations without added inorganic substrates, denitrification and DNRA were the dominant NO 3 −-reducing pathways, with DNRA contributing between 31 and 46% to the total NO 3 − reduction. The contribution of anammox was less than 1%. Denitrification rates were stimulated by low to moderate additions of ferrous iron (Fe 2+ ≤ 258 µM) but almost completely suppressed at higher levels (≥1300 µM). Conversely, DNRA was stimulated only at higher Fe 2+ concentrations. Dissolved sulfide (H 2 S, i.e., sum of H 2 S, HS − and S 2−) concentrations up to ∼80 µM, strongly stimulated denitrification, but did not affect DNRA significantly. At higher H 2 S levels (≥125 µM), both processes were inhibited. We were unable to find clear evidence for Mn 2+-supported lithotrophic NO 3 − reduction. However, at high concentrations (∼500 µM), Mn 2+ additions inhibited NO 3 − reduction, while it did not affect the balance between the two NO 3 − reduction pathways. Our results provide experimental evidence for chemolithotrophic denitrification or DNRA with Fe 2+ and H 2 S in the Lake Lugano sediments, and demonstrate that all tested potential electron donors, despite the beneficial effect at low concentrations of some of them, can inhibit NO 3 − reduction at high concentration levels. Our findings thus imply that the concentration of inorganic electron donors in lake sediments can act as an important regulator of both benthic denitrification and DNRA rates, and suggest that they can exert an important control on the relative partitioning between microbial N removal and N retention in lakes.

The role of organic matter and microbial community controlling nitrate reduction under elevated ferrous iron concentrations in boreal lake sediments

“…Although, the microbial reactions between Fe 2+ and NO 3 − have been known known to exist for more than two decades (Straub et al, 1996), the role of microbial Fe 2+ oxidation with NO 3 − reduction in natural sediments has remained unclear. In an experiment with microbial mass from Lake Lugano sediments, N 2 production was stimulated at low Fe 2+ enrichment levels (Fe 2+ ≤ 258 μM) but almost completely suppressed at higher levels (≥ 1300 μM) (Cojean et al, 2020). Because of the difference in experimental set ups, the results are not directly comparable, but stimulation of denitrification by Fe 2+ at St1 and St3 appears to be in line with the results from Lake Lugano.…”

“…Chemolithotrophic DNRA has also been thought to be negligible in freshwater ecosystem because of low availability of sulfides (Fenchel & Blackburn, 1979), which presence has been shown to favor DNRA over denitrification (Brunet & Garcia-Gil, 1996;Christensen et al, 2000). However, the recent discovery of Fe 2+ driven DNRA in lake sediments (Robertson & Thamdrup, 2017;Cojean et al, 2020) suggests that DNRA could be an important process especially because transport of Fe to boreal lakes has been increasing during the past decades (Weyhenmeyer et al, 2014). Despite the increasing evidence of the linkage between N and Fe cycles, we found negligible DNRA rates compared to denitrification in this NO 3 − and Fe rich lake, even under elevated Fe 2+ and NO 3 − availability in the sediment layers, where conditions should have been otherwise favorable for Fe 2+ driven DNRA.…”

Direct O<sub>2</sub> control on the partitioning between denitrification and dissimilatory nitrate reduction to ammonium in lake sediments

“…Potential rates of denitrification and DNRA under true anoxic conditions were quantified at both sampling sites in October 2017. Anammox rates were measured in a previous study at different times of the year, and their contribution to the total fixed-N removal was always less than 1 %, thus negligible with respect to other processes (Cojean et al, 2019). Indeed, in all experiments, denitrification and DNRA were the main benthic N transformation processes with an essentially equal contribution to the total nitrate reduction (≈ 0.1 µmol N g −1 wet sed.…”

“…We ensured that measured DNRA rates were not underestimated due to 15 NH + 4 loss through adsorption on mineral surfaces. Previous results (Cojean et al, 2019) demonstrate that adsorption of ambient or tracer ammonium does not occur at detectable levels in the dilute sediment slurries. Ammonium consumption by nitrifiers in the presence of O 2 , however, might slightly affect quantification of DNRA rates.…”

Impact of drought on water quality in the Youssef Ben Tachafine dam (Souss-Massa region, Morocco)

“…Under these conditions of total and early deep water anoxia, sediment plays an important role in water quality [13,14]. The acceleration of the eutrophication phenomenon causes the degradation of the organoleptic quality of the waters of this reservoir by the appearance of hydrogen sulphide, manganese and iron with all their negative consequences on the various uses of the water including in particular the production of drinking water [15][16][17].…”