Temporal dynamics of nitrogen loss in the coastal upwelling ecosystem off central Chile: Evidence of autotrophic denitrification through sulfide oxidation

Abstract

Coastal upwelling areas are highly productive marine systems in which the development of oxygen-depleted conditions and the availability of diverse electron donors (e.g., organic matter, NH z 4 , H 2 S) favor the processes involved in nitrogen (N) loss. We characterize the temporal and vertical variability of anammox and denitrification over the continental shelf off central Chile (36.5uS), through 15 N and 13 C tracer experiments, including amendments with H 2 S and S 2 O 2{ 3 along with measurements of 15 N 2 and 15 N 2 O production and oceanographic variables during a year (2009 to 2010). Restricted to the bottom waters, both anammox and denitrification contributed similarly (, 500 nmol N 2 L 21 d 21 ) to N loss during spring, while a marked decrease in the activity of these processes occurred in summer (103 and 14 nmol N 2 L 21 d 21 for anammox and denitrification, respectively). During fall, denitrification was the only contributor to the observed nitrogen deficit (894 nmol N 2 L 21 d 21 ). Interestingly, a substantial increase in the rates of denitrification (, 1200 nmol N 2 L 21 d 21 ) and dark 13 C assimilation were observed after the addition of H 2 S, indicating an autotrophic contribution to denitrification, which could be fueled in situ by H 2 S emitted from sediments or produced in the water column. The observed patterns seem to be controlled (stimulated or inhibited) by the availability of oxygen, organic matter, and H 2 S. This study establishes the magnitude and co-occurrence of the different processes responsible for N removal in the coastal upwelling system of central Chile. This linkage of the nitrogen, carbon, and sulfur cycles is relevant to a global climate change scenario.

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

“…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).…”

“…2b, f). Increases in the organic matter availability, measured as particulate organic carbon during the development of the upwelling season in both the oxycline and bottom waters, have been previously reported for this coastal system (Graco et al, 2001;Galán et al, 2014). The influence of organic matter on denitrification activity has been extensively documented in OMZ waters (e.g.…”

“…These conditions, coupled with the presence of already O 2 -deficient waters, and greater availability of electron donors and acceptors (as a result of the advection of inorganic substrates, local organic matter respiration, and autotrophic redox reactions), create steep gradients for O 2 and other chemicals, with the establishment of hypoxic-anoxic conditions at middle-bottom depths. 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).…”

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

“…However, during our study, anammox activity was only detected at 80 m, at a rate of 2 nmol·L −1 N·d −1 , and the process was also previously only observed close to the sedimentwater interface at this site (33,55). Hence, we do not expect anammox to contribute significantly to total nitrite oxidation here.…”

Diversity and Transcriptional Levels of RuBisCO Form II of Sulfur-Oxidizing γ-Proteobacteria in Coastal-Upwelling Waters with Seasonal Anoxia

“…These electron donors should become available during the austral springsummer season, arising from sulfate reduction taking place in the anoxic sediments (Thamdrup and Canfield, 1996) or within the water column itself (Canfield et al, 2010): As shown by Galán et al (2014) in the same study area (Station 18), the inventory (mmol m −2 ) of H 2 S during the 2009-2011 period was higher in spring-summer (upwelling) compared to fall-winter (downwelling), for the three layer analyzed; Surface (0-25 m, 3.1 mmol m −2 ), oxycline (26-65 m, 4.2 mmol m −2 ) and bottom (66-90 m, 3.8 mmol m −2 ). Also, they demonstrated experimentally that the amendment of water samples with H 2 S (under anoxic conditions) and not thiosulfate boosted the dissolved inorganic carbon assimilation and N 2 O production by the microbial community at bottom waters (90 m depth), stressing the importance of O 2 in modulating the abundance and biogeochemical relevance of chemolithoautotrophic metabolisms in these marine ecosystems (Stevens and Ulloa, 2008;Lavik et al, 2009;Walsh et al, 2009;Canfield et al, 2010;Ulloa et al, 2012;Wright et al, 2012;Glaubitz et al, 2013;Schunck et al, 2013).…”