Metabolic preference of nitrate over oxygen as an electron acceptor in foraminifera from the Peruvian oxygen minimum zone

Abstract

Benthic foraminifera populate a diverse range of marine habitats. Their ability to use alternative electron acceptors—nitrate (NO3−) or oxygen (O2)—makes them important mediators of benthic nitrogen cycling. Nevertheless, the metabolic scaling of the two alternative respiration pathways and the environmental determinants of foraminiferal denitrification rates are yet unknown. We measured denitrification and O2 respiration rates for 10 benthic foraminifer species sampled in the Peruvian oxygen minimum zone (OMZ). Denitrification and O2 respiration rates significantly scale sublinearly with the cell volume. The scaling is lower for O2 respiration than for denitrification, indicating that NO3− metabolism during denitrification is more efficient than O2 metabolism during aerobic respiration in foraminifera from the Peruvian OMZ. The negative correlation of the O2 respiration rate with the surface/volume ratio is steeper than for the denitrification rate. This is likely explained by the presence of an intracellular NO3− storage in denitrifying foraminifera. Furthermore, we observe an increasing mean cell volume of the Peruvian foraminifera, under higher NO3− availability. This suggests that the cell size of denitrifying foraminifera is not limited by O2 but rather by NO3− availability. Based on our findings, we develop a mathematical formulation of foraminiferal cell volume as a predictor of respiration and denitrification rates, which can further constrain foraminiferal biogeochemical cycling in biogeochemical models. Our findings show that NO3− is the preferred electron acceptor in foraminifera from the OMZ, where the foraminiferal contribution to denitrification is governed by the ratio between NO3− and O2.

Stable aerobic and anaerobic coexistence in anoxic marine zones

“…Results suggest that the ratio of aerobic to anaerobic respiration will generally decrease from the periphery to the core of an anoxic zone. This is consistent with the observations of foraminifera in the Peruvian AMZ [64]. The perspective here suggests that the inferred "preference" for NO À 3 utilization by the cells in conditions where oxygen is rarely supplied constitutes the consequence, not the dictation, of the outcome of the metabolic competition among a facultative population.…”

Multidecadal Changes in Marine Subsurface Oxygenation Off Central Peru During the Last ca. 170 Years

“…Within this last group, Bolivina seminuda shows a steep growing dominance from the inner shelf toward the upper slope, along the increase of nitrate and nitrite in the overlying waters. This pattern is consistent with the nitrate or nitrite respiration of B. seminuda (Piña-Ochoa et al, 2010;Glock et al, 2019). Bolivina pacifica is in general less abundant and follows B. seminuda's distribution, but is absent in the inner shelf sulfidic sediments.…”

“…On the other hand, postoxic sediments with preserved OM and available dissolved nitrate are found under lower organic input. B. seminuda and associated species thriving in the upper slope appear to be associated with availability of dissolved nitrate in the bottom waters (Glock et al, 2019;Cardich et al, unpublished results). The association of B. tenuata with δ 15 N exists in B-13 ( Figure 5A) but not in B-6 ( Figure 5B), giving more evidence that the intensity of WCD over the shelf and its effect on reducing conditions is mediated by local export production.…”

“…These samples were taken during IMARPE surveys and during the Meteor 92 cruise. We also include other studies from the upper margin of central Peru: Pérez et al (2002) and Mallon et al (2012) to better represent the fauna zonation of benthic foraminifera.…”

Sediment release of dissolved organic matter to the oxygen minimum zone off Peru

“…Stramma et al, 2008). Remineralization of organic matter under anoxia induces nitrogen (N)loss by denitrification and anammox as well as dissimilatory nitrate reduction to ammonium (DNRA) in the water column and sediments off the coast of Peru (Kalvelage et al, 2013;Arévalo-Martínez et al, 2015;Dale et al, 2016;Sommer et al, 2016;Glock et al, 2019). Although organic matter remineralization is classically assumed to be limited by the absence of oxygen (Demaison and Moore, 1980), recent studies report similar abilities of marine microbes to degrade organic matter in oxygenated surface waters and within OMZs (Pantoja et al, 2009;Maßmig et al, 2019a, b), suggesting that other factors, such as the quality of organic matter may regulate microbial activity within OMZs (Pantoja et al, 2009;Le Moigne et al, 2017).…”