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 (NO ₃ ⁻) or oxygen (O ₂)—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 O ₂ respiration rates for 10 benthic foraminifer species sampled in the Peruvian oxygen minimum zone (OMZ). Denitrification and O ₂ respiration rates significantly scale sublinearly with the cell volume. The scaling is lower for O ₂ respiration than for denitrification, indicating that NO ₃ ⁻ metabolism during denitrification is more efficient than O ₂ metabolism during aerobic respiration in foraminifera from the Peruvian OMZ. The negative correlation of the O ₂ respiration rate with the surface/volume ratio is steeper than for the denitrification rate. This is likely explained by the presence of an intracellular NO ₃ ⁻ storage in denitrifying foraminifera. Furthermore, we observe an increasing mean cell volume of the Peruvian foraminifera, under higher NO ₃ ⁻ availability. This suggests that the cell size of denitrifying foraminifera is not limited by O ₂ but rather by NO ₃ ⁻ 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 NO ₃ ⁻ is the preferred electron acceptor in foraminifera from the OMZ, where the foraminiferal contribution to denitrification is governed by the ratio between NO ₃ ⁻ and O ₂.