Revising the nitrogen cycle in the Peruvian oxygen minimum zone

Abstract

The oxygen minimum zone (OMZ) of the Eastern Tropical South Pacific (ETSP) is 1 of the 3 major regions in the world where oceanic nitrogen is lost in the pelagic realm. The recent identification of anammox, instead of denitrification, as the likely prevalent pathway for nitrogen loss in this OMZ raises strong questions about our understanding of nitrogen cycling and organic matter remineralization in these waters. Without detectable denitrification, it is unclear how NH(4)(+) is remineralized from organic matter and sustains anammox or how secondary NO(2)(-) maxima arise within the OMZ. Here we show that in the ETSP-OMZ, anammox obtains 67% or more of NO(2)(-) from nitrate reduction, and 33% or less from aerobic ammonia oxidation, based on stable-isotope pairing experiments corroborated by functional gene expression analyses. Dissimilatory nitrate reduction to ammonium was detected in an open-ocean setting. It occurred throughout the OMZ and could satisfy a substantial part of the NH(4)(+) requirement for anammox. The remaining NH(4)(+) came from remineralization via nitrate reduction and probably from microaerobic respiration. Altogether, deep-sea NO(3)(-) accounted for only approximately 50% of the nitrogen loss in the ETSP, rather than 100% as commonly assumed. Because oceanic OMZs seem to be expanding because of global climate change, it is increasingly imperative to incorporate the correct nitrogen-loss pathways in global biogeochemical models to predict more accurately how the nitrogen cycle in our future ocean may respond.

Fig. 1.

Hydrochemical properties along an east–west transect at 12°S: distribution of (A) nitrate, (B) nitrite, (C) ammonium, (D) N*, (E) phosphate, and (F) oxygen plotted against neutral density (kg m⁻³). Black-filled circles denote discrete sampling depths at Stations 1 to 7. Station numbers circled in red indicate sampling stations from which the parallel ¹⁵N-rate measurements and gene expression data presented in the current study were obtained.

Fig. 2.

Vertical distribution of oxygen (A) and the various measured ¹⁵N rates along with corresponding functional gene expression (B–E) at Stations 2 (inner shelf), 4 (mid-shelf), and 7 (offshore). (B) Anammox rates (bars) with Scalindua (red) and denitrifier (green) cd₁-containing nitrite reductase (nirS) gene expression. (C) net ¹⁵NO₃⁻ reduction rates (bars) with membrane-bound (narG) (red) and periplasmic (napA) (green) nitrate reductase gene expression. (D) net ¹⁵NH₄⁺ oxidation rates (bars) with expression of crenarchaeal, β-, and γ- proteobacterial ammonia monooxygenase (amoA) genes (red, green, and blue, respectively). (E) net ¹⁵N DNRA rates (bars) with cytochrome c nitrite reductase gene (nrfA) expression (red). n.d. denotes nondetectable reaction rate. Arrows indicate approximate depths of nitrite maxima. Please note the different scales used for the measured rates in these plots.

Fig. 3.

A revised nitrogen cycle in the Peruvian OMZ. Anammox (yellow) has been found to be the predominant pathway for nitrogen loss and was coupled directly to nitrate reduction (red) and aerobic ammonia oxidation (the first step of nitrification, green) for sources of NO₂⁻. The NH₄⁺ required by anammox originated from DNRA (blue) and remineralization of organic matter via nitrate reduction and probably from microaerobic respiration. Microaerobic conditions, at least in the upper part of the OMZ, were suggested by the occurrence of nitrification, which diminishes in importance from shelf to open ocean and in the lower OMZ. In contrast, NH₄⁺ production caused by nitrate reduction and DNRA became increasingly important in the lower OMZ and offshore. Assim (gray) denotes assimilation. Remin (brown) denotes remineralization. Nitrogen fixation (gray dashes) might be coupled spatially to nitrogen loss near the OMZ but has not been assessed in this study.