The 'oxygen' in oxygen minimum zones

Abstract

Aerobic processes require oxygen, and anaerobic processes are typically hindered by it. In many places in the global ocean, oxygen is completely removed at mid-water depths forming anoxic oxygen minimum zones (A-OMZs). Within the oxygen gradients linking oxygenated waters with A-OMZs, there is a transition from aerobic to anaerobic microbial processes. This transition is not sharp and there is an overlap between processes using oxygen and those using other electron acceptors. This review will focus on the oxygen control of aerobic and anaerobic metabolisms and will explore how this overlap impacts both the carbon and nitrogen cycles in A-OMZ environments. We will discuss new findings on non-phototrophic microbial processes that produce oxygen, and we focus on how oxygen impacts the loss of fixed nitrogen (as N₂ ) from A-OMZ waters. There are both physiological and environmental controls on the activities of microbial processes responsible for N₂ loss, and the environmental controls are active at extremely low levels of oxygen. Understanding how these controls function will be critical to understanding and predicting how fixed-nitrogen loss in the oceans will respond to future global warming.

FIGURE 1

Cartoon showing typical depth distribution of biogeochemical properties in A‐OMZ waters. Typical concentration ranges of chemical species and chl a in A‐OMZs are also given.  Source: Figure inspired by Ulloa et al. (2012)

FIGURE 2

Carbon oxidation rates with depth in A‐OMZ waters from northern Chile/southern Peru together with t depth distributions of oxygen and nitrite. Measured rates of denitrification and nitrate reduction were converted into rates of carbon oxidation. The rates of carbon oxidation required to supply the ammonium needs of anammox are based on measured anammox rates and an assumed 5.8/1 stoichiometry between carbon mineralized to ammonium liberated in A‐OMZ waters. Also shown are expected rates of carbon mineralization based on different models of carbon flux attenuation with depth from sediment traps. See text for details

FIGURE 3

Cartoon showing the oxygen sensitivity of aerobic (blue) and anaerobic (orange) microbial processes. While anammox bacteria can metabolize under low micromolar concentrations of oxygen, microbial ammonium and nitrite oxidation are very efficient at very low‐oxygen concentrations removing these substrates from anammox bacteria at oxygen levels where they would otherwise be active. Thus, in the BoB OMZ, oxygen is sufficiently low that anammox bacteria should be active, but sufficiently high that nitrite and ammonium are effectively oxidized, so there is no anammox activity. In the upper A‐OMZ oxygen concentrations are below detection, and the oxygen range depicted here is an educated guess. Still, anammox activity, while measurable, is restricted due to active ammonium oxidation with oxygen likely coming from oxygenic phototrophic cyanobacteria and possibly N. maritimus. In the A‐OMZ core oxygen concentrations are likely even lower, and an oxygen source is apparently restricted. Here, anammox bacteria operate to their full potential. While physiological possible through a great range of oxygen concentrations, denitrification plays a minor role in both N₂ production and carbon mineralization in A‐OMZ environments

FIGURE 4

(A) Model results from a 3‐box OMZ model showing the evolution of oxygen in the OMZ box with different values of K _m for oxic respiration. Insert shows results on a log scale. (B) As in A, but with variable proportions of the organic matter oxidized with Michaelis–Menten control, with the rest oxidized with zero‐order O₂ control; y = 1 reflects full Michaelis–Menten control. K _m is set at 0.4 μM O₂. See text for details