A theoretical basis for a nanomolar critical oxygen concentration

When aerobic microbes deplete oxygen sufficiently, anaerobic metabolisms activate, driving losses of fixed nitrogen from marine oxygen minimum zones. Biogeochemical models commonly prescribe a 1–10 lM critical oxygen concentration for this transition, a range consistent with previous empirical and recent theoretical work. However, the recently developed STOX sensor has revealed large regions with much lower oxygen concentrations, at or below its 1–10 nM detection limit. Here, we develop a simplified metabolic model of an aerobic microbe to provide a theoretical interpretation of this observed depletion. We frame the threshold as O 2, the subsistence oxygen concentration of an aerobic microbial metabolism, at which anaerobic metabolisms can coexist with or outcompete aerobic growth. The framework predicts that this minimum oxygen concentration varies with environmental and physiological factors and is in the nanomolar range for most marine environments, consistent with observed concentrations. Using observed grazing rates to calibrate the model, we predict a minimum oxygen concentration of order 0.1–10 nM in the core of a coastal anoxic zone. We also present an argument for why anammox may be energetically favorable at a higher oxygen concentration than denitrification, as some observations suggest. The model generates hypotheses that could be tested in the field and provides a simple, mechanistic, and dynamic parameterization of oxygen depletion for biogeochemical models, without prescription of a fixed critical oxygen concentration. Anaerobic processes in marine oxygen minimum zones (OMZs) are one of the major loss pathways for fixed nitrogen in the ocean (Ward 2013). With predicted marine deoxygenation and the open question of whether or not OMZs may expand due to global warming (IPCC 2014), establishing theory for the controls on aerobic vs. anaerobic processes is timely. Qualitatively, the mechanisms that form OMZs and lead to fixed nitrogen loss are well understood: in productive areas of the ocean, enhanced aerobic respiration in poorly ventilated subsurface waters depletes oxygen (Devol 2008). When oxygen is sufficiently low, anaerobic metabolisms become energetically competitive pathways, resulting in the accumulation of metabolic products such as nitrogen gas (N2) and nitrous oxide (N2O) (Devol 2008; Ulloa et al. 2012; Wright et al. 2012). In OMZs, two pathways—heterotrophic denitrification and chemoautotrophic anaerobic ammonium oxidation (anammox)—account for the majority of fixed nitrogen loss (Ward 2013). Studies of microbial processes in aquatic oxygen minimum zones have revealed complex biogeochemical habitats (Lam and Kuypers 2011; Wright et al. 2012). Microbial community composition exhibits structure along the oxygen gradient between end-member fully oxic and fully sulfidic environments (Gonsalves et al. 2011; Ulloa et al. 2012; Jayakumar et al. 2013; Hawley et al. 2014). In the oxycline, as oxygen sharply depletes by up to five orders of magnitude (Fig. 1), microbial communities have been observed to be more diverse than in the anoxic cores (Jayakumar et al. 2009; Zaikova et al. 2010; Bryant et al. 2012), although not always (Stevens and Ulloa 2008). Organic matter supply to the subsurface that varies in time and space creates a dynamic oxycline (Ward et al. 2008), which may support this diversity, with competitive exclusion operating progressively with depth as environmental conditions stabilize (Hutchinson 1961). Devol (1978) noted that predicting the oxygen concentration of the switch between aerobic and anaerobic respiration is crucial for accurate OMZ modeling. He conducted an exhaustion curve experiment with bacterial isolates from anoxic marine areas to determine average growth-limiting oxygen concentrations of about 1–4 lM, at the limits of then-current sensors. Many biogeochemical models prescribe a critical oxygen concentration in this range or higher, setting the transition to nitrate reduction and denitrification (e.g., Anderson et al. 2007; Najjar et al. 2007; Deutsch et al. *Correspondence: [email protected] Additional Supporting Information may be found in the online version of this article. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. 1 LIMNOLOGY and OCEANOGRAPHY Limnol. Oceanogr. 00, 2016, 00–00 VC 2016 The Authors Limnology and Oceanography published by Wiley Periodicals, Inc. on behalf of Association for the Sciences of Limnology and Oceanography doi: 10.1002/lno.10461