Microbial oceanography of anoxic oxygen minimum zones

Abstract

Vast expanses of oxygen-deficient and nitrite-rich water define the major oxygen minimum zones (OMZs) of the global ocean. They support diverse microbial communities that influence the nitrogen economy of the oceans, contributing to major losses of fixed nitrogen as dinitrogen (N(2)) and nitrous oxide (N(2)O) gases. Anaerobic microbial processes, including the two pathways of N(2) production, denitrification and anaerobic ammonium oxidation, are oxygen-sensitive, with some occurring only under strictly anoxic conditions. The detection limit of the usual method (Winkler titrations) for measuring dissolved oxygen in seawater, however, is much too high to distinguish low oxygen conditions from true anoxia. However, new analytical technologies are revealing vanishingly low oxygen concentrations in nitrite-rich OMZs, indicating that these OMZs are essentially anoxic marine zones (AMZs). Autonomous monitoring platforms also reveal previously unrecognized episodic intrusions of oxygen into the AMZ core, which could periodically support aerobic metabolisms in a typically anoxic environment. Although nitrogen cycling is considered to dominate the microbial ecology and biogeochemistry of AMZs, recent environmental genomics and geochemical studies show the presence of other relevant processes, particularly those associated with the sulfur and carbon cycles. AMZs correspond to an intermediate state between two "end points" represented by fully oxic systems and fully sulfidic systems. Modern and ancient AMZs and sulfidic basins are chemically and functionally related. Global change is affecting the magnitude of biogeochemical fluxes and ocean chemical inventories, leading to shifts in AMZ chemistry and biology that are likely to continue well into the future.

Fig. 1.

Location and characteristic biogeochemical profiles of AMZs. (A) Global map of major AMZs derived from the distribution of waters with ≤2 μM oxygen and ≥0.5 μM nitrite based on data from the US National Oceanographic Database (NODC) and from Thamdrup et al. (3) and Canfield et al. (17) (observations from inland seas, such as the Baltic Sea, have not been included). Note that oxygen measurements reported in the NODC database are based on traditional standard techniques, with detection limits in the low micromolar range, and not the new highly sensitive STOX sensors. (B) Cartoon of characteristic profiles in AMZs illustrate the accumulation of nitrite within the AMZ, due to the anaerobic microbial process of nitrate reduction, and the high N₂O concentrations at the boundaries (oxyclines). The figure also shows the presence of high microbial cell abundance and of a secondary chlorophyll-a maximum due to picocyanobacteria within the AMZ waters.

Fig. 2.

Profiling float observations of oxygen, particle backscattering at 700 nm (an index of particle abundance), and salinity in the upper 800 m of the AMZ of the ETSP. Oxygen-deficient conditions associated with a high particle load persist over several months within the AMZ but are occasionally interrupted by instructions of waters with higher oxygen concentrations and lower salinities. (Inset) Trajectory of the float, which profiled each 3 d during the 9 mo in 2007. Data are from Whitmire et al. (28).

Fig. 3.

Key patterns in metabolic protein-coding transcripts and gene sequences in the AMZ off Iquique, Chile. (A) Metatranscriptome sequencing reveals diverse transcripts matching the genomes or metagenomes of functionally diagnostic taxa. (*Pelagibacter-like transcripts encoding enzymes of heterotrophic aerobic respiration are mostly restricted to oxycline depths. Pelagibacter-like transcripts at the AMZ core primarily encode transport-related proteins.) (B) Relative transcriptional activity of genera representing distinct functional clades varies with depth. Reactions (boxed) are based on the characterized metabolisms of closely related taxa. Colors match those in A. (C) Genes for dissimilatory sulfur and nitrogen metabolism are transcribed in depth-specific patterns. amo, ammonia monooxygenase (amoABC subunits combined); apr, APS reductase (subunits aprAB and membrane anchor aprM combined); dsr, dissimilatory sulfite reductase pathway (all dsr genes combined); hzo, hydrazine oxidoreductase; narG, nitrate reductase; nirS/nirK, NO-forming nitrite reductase; norB, NO reductase; nosZ, N₂O reductase; sox, sulfur oxidation pathway (all sox genes combined). The scale differs for the amo gene. (D) Metagenome (DNA) sequences matching the aprA gene suggest a diverse AMZ community of both sulfur oxidizers and sulfate reducers. Abundances are shown as percentages of the total number of protein-coding sequences in shotgun-sequenced community RNA (A–C) and DNA (D) datasets. Protein-coding genes are arrayed along the x axis in A, with per-gene transcript abundance normalized to kilobases of gene length. Figures are based on samples collected from the ETSP AMZ in June 2008 (29) (A–C) and January 2010 (17) (D).

Fig. 4.

Major microbial biogeochemical processes in the AMZ core and in the adjacent oxic waters. The heterotrophic processes within the core are anaerobic and include sulfate reduction, nitrate reduction to nitrite, nitrate reduction to ammonium (DRNA), and denitrification to N₂ gas. These processes oxidize organic matter and liberate ammonia for use by anammox bacteria. The sulfide produced by sulfate reducers is oxidized again to sulfate through autotrophic microbial metabolisms with nitrate and nitrite as electron acceptors. Sulfur metabolisms are given with blue arrows, and nitrogen metabolisms are given with black arrows, except those coupled to sulfur (sulfide plus S-intermediate compounds), which are given by red arrows. Anammox is also an autotrophic microbial process. Ammonium oxidation (nitrification) is a significant aerobic microbial process in the oxic waters surrounding the AMZ core and most probably occurring during oxygen intrusions into the core. Nitrogen fixation is the energy-intensive fixation of N₂ gas to organic nitrogen (the oxidation state of ammonium) and is accomplished by a wide range of microorganisms, including sulfate reducers, sulfur oxidizers, and cyanobacteria. It occurs in both the oxygenated upper layers of AMZ settings and in the AMZ core.

Fig. 5.

Cartoon shows the development of different chemistries depending on the relative mix of different driving parameters, including rates of primary production, rates of nitrogen fixation, and the availability of oxygen. Oxygen availability could imply oxygen limitation as observed in modern anoxic basins, such as the Black Sea, or the limitation of oxygen availability as occurred during times in the geological past when atmospheric oxygen concentrations were lower. If oxygen availability becomes limiting enough, rates of primary production and nitrogen fixation may take a secondary role in determining the development of water column chemistry. Based on information provided in the text, OMZs include those regions of the global ocean where oxygen is decreased as a result of respiration but where nitrite does not accumulate (except a nitrite maximum that typically occurs in well-oxygenated, near-surface waters as a result of nitrification). Modern measurements suggest that nitrite accumulation occurs at oxygen levels of less than 50 nM. AMZs occur as oxygen falls below about 50 nM and nitrite begins to accumulate.