Aerobic Microbial Respiration In Oceanic Oxygen Minimum Zones

Abstract

Oxygen minimum zones are major sites of fixed nitrogen loss in the ocean. Recent studies have highlighted the importance of anaerobic ammonium oxidation, anammox, in pelagic nitrogen removal. Sources of ammonium for the anammox reaction, however, remain controversial, as heterotrophic denitrification and alternative anaerobic pathways of organic matter remineralization cannot account for the ammonium requirements of reported anammox rates. Here, we explore the significance of microaerobic respiration as a source of ammonium during organic matter degradation in the oxygen-deficient waters off Namibia and Peru. Experiments with additions of double-labelled oxygen revealed high aerobic activity in the upper OMZs, likely controlled by surface organic matter export. Consistently observed oxygen consumption in samples retrieved throughout the lower OMZs hints at efficient exploitation of vertically and laterally advected, oxygenated waters in this zone by aerobic microorganisms. In accordance, metagenomic and metatranscriptomic analyses identified genes encoding for aerobic terminal oxidases and demonstrated their expression by diverse microbial communities, even in virtually anoxic waters. Our results suggest that microaerobic respiration is a major mode of organic matter remineralization and source of ammonium (~45-100%) in the upper oxygen minimum zones, and reconcile hitherto observed mismatches between ammonium producing and consuming processes therein.

Fig 1. Physicochemical zonation and rates of microbial respiration in the OMZs off Namibia and Peru.

(a-c) Namibian shelf (station 252, 111m). (d-f) Peruvian coastal OMZ (station 807, 115 m). (g-i) Offshore Peruvian OMZ (station 3, 4697 m). Dashed lines indicate the upper OMZ boundary (O₂ ≤15 μmol l^-1). Previously determined rates of aerobic and anaerobic NH₄ ⁺ oxidation [14,24,25] are tenfold magnified. Please note the differences in scale between stations. *Chlorophyll a concentrations in panel b in relative units.

Fig 2. Abundance of genes and transcripts encoding for terminal respiratory oxidases in the ETSP OMZ.

(a, b) Abundance of low-affinity (cytochrome c oxidase) and high-affinity (cytochrome bd and cbb₃ oxidase) aerobic oxidases in the Peruvian OMZ (station 3). (c-f) Abundance and expression of cytochrome oxidase genes in the OMZ off Chile during cruise MOOMZ-1 [34]. Taxonomic affiliations of cytochrome oxidases are shown on domain, phylum or class level if represented by at least 5% of oxidase-coding sequences. Exact abundance and expression levels as well as taxonomic assignments of the individual types of cytochrome oxidases are given in S3 Table.

Fig 3. Oxygen sensitivity of aerobic respiration and OMZ particle size distributions.

(a) O₂ sensitivity assays in the Namibian (station 225) and Peruvian OMZ (stations 13 and 28) during cruises M76 and M77-3, respectively. Oxygen consumption rates are given as percentages of the highest rate observed (= 100%) among all O₂ treatments (see S2 Table for absolute rates). Error bars for O₂ consumption rates are standard errors calculated from linear regression. Isolines (grey) indicate diffusion-limited respiration rates inside aggregates of 0.01–25 mm in diameter. A detailed description of how aggregate-size-dependent rates were calculated is included in the S1 File. (b) Vertical distribution of particle volumes (20 m bins) for six size classes between 0.06 and 5.32 mm (ESD) in the central Peruvian OMZ (12.62°S/77.55°W) during cruise M93. Color shading indicates diffusion limitation of aerobic respiration inside particles. For clarity, particles >5.32 mm are not depicted here. A more general overview of particle size distributions in the ETSP OMZ is given in S2 Fig.