Research Article: Aerobic Microbial Respiration In Oceanic Oxygen Minimum Zones

Date Published: July 20, 2015

Publisher: Public Library of Science

Author(s): Tim Kalvelage, Gaute Lavik, Marlene M. Jensen, Niels Peter Revsbech, Carolin Löscher, Harald Schunck, Dhwani K. Desai, Helena Hauss, Rainer Kiko, Moritz Holtappels, Julie LaRoche, Ruth A. Schmitz, Michelle I. Graco, Marcel M. M. Kuypers, Zhe-Xue Quan.


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.

Partial Text

Most of the organic matter in the world’s oceans is remineralized via aerobic respiration by heterotrophic microorganisms. Only when oxygen (O2) becomes scarce, microorganisms use thermodynamically less favourable electron acceptors, predominantly nitrate (NO3-), for the oxidation of organic matter [1]. Large, permanently O2-depleted water masses favouring NO3- respiration, so-called oxygen minimum zones (OMZs), are found in association with tropical and subtropical upwelling systems [2]. These regions are characterized by high surface productivity and thus strong O2 depletion via degradation of sinking organic matter at mid-depth, exacerbated by limited O2 replenishment [3]. Nitrate respiration in OMZs accounts for ~20–40% of global oceanic nitrogen (N) loss [4]. The N-deficient OMZ waters (relative to phosphorus) are eventually upwelled and result in largely N-limited surface primary production at low latitudes [5]. Hence, despite a combined volume of only ~1% (O2 ≤20 μmol l-1) of the global ocean [1], OMZs play an important role in regulating phytoplankton nutrient availability, and thus carbon (C) fixation in the oceans.

In summary, extensive rate measurements combined with metagenomic as well as metatranscriptomic analyses show widespread potential for microaerobic respiration in the Namibian and South Pacific OMZs. Microorganisms inhabiting the OMZ use high-affinity respiratory oxidases to exploit traces amounts of O2, brought in via intrusions of oxygenated surface waters, lateral advection of O2-bearing water masses, or produced locally by low-light adapted phytoplankton. At the upper OMZ boundary, where micromolar O2 concentrations persist, microaerobic respiration is the major mode of organic matter degradation and primary source of NH4+ for aerobic NH4+ oxidation and N-loss via anammox. The close spatial coupling of aerobic and anaerobic pathways in (O2-carrying) OMZ waters is likely facilitated by formation of O2-reduced microniches in sinking aggregates.