Aerobic Microbial Respiration In Oceanic Oxygen Minimum Zones

PLoS One. 2015 Jul 20;10(7):e0133526. doi: 10.1371/journal.pone.0133526. eCollection 2015.

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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Ammonium Compounds / metabolism*
  • Bacteria, Aerobic / classification
  • Bacteria, Aerobic / genetics
  • Bacteria, Aerobic / metabolism
  • Bacteria, Anaerobic / classification
  • Bacteria, Anaerobic / genetics
  • Bacteria, Anaerobic / metabolism
  • Electron Transport Complex IV / genetics
  • Electron Transport Complex IV / metabolism
  • Gene Expression
  • Metagenome / genetics
  • Namibia
  • Oceans and Seas
  • Organic Chemicals / metabolism
  • Oxidation-Reduction
  • Oxidoreductases / genetics
  • Oxidoreductases / metabolism
  • Oxygen / metabolism*
  • Oxygen Consumption*
  • Peru
  • Seawater / chemistry
  • Seawater / microbiology*
  • Transcriptome / genetics

Substances

  • Ammonium Compounds
  • Organic Chemicals
  • Oxidoreductases
  • Electron Transport Complex IV
  • Oxygen

Associated data

  • SRA/SUB910041
  • SRA/SUB910044
  • SRA/SUB910045
  • SRA/SUB910046

Grants and funding

The authors were supported by the following funders: TK, GL, CL, HS, DKD, HH, RK, JLR, RS, MIG, MMK: DFG-funded Sonderforschungsbereich 754 “Climate-Biogeochemistry Interactions in the Tropical Ocean” (www.sfb754.de); TK, GL, MMJ, MH, MMMK: Max Planck Society (www.mpg.de); TK: Canada Excellence Research Chair in Ocean Science and Technology (http://www.cerc.gc.ca/chairholders-titulaires/wallace-eng.aspx); NPR: European Research Council (http://erc.europa.eu), grant 267233, and Danish Council for Independent Research: Natural Sciences (http://ufm.dk/en/research-and-innovation/councils-and-commissions/the-danish-council-for-independent-research/the-council-1/the-danish-council-for-independent-research-natural-sciences), grants 10-083140 and 272-07-0057. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.