Production of oceanic nitrous oxide by ammonia-oxidizing archaea

Abstract

<jats:p>Abstract. The recent finding that microbial ammonia oxidation in the ocean is performed by archaea to a greater extent than by bacteria has drastically changed the view on oceanic nitrification. The numerical dominance of archaeal ammonia-oxidizers (AOA) over their bacterial counterparts (AOB) in large parts of the ocean leads to the hypothesis that AOA rather than AOB could be the key organisms for the oceanic production of the strong greenhouse gas nitrous oxide (N2O) which occurs as a by-product of nitrification. Very recently, enrichment cultures of marine ammonia-oxidizing archaea have been described to produce N2O. Here, we demonstrate that archaeal ammonia monooxygenase genes (amoA) were detectable throughout the water column of the Eastern Tropical North Atlantic (ETNA) and Eastern Tropical South Pacific Oceans (ETSP). Particularly in the ETNA, maxima in abundance and expression of archaeal amoA genes correlated with the N2O maximum and the oxygen minimum, whereas the abundances of bacterial amoA genes were negligible. Moreover, selective inhibition of archaea in seawater incubations from the ETNA decreased the N2O production significantly. In studies with the only cultivated marine archaeal ammonia-oxidizer Nitrosopumilus maritimus SCM1, we provide the first direct evidence for N2O production in a pure culture of AOA, excluding the involvement of other microorganisms as possibly present in enrichments. N. maritimus showed high N2O production rates under low oxygen concentrations comparable to concentrations existing in the oxycline of the ETNA, whereas the N2O production from two AOB cultures was comparably low under similar conditions. Based on our findings, we hypothesize that the production of N2O in tropical ocean areas results mainly from archaeal nitrification and will be affected by the predicted decrease in dissolved oxygen in the ocean.</jats:p>

Significance of archaeal nitrification in hypoxic waters of the Baltic Sea

“…In the globally expanding marine oxygen minimum zones and in other oxygen-deficient systems, archaea are prominently embedded in the cycles of carbon (C) and nitrogen (N) (Lö scher et al, 2012;Stewart et al, 2012), consistent with the recognition of these systems as hot spots for chemolithoautotrophs . Concerted dissimilatory microbial processes successively transform fixed nitrogen species into dinitrogen gas (Lam and Kuypers, 2011) and autotrophy promotes the fixation of inorganic carbon into biomass (Herndl et al, 2005).…”

“…AOA and AOB belong to different domains with specific physiologies, and levels of functional gene expression may not be equally extrapolated to the process rates, and hence alternative experimental approaches are required to confirm this hypothesis. In the case of ammonia oxidation, rate measurements can be linked with archaeal vs bacterial contributions by the use of inhibitors specific for either Bacteria or Archaea (Lö scher et al, 2012;Yokokawa et al, 2012).…”

Nitrogen cycling driven by organic matter export in the South Pacific oxygen minimum zone

“…Nucleic acids were extracted using a Qiagen DNA/RNA All prep Kit following the manufacturers protocol with minor modifications 50 . Functional genes for archaeal and 315 bacterial (β-/γ-proteobacterial) NH 3 oxidation (arch-amoA and β-/γ-amoA, respectively), anammox (hzo1 and 2), denitrification (denitrifier-nirS) and DNRA (nrfA) were PCRamplified as described in Löscher et al 49 .…”

Structure of denitrifying communities reducing N2O at suboxic waters off northern Chile and Perú

“…For example, N 2 O concentrations as high as 172.7 nM off Peru (Codispoti et al 1992) and 124 nM off northern Chile (Farías et al 2007) were registered in subsurface water (below the mixed layer), constituting a large N 2 O source estimated in ~12.78 Gg (Cornejo & Farías 2012). N 2 O can be produced by nitrification and partial denitrification of bacteria and Archaea (Cabello et al 2004, Castro-González & Farías 2004, Santoro et al 2011, Loescher et al 2012 as well as nitrifier denitrification (Shaw et al 2006), processes which can co-occur at oxyclines and pycnoclines, while dissimilative N 2 O to N 2 reduction at suboxic or anoxic condition takes place only by complete denitrification (Bange et al 2010).…”