Ammonium Uptake by Phytoplankton Regulates Nitrification in the Sunlit Ocean

Abstract

Nitrification, the microbial oxidation of ammonium to nitrate, is a central part of the nitrogen cycle. In the ocean’s surface layer, the process alters the distribution of inorganic nitrogen species available to phytoplankton and produces nitrous oxide. A widely held idea among oceanographers is that nitrification is inhibited by light in the ocean. However, recent evidence that the primary organisms involved in nitrification, the ammonia-oxidizing archaea (AOA), are present and active throughout the surface ocean has challenged this idea. Here we show, through field experiments coupling molecular genetic and biogeochemical approaches, that competition for ammonium with phytoplankton is the strongest regulator of nitrification in the photic zone. During multiday experiments at high irradiance a single ecotype of AOA remained active in the presence of rapidly growing phytoplankton. Over the course of this three day experiment, variability in the intensity of competition with phytoplankton caused nitrification rates to decline from those typical of the lower photic zone (60 nmol L−1 d−1) to those in well-lit layers (<1 nmol L−1 d−1). During another set of experiments, nitrification rates exhibited a diel periodicity throughout much of the photic zone, with the highest rates occurring at night when competition with phytoplankton is lowest. Together, the results of our experiments indicate that nitrification rates in the photic zone are more strongly regulated by competition with phytoplankton for ammonium than they are by light itself. This finding advances our ability to model the impact of nitrification on estimates of new primary production, and emphasizes the need to more strongly consider the effects of organismal interactions on nutrient standing stocks and biogeochemical cycling in the surface of the ocean.

Changes in Marine Prokaryote Composition with Season and Depth Over an Arctic Polar Year

“…The almost total disappearance of the Thaumarchaeota from the photic zone during the summer months ( Figure 5) is therefore suggestive of photoinhibition of ammonia oxidation (Guerrero and Jones, 1996;Murray et al, 1998;Mincer et al, 2007;Schleper and Nicol, 2010;Merbt et al, 2012), or has been more recently posited, a sensitivity to reactive oxygen species produced as a result of photosynthesis (Tolar et al, 2016). The reasons may however be multifactorial and it is thought that the Archaea may also be outcompeted by phytoplankton (Murray et al, 1998;Ward, 2000Ward, , 2005Church et al, 2003;Herfort et al, 2007;Smith et al, 2014) and Bacteria (which are much more active in the uptake of the labile bloomproduced substrates Alonso-Sáez et al, 2008;Kalanetra et al, 2009), or even subjected to selective viral infection (Labonté et al, 2015). The proportional abundance of Thaumarchaeota has been correlated with ammonium concentrations (Herfort et al, 2007;Kirchman et al, 2007) and their peak abundance in winter surface waters has been hypothesized to result from mixing with deep water masses in Antarctic seas (Kalanetra et al, 2009;Grzymski et al, 2012); however, in areas of the Arctic Ocean where the water column tends to remain stratified during the winter (Forest et al, 2011), recent data suggests that the increase is in fact due to growth and proliferation of surface water Thaumarchaeota populations in situ (Alonso-Sáez et al, 2012).…”

Diverse, uncultivated bacteria and archaea underlying the cycling of dissolved protein in the ocean

“…δ 15 N precision, determined by repeat analysis of the reference materials, was found to be 0.15‰ for the entire data set. Resultant δ 15 N NOx data were used to calculate rates of NH 4 + oxidation or labeled protein remineralization using previously described methods (Smith et al, 2014) derived from the original equations laid out by Dugdale and Goering (1967).…”

Enzyme‐level interconversion of nitrate and nitrite in the fall mixed layer of the Antarctic Ocean

“…Coupled with the significant competitive advantage that phytoplankton have over nitrifiers for NH 4 + [Ward, 1985;Smith et al, 2014] The NO 2 À produced from NH 4 + oxidation can either be assimilated with an isotope effect of~0‰ [Waser et al, 1998] or be oxidized to NO 3 À with an inverse isotope effect of À12.8‰ [Casciotti, 2009]. If most of the NO 2 À is assimilated, the δ 15 N of the unassimilated NO 2 À will remain effectively unchanged, at either À5‰ or in the range of À24‰ to À19‰.…”