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.

Highlights

  • The quantity of nitrogen (N) supplied to the sunlit layers of the ocean regulates levels of primary production and phytoplankton community composition [1]

  • The detection of ammonia monooxygenase genes and mRNA transcripts associated with three major groups of marine ammonia oxidizing microorganisms (AOM), ‘Water Column A’ (WCA) and ‘Water Column B’ (WCB) ecotypes of the ammonia-oxidizing archaea (AOA) and betaproteobacterial ammonia oxidizing bacteria (b-ammonia-oxidizing bacteria (AOB)), confirmed that putatively light-sensitive AOM were present and active at the start of our experiments (Table 1)

  • These data revealed that the WCA ecotype of AOA comprised the majority of ammonia monooxygenase (amoA) gene (79%620%) and transcript (88%65%) pools in all samples (Table 1)

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Summary

Introduction

The quantity of nitrogen (N) supplied to the sunlit layers of the ocean regulates levels of primary production and phytoplankton community composition [1]. The occurrence of nitrification in the photic zone complicates these paradigms by providing a regenerated source of NO32 Accounting for this process is needed in order to make accurate estimates of new primary production [2], and the strength of the ocean’s biological pump [1]. Despite decades of observations of nitrification in the photic zone [3,4,5,6,7,8], the impacts of this process on global estimates of new production were assessed only recently From this recent meta analysis, it was suggested that between 18 and 33% of NO32 in the photic zone is regenerated within it by nitrification, causing modelbased estimates of oceanic new production to be 1.5 to 3-fold higher than actual [9]. The primary sources of uncertainty in these estimates are the poor spatiotemporal coverage in the global data set [9], and the fact that we have yet to establish strong relationships between ecological and environmental factors and nitrification

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