Dinitrogen fixation in aphotic oxygenated marine environments

Eyal Rahav,Hila Elifantz,Barak Herut,Ilana Berman-Frank,Natalia Belkin,Margaret R Mulholland,Sarah Ohayon,Edo Bar-Zeev

doi:10.3389/fmicb.2013.00227

Abstract

We measured N2 fixation rates from oceanic zones that have traditionally been ignored as sources of biological N2 fixation; the aphotic, fully oxygenated, nitrate (NO−3)-rich, waters of the oligotrophic Levantine Basin (LB) and the Gulf of Aqaba (GA). N2 fixation rates measured from pelagic aphotic waters to depths up to 720 m, during the mixed and stratified periods, ranged from 0.01 nmol N L−1 d−1 to 0.38 nmol N L−1 d−1. N2 fixation rates correlated significantly with bacterial productivity and heterotrophic diazotrophs were identified from aphotic as well as photic depths. Dissolved free amino acid amendments to whole water from the GA enhanced bacterial productivity by 2–3.5 fold and N2 fixation rates by ~2-fold in samples collected from aphotic depths while in amendments to water from photic depths bacterial productivity increased 2–6 fold while N2 fixation rates increased by a factor of 2 to 4 illustrating that both BP and heterotrophic N2 fixation were carbon limited. Experimental manipulations of aphotic waters from the LB demonstrated a significant positive correlation between transparent exopolymeric particle (TEP) concentrations and N2 fixation rates. This suggests that sinking organic material and high carbon (C): nitrogen (N) micro-environments (such as TEP-based aggregates or marine snow) could support high heterotrophic N2 fixation rates in oxygenated surface waters and in the aphotic zones. Indeed, our calculations show that aphotic N2 fixation accounted for 37 to 75% of the total daily integrated N2 fixation rates at both locations in the Mediterranean and Red Seas with rates equal or greater to those measured from the photic layers. Moreover, our results indicate that that while N2 fixation may be limited in the surface waters, aphotic, pelagic N2 fixation may contribute significantly to new N inputs in other oligotrophic basins, yet it is currently not included in regional or global N budgets.

Highlights

In many of the world’s oceans, the availability of dissolved inorganic nitrogen (N) controls primary production in surface waters (Falkowski, 1997; Karl et al, 2002)
At the Levantine Basin (LB) station, temperatures and salinities of the aphotic layer were significantly lower than those measured for the Gulf of Aqaba (GA) station, averaging 16.1 ± 1.1◦C and 39.1 ± 0.1, respectively (Figures 1C,D; Table 2), while within the photic layer temperature and salinities averaged 23 ± 5◦C and 39.3 ± 0.2, respectively, during the stratified period (Figures 1C,D; Table 2)
Most marine N2 fixation studies neglect the potential contribution of biological N2 fixation in deep, aphotic, NO3-rich waters that comprise the majority of the world’s oceans (Karl et al, 2002; Zehr and Ward, 2002). This is likely because phototrophic and cyanobacterial diazotrophs have an ecological advantage in surface waters where productivity is often limited by the availability of fixed nitrogen yet there is sufficient energy to drive both photosynthetic C uptake and the costly process of N2 fixation (Howarth et al, 1988; Postgate, 1998; Karl et al, 2002)

Summary

Introduction

In many of the world’s oceans, the availability of dissolved inorganic nitrogen (N) controls primary production in surface waters (Falkowski, 1997; Karl et al, 2002). This is because the most abundant form of N in the oceans, dinitrogen (N2), is biologically unavailable to the majority of organisms that reside there. Subgroups of prokaryotic organisms (diazotrophs) fix N2 and convert it to ammonium via the nitrogenase enzyme complex This biological process is an important source of “new” N to oceanic systems that can stimulate production and growth of microbial communities. The balance between N2 fixation and denitrification (including annamox) is considered to critically impact the oceanic inventory of bioavailable nitrogen and primary productivity (PP) in the oceans (Gruber and Galloway, 2008)

Methods

Results

Conclusion