Global rates of water-column denitrification derived from nitrogen gas measurements

Abstract

Biologically available nitrogen (N) limits phytoplankton growth over much of the ocean. The rate at which N is removed from the contemporary ocean by denitrifying bacteria is highly uncertain 1-3 . Some studies suggest that N losses exceed inputs 2,4-6 ; others argue for a balanced budget 3,7,8 . Here, we use a global ocean circulation model to simulate the distribution of N 2 gas produced by denitrifying bacteria in the three main suboxic zones in the open ocean. By fitting the model to measured N 2 gas concentrations, we infer a globally integrated rate of water-column denitrification of 66 ± 6 Tg N yr −1 . Taking into account isotopic constraints on the fraction of denitrification occurring in the water column versus marine sediments, we estimate that the global rate of N loss from marine sediments and the oceanic water column combined amounts to around 230 ± 60 Tg N yr −1 . Given present estimates of N input rates, our findings imply a net loss of around 20 ± 70 Tg of N from the global ocean each year, indistinguishable from a balanced budget. A balanced N budget, in turn, implies that the marine N cycle is governed by strong regulatory feedbacks.The loss of N in the ocean occurs as bacteria reduce N to N 2 gas through a combination of heterotrophic denitrification and anaerobic ammonium oxidation (hereafter collectively termed denitrification). Suboxic conditions in which O 2 is scarce enough to favour these processes are found in three principal locations in the water column: the Arabian Sea, the eastern tropical South Pacific (ETSP) and the eastern tropical North Pacific (ETNP; Fig. 1). Denitrification rates in these areas estimated from nitrate deficits and water-mass age tracers yield a global rate of watercolumn denitrification in the range of 60-90 Tg N yr −1 (refs 9-14), but recently rates as large as 150 Tg N yr −1 have been proposed 2 . Denitrification also occurs in suboxic pore waters of sediments throughout the ocean, but the rates are spatially heterogeneous and have been measured at only a handful of sites 15 , precluding a direct global estimate. However, the global rate of sedimentary N loss (primarily denitrification, but also a small burial of organic N) is constrained by the isotopic ratio of mean ocean nitrate to be one to four times as large as the rate of denitrification in the suboxic water column 6,16,17 . Estimates of the total rate of N loss in the ocean therefore inherit and amplify the uncertainty in the rate of denitrification in suboxic waters, yielding a combined rate of about 270 Tg N yr −1 (ref.3) to more than 400 Tg N yr −1 (refs 2,6). These rates far exceed the estimated global rate of N fixation, which is in the range of 100-160 Tg N yr −1 (refs 7,18). The apparent deficit is partially offset by riverine and atmospheric inputs of about 40-125 Tg N yr −1 (refs 3,15). Still, if the upper end of the denitrification-rate estimates are correct, the ocean must be rapidly losing fixed N.

Enhancement of anammox by the excretion of diel vertical migrators

“…Without DVM, the model produces ∼60 TgN·y −1 of water column fixed N removal, partitioned as 73% denitrification and 27% anammox, consistent with previous results (2,29), and with the expected stoichiometry of anaerobic reactions (10). As the proportion of active versus particle export (f dvm ) increases, anammox becomes more important, so that, for f dvm = 0.1, 0.2, and 0.5, when averaged globally, anammox amounts to, respectively, 34%, 38%, and 51% of N 2 production.…”

“…anammox | denitrification | oxygen minimum zone | diel vertical migration W ater column oxygen minimum zones (OMZs), where oxygen concentrations plummet to submicromolar levels (1), are responsible for approximately one-third of the total removal of fixed nitrogen from the oceans (2,3). Several processes mediated by specialized prokaryotes convert fixed inorganic nitrogen (NH 4 + , NO 2 − , and NO 3 − ) to N 2 in anoxic waters.…”

Biogenic nitrogen gas production at the oxic–anoxic interface in the Cariaco Basin, Venezuela

“…These observations support the conclusion of Chang et al (2010) that measurements of N xs 2 provide a useful means for estimating N-loss rates in oxygen minimum zones, and that N xs 2 concentrations can be used to validate N-loss rates in marine systems (see DeVries et al, 2012) where DIN deficits or N* estimates are affected by non-Redfield N : P ratios. Some potential problems of using DIN deficits calculated from SRP include variable N : P ratios, the scavenging of SRP by redox species such as iron and manganese oxides, or (specifically for Cariaco) the accumulation of SRP and ammonium below the oxic-anoxic interface Zhang and Millero, 1993).…”

“…This estimate is based in part on the accumulation of nitrate deficit (with respect to the Redfield N : P ratio [N * ]; Gruber and Sarmiento, 1997) as a function of the residence time of oxygen-depleted 268 E. Montes et al: Biogenic nitrogen gas production at the oxic-anoxic interface water masses (Gruber, 2004;Sarmiento, 1997, 2002). Whether this imbalance in the nitrogen inventory is due to an underestimation of nitrogen fixation or an overestimation of N-loss is a topic of current debate (Capone and Knapp, 2007;Codispoti, 2007;Deutsch et al, 2007;Dalsgaard et al, 2012;DeVries et al, 2012). More recently, the removal of fixed nitrogen has been estimated by measuring excess N 2 (N xs 2 , with respect atmospheric equilibrium), such as in the Arabian and Baltic Seas and the eastern tropical South Pacific (Chang et al, 2010;Devol et al, 2006;Löffler et al, 2011), in order to reduce uncertainties associated with regional variations in N : P ratios and the complexities of DIN conversion pathways.…”

“…More recently, the removal of fixed nitrogen has been estimated by measuring excess N 2 (N xs 2 , with respect atmospheric equilibrium), such as in the Arabian and Baltic Seas and the eastern tropical South Pacific (Chang et al, 2010;Devol et al, 2006;Löffler et al, 2011), in order to reduce uncertainties associated with regional variations in N : P ratios and the complexities of DIN conversion pathways. DeVries et al (2012) used N xs 2 measurements coupled with a global circulation model to estimate oceanic water-column N-loss rates. In anoxic waters of the Black Sea, interannual variations in N xs 2 were attributed to changes in the downward flux of organic matter from phytoplankton blooms (Fuchsman et al, 2008).…”