Biologically useful nitrogen is delivered to the upper ocean from the depths by vertical transport processes — or such was the received wisdom. In fact, bacteria that convert atmospheric nitrogen may be just as crucial.
Next to light, nitrogen is the main factor that limits the biological productivity of primary producers in the sea. All photosynthetic organisms need nitrogen to grow, yet most cannot use it in its simplest form, molecular N2. But biologically useful, ‘fixed’ forms of nitrogen are scarce over much of the illuminated upper ocean. Writing in Global Biogeochemical Cycles, Capone et al.1 highlight a little-considered mechanism for supplying the upper ocean with nitrogen — bacteria that fix molecular nitrogen from the atmosphere.
The scarcity of fixed nitrogen in the illuminated ocean results from a continuous loss of nitrogen to the dark, abyssal ocean, resulting primarily from the sinking of organic nitrogen (Fig. 1). If this lost nitrogen were not recycled to the upper ocean, primary production in the sea would plummet within a few years. So identifying and quantifying the replenishment mechanism is essential for understanding marine productivity. Furthermore, as the biologically induced cycling of nitrogen is closely coupled to the cycling of carbon, these processes are also of prime relevance for understanding the oceanic carbon cycle, and hence atmospheric carbon dioxide levels.
Over much of the ocean, upward mixing and transport of nitrate (NO3−) constitutes the primary supply pathway (Fig. 1). Nitrate is the dominant form of fixed nitrogen and is generated in the dark ocean from the mineralization of sinking organic nitrogen. In most regions of the tropical and subtropical ocean, however, vertical transport is insignificant, and mixing tends to be inefficient. Surprisingly, biological productivity in these regions is often much higher than might be expected from the poor vertical supply of nitrate, implying the involvement of other, unidentified nitrogen sources2. One candidate source was the biological fixation of molecular N2 from the atmosphere, but based on the measurements then available, this was generally considered unimportant.
Capone and colleagues1 now demonstrate, in the most exhaustive and comprehensive study so far, that over large regions of the tropical and subtropical Atlantic, biological N2 fixation is indeed substantial. In fact, it provides the ecosystem of the illuminated ocean with a source of nitrogen that rivals the vertical supply of nitrate. The contribution cements a paradigm shift that has been occurring over the past decade in models of marine nitrogen cycling (see ref. 3 for an example).
The authors focused1 on the contribution of Trichodesmium, a cyanobacterium that is the most conspicuous and best-studied marine N2 fixer. In a painstaking effort, they measured the N2 fixation rates of gently collected colonies of Trichodesmium at more than 150 stations during six cruises to the tropical and subtropical Atlantic. Averaged over all stations and integrated over the depth of the upper ocean at each station, the annual N2 fixation rate was 87 ± 14 millimol of N per square metre. This value is of the same order of magnitude as the vertical flux of nitrate into the upper ocean in the region studied.
What makes Capone and colleagues' study particularly compelling is that they estimated N2 fixation rates using an array of independent methods, each with their own strengths and weaknesses. This results in an unprecedented level of confidence in the estimates obtained. In particular, the authors used measurements of the ratio of the two stable isotopes of nitrogen, 14N and 15N, to confirm that about half of the organic nitrogen in the surface ocean stems from atmospheric N2 (Fig. 1).
Assuming that their estimate of the biological N2 fixation rate is representative of most of the tropical and subtropical North Atlantic, Capone et al. estimate1 that Trichodesmium annually adds between 1.6 and 2.4 teramol (a teramol is 1012 mol) of fixed nitrogen to this region, almost an order of magnitude larger than earlier estimates of N2 fixation over the whole Earth4. This extrapolation is consistent with several indirect geochemical estimates5,6,7 of the biological fixation rate that are based on anomalies in the relative abundance of nitrate and phosphate (PO43−); these ranged, with one exception7, from 2 to 6 teramol of nitrogen per year. As these estimates are integrated explicitly over time and space, they are less prone to the difficulties associated with extrapolating local rate measurements. They are, however, based on a number of assumptions — some of which, such as the exact amount of nitrogen and phosphorus required by primary producers that do not fix N2 — are difficult to verify.
Capone et al. also show that their extrapolation is broadly consistent with the value inferred from a region-wide analysis of the 15N-isotopic mass balance. To determine the rate of N2 fixation, they combine their estimate derived from the nitrogen isotopic ratio — that some 50% of the organic nitrogen in the upper ocean comes from atmospheric N2 — with an estimate for the turnover rate of organic nitrogen. This value is in fact somewhat larger than the value the authors find based on Trichodesmium. But the discrepancy might be explained by the fact that mass-balance analysis includes all sources of N2 fixation, including recently discovered single-cell cyanobacteria8 and a cyanobacterium that lives symbiotically within a marine diatom9.
Not only does N2 fixation provide a pathway for adding new nitrogen to the illuminated ocean, but it is also the main source of fixed nitrogen to the ocean as a whole. On long timescales, this source could compensate for the effects of denitrification, a respiratory process that converts fixed nitrogen back to N2 (Fig. 1). It has been suggested10 that past estimates of the loss of fixed nitrogen from the ocean need to be revised substantially upwards. If the rate of N2 fixation is as low as was estimated two decades ago, this would imply that the present-day marine nitrogen budget is seriously out of balance. The much higher estimates of N2 fixation proposed on the basis of geochemical methods had brought the budget back to near-balance5, but without direct measurements that conclusion remained tentative. The new convergence of estimates for the Atlantic provides good evidence that N2 fixation in the ocean may occur on a large enough scale to balance losses of fixed nitrogen.
A fascinating corollary is the question of how marine N2 fixation and denitrification are coupled. With both processes occurring at such high rates, the residence time of fixed nitrogen in the ocean can be only a few thousand years. This would require a well-established balance between the two processes in order to avoid large swings in the biological productivity of the oceans. Because all organisms need phosphorus as well as nitrogen to survive, the marine phosphorus content almost certainly plays an important role here. Room for surprises in the marine nitrogen cycle remains, but one conclusion is clear: that cycle is much more dynamic than was thought only a few years ago.
Capone, D. G. et al. Glob. Biogeochem. Cycles 19, GB2024, doi:10.1029/2004GB002331 (2005).
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