Phosphate Depletion in the Western North Atlantic Ocean

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Science  04 Aug 2000:
Vol. 289, Issue 5480, pp. 759-762
DOI: 10.1126/science.289.5480.759


Surface waters of the subtropical Sargasso Sea contain dissolved inorganic phosphate (DIP) concentrations of 0.2 to 1.0 nanomolar, which are sufficiently low to result in phosphorus control of primary production. The DIP concentrations in this area (which receives high inputs of iron-rich dust from arid regions of North Africa) are one to two orders of magnitude lower than surface levels in the North Pacific (where eolian iron inputs are much lower and water column denitrification is much more substantial). These data indicate a severe relative phosphorus depletion in the Atlantic. We hypothesize that nitrogen versus phosphorus limitation of primary production in the present-day ocean may be closely linked to iron supply through control of dinitrogen (N2) fixation, an iron-intensive metabolic process. Although the oceanic phosphorus inventory may set the upper limit for the total amount of organic matter produced in the ocean over geological time scales, at any instant in geological time, oceanic primary production may fall below this limit because of a persistent insufficient iron supply. By controlling N2 fixation, iron may control not only nitrogen versus phosphorus limitation but also carbon fixation and export stoichiometry and hence biological sequestration of atmospheric carbon dioxide.

Photosynthetic carbon fixation and subsequent settling of particulate fixed carbon to the ocean's interior represent a biological carbon pump that regulates atmospheric CO2 concentrations and climate over geological time scales (1). This carbon pump is largely controlled by the availability of the major nutrients: nitrogen (N) and phosphorus (P). Nutrient enrichment experiments in the Pacific suggest that phytoplankton growth is limited by available N (2). Nutrient distributions in the modern ocean indicate that upward fluxes of inorganic nutrients from the deep ocean are depleted in N relative to P in relation to the elemental requirements of eukaryotic photoautotrophs growing at their maximum rates (3). This nitrate deficit has been attributed to a slight imbalance between N2 fixation and denitrification (4, 5), caused by an iron limitation of N2 fixation (6–8). With ample iron, increased N2 fixation should drive oceanic ecosystems toward phosphorus limitation as occurs in most lakes (9) and has been proposed for the ocean during glacial periods (6). This conceptual model, however, contradicts the prevailing view of geochemists that net N2 fixation and the balance between N2 fixation and denitrification are ultimately set by riverine input of phosphorus, not by eolian iron supply (10). To help resolve this controversy, we compared dissolved nitrate plus nitrite (DNN) and dissolved inorganic phosphate (DIP) distributions in iron-replete waters of the western North Atlantic subtropical gyre, where little denitrification exists, with those in iron-poor regions of the subtropical North Pacific, where water column denitrification is substantial, to examine the influence of iron supply on N versus P limitation. Subnanomolar concentrations of DIP in the surface seawater of the western North Atlantic were observed with a highly sensitive MAGIC method for P analysis (11).

In a transect from the seasonally stratified Sargasso Sea near Bermuda to permanently stratified waters farther south, we observed no measurable changes in surface concentrations of dissolved organic phosphorus [DOP = total dissolved phosphorous (TDP) − DIP] (Table 1), which accounted for 94 to 99% of the total phosphorus. DIP concentrations in surface waters decreased from 3.9 nM in surface waters near Bermuda to an average value of 0.4 nM in the region of permanent stratification (Fig. 1). This DIP concentration is only ∼4% of the mean DIP in nutrient-depleted waters of the North Pacific gyre (Fig. 1, Table 1), indicating a relative DIP depletion in the Sargasso Sea (12, 13).

Figure 1

Surface (∼0.5 m) DIP concentrations along a transect from 31.67°N, 64.17°W to 26.10°N, 70.00°W in the Sargasso Sea in March 1998 are compared with those in the North Pacific gyre. –•–, western North Atlantic in March 1998; –▪–, North Pacific in November 1997 (37); ○, North Pacific near Hawaii in 1991–97 (HOT 11-85) (35); ▴, Pacific near Hawaii in November 1998.

Table 1

A comparison of euphotic zone biogeochemical parameters between North Atlantic and North Pacific gyres.

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Phosphate depletion in Sargasso Sea surface waters can be attributed to the high ratio of DNN to DIP of 20 to 32 in the upper nutricline relative to the planktonic 16 N:1 P ratio (14) (Fig. 2). This high nutrient source N:P ratio causes available P to be depleted before N by algal growth after upward nutrient injections into the euphotic zone through advection or diffusion. The scenario is different in the North Pacific where the DNN versus DIP supply ratio from the upper nutricline to the euphotic zone is lower than the N:P ratio of 16 in plankton (Fig. 2), resulting in an N-limited condition with algal growth (2). The difference in N:P ratios between the North Pacific and North Atlantic can be further demonstrated by plots of DNN versus DIP measured at Bermuda Atlantic time-series (BATS) and Hawaii Ocean time-series (HOT) stations for the period July 1998 to July 1999 (Fig. 3). A positive intercept on the DNN axis (N excess in the surface water) and a slope of 17.2 indicate a strong P depletion in the North Atlantic. In contrast, the DNN versus DIP plot for the North Pacific shows a negative intercept (excess phosphate in the surface) and a slope of 15.0, suggesting an N depletion.

Figure 2

Vertical profiles of N:P molar ratios in the Sargasso Sea near Bermuda (31.67°N, 64.17°W) (•) and in the Pacific near Hawaii (HOT USJGOFS Web site (□).

Figure 3

The plot of phosphate versus nitrate measured from BATS ( and HOT ( time series for the period July 1998 to July 1999 (38).

Although the relative N enrichment in the North Atlantic thermocline is probably due to N2 fixation, N depletion in the Pacific must result from enhanced levels of denitrification in low oxygen thermocline waters (15). However, N depletion in the Pacific should promote the growth of N2 fixers that would replenish fixed N, driving the system back toward P limitation, as occurs in most lakes (9). Contemporary N2 fixation in the Pacific appears to be restricted by an insufficient supply of iron (6–8), an important nutrient cofactor for the nitrogenase enzyme.

Microorganisms using N2 as their source of N require at least one order of magnitude more Fe than for growth on nitrate or ammonium (16). Iron limitation of N2fixation has been demonstrated for natural assemblages of diazotrophs in N-deficient lakes (17) and in culture studies with both freshwater cyanobacteria and the dominant marine diazotrophic genus Trichodesmium (8, 18). However, there is currently no convincing direct evidence for iron limitation in natural assemblages of marine diazotrophs. In the North Pacific gyre, the iron flux from below the euphotic zone is too low to support observed rates of phytoplankton growth (19), and most of the iron in surface waters is derived from eolian deposition (20). Areal rates of eolian iron input into surface Pacific waters are 2- to 10-fold lower than in the Sargasso Sea, which receives high inputs of iron-rich dust from northern Africa (20). The higher iron inputs to the North Atlantic subtropical gyre are thought to support higher rates of N2 fixation (21,22).

Other than available iron, do any other factors limit N2 fixation in the North Pacific? Although N2fixers need P for growth and metabolism, the excess DIP detected in surface waters of the North Pacific suggests that P cannot limit N2 fixation in the Pacific. Simple box model calculations (23) show that in the Pacific gyre near Hawaii, the DIP flux from the upper thermocline to the euphotic zone is ∼30% higher than that needed to meet the growth demands of phytoplankton (based on the upward nitrate flux and the 16 N:1 P ratio in plankton). Only about half of this extra phosphate is consumed during N2fixation, and the rest (∼15% of the total upward flux) remains unused and is mixed downward as inorganic phosphorus. In contrast, the DIP concentration in the North Atlantic is much lower, suggesting that P is an important limiting factor for N2 fixation as it is in most lakes (9). Other potentially controlling factors such as light, temperature, mixed layer depth, and dissolved oxygen (O2) also cannot explain the lower than expected N2 fixation in the North Pacific. Sunlight, a warm, calm sea surface, and a shallow mixed layer all favor the growth of N2-fixing diazotrophs. These factors, however, are not very different in the two oligotrophic gyres. In fact, in the North Pacific near Hawaii (HOT), the annual mean surface temperature is higher and the mixed layer depth is shallower than in the North Atlantic near Bermuda. This should favor a higher N2fixation rate at HOT. In contrast, estimated gyre-average N2 fixation rates are higher in the North Atlantic than in the North Pacific (Table 1). Although O2 gas is a major inhibitor of nitrogenase activity, Trichodesmium can photosynthesize and fix N2 at the same time (24). At present, there is no good evidence to show that O2 inhibition causes any substantial difference in N2 fixation between the two oceans. Thus, iron remains the most probable factor limiting N2 fixation in the North Pacific, although it remains to be proven by more direct evidence such as in situ Fe addition experiments in the future.

Because the DNN:DIP ratio is higher than the Redfield value (N:P = 16:1) in the Atlantic (Fig. 2), the upward flux of N will be in excess of that needed to support algal growth. Thus, if N is not limiting, why should N2 fixation occur at all in the Atlantic? N2-fixing diazotrophs should not fix N2 for biological production if fixed nitrogen is readily available (25). The answer to the paradox may lie in the preferential conversion of excess inorganic fixed nitrogen (DIN) into biologically refractory dissolved organic nitrogen (DON) by biological nutrient cycling in the stratified surface waters.

A variety of DON and DOP compounds are released into the water column by a number of processes: viral cell lysis, cell disruption during grazing, excretion of digestion waste products, and excretion of oxidatively damaged biomolecules. Many of these compounds, such as amino acids and phospholipids, are biologically labile and are readily reassimilated by microorganisms. However, many others, such as partially oxidized and polymerized biomolecules (humic acids), have complex and varied structures that are not amenable to biological utilization. The N and P in the labile compounds are reassimilated (either directly or after enzymatic degradation, e.g., by phosphatases or deaminases), whereas N and P in the refractory compounds remain in the water. With continued nutrient cycling (26), there is a progressive transfer of N and P from biologically available inorganic pools to increasingly biologically refractory organic ones. There is evidence that the DON in seawater is relatively more “resistant” to microbial assimilation and decomposition than is the DOP (27). Consequently, biological nutrient cycling would cause a greater percentage of DIN than DIP to be converted to refractory organic forms. Thus, although excess DIN is upwelled from below the euphotic zone, the intense nutrient cycling in stratified surface waters could decrease the concentrations of available fixed nitrogen to limiting levels, promoting N2 fixation by diazotrophs.

The cycling of phosphorus from the more biologically labile DOP pool ultimately provides much of the excess P required for N2 fixation even when the N:P ratio in the nutrient flux to the surface is much higher than that found in plankton (28). In addition, some species of N2 fixers such asTrichodesmium can migrate vertically to acquire phosphate from below the mixed layer (29), providing an additional phosphate source for diazotrophic growth. The continued input of recently fixed N by N2 fixation (without an extra P supply from the deep ocean) increases the total dissolved nitrogen to total dissolved phosphorus ratio (TDN:TDP) in the upper ocean of the western North Atlantic to values well above the Redfield ratio (30), as observed in our present data (Table 1).

Our comparison of the nutrient cycles in North Pacific and North Atlantic gyres is consistent with the hypothesis that N versus P limitation in the contemporary ocean is closely linked to eolian Fe supply. Although we cannot directly prove this hypothesis with the currently available data, our results do indicate that the ocean N and P cycles are more complex than predicted by simple models (10). Although enhanced N2 fixation causes P depletion in the more iron-rich North Atlantic, a lack of Fe appears to limit N2 fixation in the N-depleted North Pacific gyre. If indeed N2 fixation in the Pacific is limited by bioavailable Fe, and if inefficient nutrient cycling between DON and DIN promotes N2 fixation in an N-replete condition (N:P > 16), these conditions have important implications for oceanic carbon fixation and export and biological sequestration of atmospheric CO2 over geological time scales.

It has long been argued that because the oceanic residence time for P (∼50,000 years) is much longer than that for N (∼3000 years), P inventory would set the upper limit for the amount of organic matter produced in the ocean over long time scales (10, 31). But, if N2 fixation is controlled by Fe supply, a dearth of iron could lower total primary production below this limit (32). The effect may occur on various time scales. A persistently low iron input could result in an imbalance between N2 fixation and denitrification over long time scales. If this imbalance is small, the oceanic N inventory can vary over time scales much longer than the N residence time. If the imbalance is large, one would expect changes to a new steady state over much shorter time scales (6). In this situation, steady state oceanic N inventory and productivity would be limited by insufficient iron, not by phosphorus. Only when there is enough iron would nitrogen inventory in the ocean be controlled by phosphorus (10, 31).

Although exact information on the oceanic P inventory in the geological past is not known, its long residence time implies that a large (over 30%) change in P inventory on glacial-interglacial time scales is unlikely. However, P control of the N inventory could be affected to some extent by the ability of N2 fixation to adjust oceanic N:P ratio to values exceeding 16 as occurs in the contemporary western North Atlantic Ocean. Although information on the N:P ratio in the ocean over geological time is lacking and the limit for P control of N inventory remains to be understood, it is likely that by controlling N2 fixation, iron has exerted an important role on N inventories and hence biological sequestration of CO2 into the ocean between the present and the Last Glacial Maximum. It has been argued that increased inputs of iron-rich dust to the ocean during drier and windier glacial periods should have increased N2 fixation rates (6, 22). This effect, in combination with decreased denitrification (4, 33), would increase the global oceanic N inventory, resulting in a decrease in atmospheric CO2 from the atmosphere by a stronger oceanic biological pump (7,34). In such a situation, the interrelationships between iron supply, N2 fixation, and phosphate limitation in much of the ocean may have resembled the current situation in the western North Atlantic. Investigating iron versus phosphate limitation of N2 fixation and its role in nutrient cycling in this region may provide a better understanding of oceanic carbon fixation and export during glacial periods and the interrelationship between this interaction and global climate variations.


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