Phosphorus in the Upper Ocean
Phosphorus (P) is a key element in the growth of microorganisms throughout the worlds oceans. However, little is known about the cycling of this nutrient within coastal and open ocean environments. In general, phytoplankton consume P for their nutrient needs in the form of HPO42-. As a result, scientists have often ignored the other P containing pools. Recent evidence, however, suggests that bacteria may produce an additional source of inorganic P by remineralizing specific P containing organic compounds. Thus, the importance of other P pools can no longer be overlooked. An overview of upper ocean P cycling is given in the following discussion and includes the latest information regarding the chemical composition, bioavailability, and utilization of P within marine ecosystems.
Phosphorus is an essential nutrient utilized by all living organisms. Yet little is known about the role it plays in limiting the growth and distribution of marine phytoplankton (Fig. 1). These microscopic organisms are at the base of the foodweb. Thus, their abundance is a major controlling factor in foodweb composition throughout the oceanic realm. In addition, phytoplankton consume CO2, a greenhouse gas, during photosynthesis and convert the carbon into biomass during growth. During phytoplankton grazing and egestion, zooplankton produce particles that sink below the upper layers of the ocean. Phytoplankton will also sink from the oceans surface via aggregation into larger particles, especially during blooms. In this manner, CO2, in the form of sinking particulate organic matter, is removed from the upper ocean and prevented from interacting with the atmosphere on timescales of 1000 years (Fig. 2). In fact, the oceans may be responsible for the removal of up to 50% of the total anthropogenic CO2 emitted to the atmosphere over the last century (Quay et al., 1992). Sinking organic material also removes pollutants, such as lead, which adsorb to the particles surfaces as they sink through the water column (Wageman & Muir, 1994). By this process, these harmful contaminants are removed from the upper ocean, thereby limiting their potential uptake and bioaccumulation by marine animals, which may eventually be eaten by humans.
So what controls the distribution and growth of phytoplankton in the upper ocean? Physical (e.g., light, temperature, mixed layer depth), chemical (e.g., nutrient concentrations) and biological (e.g., grazing) factors may control phytoplankton growth. The role of phosphorus (P) in nutrient limitation depends on the accessibility of other nutrients and trace elements, such as iron. The availability of these nutrients may in turn vary seasonally and spatially. Unfortunately, understanding which nutrient is limiting growth and when, is complicated. It is necessary to know the nutrient concentration, the form in which it is consumed, and its recycling rate. The relative importance of each of these factors is highly contested within the scientific community (Hecky & Kilham, 1988; Codispoti, 1989; Hutchins & Bruland, 1998). Nonetheless, P has been observed to limit phytoplankton production in regimes ranging from restricted, shallow-marine areas (Krom et al., 1991; Fourqurean et al., 1992) to the open ocean, oligotrophic sites of the North Atlantic and North Pacific (Cotner et al., 1997; Karl et al., 1997).
Even in instances when P is not a limiting factor, increasing anthropogenic P inputs in coastal ecosystems may substantially change the dynamics within these fragile communities. In the heavily populated areas of the worlds coastlines, the anthropogenic inputs of P into the coastal ocean (e.g. from fertilizers in agriculture and detergents) are 10-100 times greater than in pre-industrial times (Caraco, 1993). The consequences of such an increase are numerous and include reducing food web diversity, altering phytoplankton compositions and an increase in the intensity and frequency of red tides (e.g. Nixon, 1993). These transformations could also greatly effect phytoplankton growth and zooplankton grazing, thereby potentially altering the extent of particulate matter production in the coastal ocean. While coastal zones represent less than one tenth of the area of the worlds oceans, they are responsible for 20-40% of the marine particulate matter that is exported from the oceans surface (Eppley & Peterson, 1978). Thus, it is essential that we understand the role that P plays in these environments.
Phosphorus sources, composition, and sinks
P enters the coastal oceans predominantly through rivers. Estimates of the dissolved inorganic P input range from 3-15 x 1010 mol P yr (Delaney, 1998). Atmospheric deposition of P which is soluble in seawater, has been estimated to be significantly lower, between 1-2 x 1010 mol P yr-1 (Duce, 1986). Although small, the atmospheric deposition of P has been increasingly recognized as being important in the open ocean. In the upper water column, inorganic P (HPO42-) is depleted via phytoplankton growth and incorporation into sinking organic matter. In general, this particulate material is remineralized at depth, such that typical profiles show large depth gradients in P concentrations (Fig. 3). P is subsequently brought back into the surface ocean via physical mixing (upwelling and diffusion). These processes are responsible for some of the most productive fishing areas in the world, such as off the coast of Peru.
Currently, the distribution of P in aquatic systems is defined analytically. The dissolved P pool is generally defined as the material that passes through a 0.2 - 0.7 micron diameter filter. In most studies, the dissolved inorganic P pool (presumably as HPO42-) is characterized as the fraction which reacts under acidic conditions (pH < 2) to produce a colored compound, phosphomolybdate (Murphy & Riley, 1962). A number of investigations, however, have found that this treatment will also include an unknown proportion of acid-labile organic compounds, such as sugar phosphates (McKelvie et al., 1995, and references therein). A more appropriate term for the above fraction is soluble reactive phosphorus or SRP. The concentration of total dissolved P (TDP) is generally quantified by using high temperature and/or high pressure in the presence of a strong oxidizing reagent (McKelvie et al., 1995). In this manner, all of the P within a sample is converted to inorganic P and measured using the above phosphomolybdate method. The difference between TDP and SRP is then often referred to as the dissolved organic P (DOP) component. This DOP fraction, however, can also contain non-reactive inorganic compounds, such as polyphosphates. Thus, this fraction should really be termed soluble non-reactive P or SNP.
In coastal marine environments, the SRP pool ranges from 50-100% of the TDP pool (Table 1). In contrast, in the open ocean, SRP is often less than 25% (Karl & Yanagi, 1997). As a result, the importance of identifying the composition of the SNP pool increases with greater distance from shore. Employing a variety of techniques, several classes of SNP compounds have been shown to exist in seawater and include polyphosphates, nucleotides, nucleic acids, phosphonates and monophosphate esters (Solerzano & Strickland, 1968; Karl & Bailiff, 1989; Nawrocki & Karl, 1989; Clark et al., 1998). The actual percent composition of SNP, however, has remained elusive. Recently, Karl and Yanagi (1997) utilized more sensitive techniques to characterize part of the SNP pool within the oligotrophic North Pacific. In the upper water column (<100 m), they found that 66% of the SNP pool was most likely dominated by monophosphate esters, compounds used by phytoplankton for catabolic functions. In contrast, in the deeper waters this fraction decreased to less than 50% of the SNP Pool, indicating preferential remineralization of one component over the other.
Additional evidence for a more bioavailable pool was found using 31P Nuclear Magnetic Resonance (NMR). In this study, Clark and coworkers (1998) found that the high molecular weight fraction of dissolved organic P (1 -100 nm size range), or 19-38% of the total dissolved organic matter, was dominated by phosphorus esters and phosphonates. In plankton phosphonates are associated with phosphonolipids, compounds used in cell structure. Their abundance within marine phytoplankton, however, was almost ten times lower than that found in the dissolved organic phosphorus pool. This result again suggests that other P containing components must be preferentially removed in order to increase the relative concentration of phosphonates in the water column.
The above studies have provided indirect evidence that there is a pool of P within marine systems which is being preferentially eliminated from the water column. How does this removal occur? It is most likely by marine bacteria (Azam, 1998). Bacteria contain enzymes located within the outer membrane that are capable of liberating inorganic P from organic compounds. Alkaline phosphatase and 5 nucleotidase are two of the major enzyme classes found in marine bacteria (Ammerman & Azam, 1985). Over the last several years, laboratory studies have demonstrated that bacteria readily degrade compounds such as monophosphate esters and nucleotides, through the use of these enzymes (Ammerman & Azam, 1985; Bjorkman & Karl, 1994). In fact, using diagnostic enzymatic assays, between 10-50% of the SNP in coastal marine environments could be available (Strickland & Solorzano, 1966; Taft et al., 1977; Kobori & Taga, 1979). The role of bacteria in the cycling of organic matter in the open ocean, where the concentration of SNP relative to TDP is greater, may be even more significant.
Bacteria are the major food source for heterotrophic protozoa. Laboratory studies have demonstrated that through feeding and egestion, protozoa can convert between 20-90% of the P within the bacterial biomass to soluble forms (Anderson et al., 1986; Jurgens & Gude, 1990; Ferrier-Pages & Rassoulzadegan, 1994; Eccleston-Parry & Leadbeater, 1995). The dissolved P produced from these processes is dominated by inorganic P, although organic P is also formed (Anderson et al, 1986; Jurgens & Gude, 1990). The efficiency of P regeneration appears to be dependent on the nutrient-limitation conditions, as well as the phase of protozoan growth (Anderson et al., 1986; Jurgens & Gude, 1990). Controversy still exists over the specific role that protozoans play in nutrient regeneration in natural systems. In fact, there is little direct evidence of the magnitude of bacterial and heterotrophic protozoa remineralization processes and their effect on phytoplankton production in general. In order to constrain their importance, we must also identify the P recycling rates within each of these biological pools.
Phosphorus Recycling Rates
One method of elucidating the timescales over which nutrient recycling occurs is through the use of radioisotopes. In essence, radioisotopes behave as a clock, enabling one to trace processes that have occurred over a well-defined time interval. There are three isotopes of P, one stable, 31P, and two radioactive, 32P (t_ = 14.3 days) and 33P (t_ = 25.3 days). Using 32P and 33P one can monitor the movement of P throughout various biological reservoirs and determine a net age of P within each particular pool. More simply, the ratio of 33P/32P will increase with time due to the differential decay rates of 32P and 33P. These tracers have been used to investigate the recycling rate of P within a number of aquatic regimes. In the past, the use of these isotopes was restricted to incubation experiments in which artificially produced 32P and 33P had been added. The difficulty with such types of research is that they involve significant perturbations to the system of interest. For example, samples are first separated from the ecosystem before incubation. Bottle incubations will, at best, miss sporadic bloom events and provide rate estimates that are only valid for discrete depths and times. Nonetheless, these studies have found that phytoplankton and bacteria rapidly consume P and that there was rapid exchange between inorganic and organic P pools (Perry & Eppley, 1981; Orret & Karl, 1987; Bjorkman & Karl, 1994).
How does this relate to the oceanographic realm? Over the last decade, several researchers have used naturally produced 32P and 33P to directly investigate the cycling of marine P. 32P and 33P are naturally produced in the atmosphere via cosmic ray interactions with atmospheric argon nuclei. Once produced, these isotopes quickly scavenge onto particles and enter the oceans predominantly in rain. While the magnitude of 32P and 33P concentrations will vary dramatically from one rain event to another, studies have shown that in general, the ratio of 33P/32P remains constant (Waser & Bacon, 1995; Benitez-Nelson & Buesseler, 1999a). The advantage of using naturally produced 32P and 33P is that they enable scientists to examine the recycling of P without disturbing the regime of interest. Furthermore, results will integrate over all of the processes that have affected the distribution of 32P and 33P over the prior 20 to 35 days. Preliminary results provided evidence that this type of investigation has enormous potential for understanding P cycling in marine systems (Lal & Lee, 1988; Waser et al., 1996). In general, it was found that the age of P increased as one moved up through the food chain. In the open ocean, the recycling rate of P in zooplankton ranged from 60-70 days (Waser et al., 1996). In contrast, the recycling rate of zooplankton off the coast of California was less than 40 days (Lal & Lee, 1988). Measurement of 32P and 33P in the SRP and SNP pools also indicated that the recycling time of SRP was short, while that of SNP was substantially longer at 6 weeks (Lal & Lee, 1988). Unfortunately, these results had large uncertainties due to the fact that naturally produced 32P and 33P were very difficult to measure in the field.
New advances in technology have enabled a much more comprehensive investigation of P recycling using 32P and 33P. Within the Gulf of Maine, 32P and 33P were measured in SRP, SNP and TDP as well as in various biological pools, including bacteria, throughout the Spring and Summer months (Benitez-Nelson & Buesseler, 1999b). In this study, it was found that dissolved P recycling rates varied significantly from season to season. SRP turnover rates were always high, regardless of the actual concentration. SNP turnover rates, on the other hand, ranged from a month to greater than three months. In the summer, marine bacteria were consuming SNP directly, even though there were measurable amounts of SRP. While the bacterially-consumed SNP was only a small fraction of the total SNP, it is highly likely that this material was younger than the rest of the SNP pool.
What does this all mean in terms in of the cycling of P? The rapid cycling of SRP indicates that low P concentrations can support much higher levels of biological production than previously thought. In contrast, the higher turnover rates of SNP imply that much of this pool is not available for biological uptake. Nonetheless, there is a small fraction of SNP that can be directly utilized by bacteria, indicating that SNP in this regime is made up of a chemically diverse group of compounds that cycle over very different timescales. The observation that bacteria were consuming SNP in the presence of SRP, suggests that bacteria were remineralizing SNP for other nutrient requirements, such as for carbon or nitrogen. Regardless of why, the evidence that bacteria are consuming specific organic P compounds within marine ecosystems is novel and indicates that this process can provide a new source of inorganic nutrients to phytoplankton. Interestingly, there is no evidence that heterotrophic protozoa consume bacteria, or are significantly involved in the P remineralization process.
This study (Benitez-Nelson & Buesseler, 1999b) provided the first direct evidence that marine bacteria may preferentially remineralize specific compounds of SNP. Since this bacterially-utilized SNP fraction was younger than the bulk DOP pool, it most likely consists of P compounds that have rapid recycling rates within marine plankton. These include such compounds as monophosphate esters and nucleotides, which have been shown to be preferentially remineralized in the laboratory. Thus, we now have a clearer picture of the types of P compounds that are available for bacterially-mediated remineralization. Furthermore, 32P and 33P represent an effective technique to further investigate the cycling of P in the oceans.
Changes within the biogeochemical cycle of P have the potential to impact the world in many different ways. Thus, it is essential that we understand the distribution, composition, and recycling rate of P within the oceanic realm. Knowledge of the composition of P within marine systems, however, remains lacking. In order to fully describe the P composition new methods need to be developed. The indication that bacteria are remineralizing specific organic P compounds greatly impacts how scientists currently view nutrient limitation. This information, along with recent studies that demonstrate rapid recycling of SRP, will need to be included in all future models of phytoplankton distributions and their role in the uptake of CO2 and other anthropogenic components.
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Bacteria: Ubiquitous in nature, these prokaryotic organisms lacks organelles, such as nuclei.
Bioaccumulation: The process by which marine animals consume harmful components and concentrate them within their tissues.
Blooms: Most common in the spring, these refer to a large increase in phytoplankton abundance at the oceans surface.
Cosmic rays: High-energy particles, such as protons and neutrons, which continuously bombard the Earths surface.
Greenhouse Gas: One of many gases that are emitted to the atmosphere through mans activities and has been hypothesized to create a global increase in temperature.
Heterotrophic protozoa: Passively floating unicellular organisms that consume organic material.
1 Mol = 6.02 x 1023 molecules.
Nutrient Limitation: In biological systems, one nutrient tends to be depleted first during growth, and must be re-supplied for further growth to occur.
Oligotrophic: Those aquatic systems that are low in the nutrients which support the growth of phytoplankton.
Phytoplankton: Passively floating photosynthetic organisms which dominate the marine environment and include the three domains of life: Bacteria, Archea, and Eukarya.
Radioisotopes: Elements that are unstable, such that they decay to a more stable form via the emission of radiation. Radioisotopes are characterized by half-lives (t_), which is the length of time necessary for exactly half of the number of original radionuclide atoms to decay away. For example, after two half-lives have passed, only one quarter of the starting radionuclide material will still exist. By using the difference between the known initial radioisotope concentration and what is actually measured in the sample, one can estimate how much time has elapsed since sample formation. This is the basis for many radioisotope-dating techniques.
Red Tides: An aquatic phenomena caused by blooms of toxin-producing dinoflagellates. Concentrations of these species are high enough to give the water a red-brown appearance.
Remineralization: The process by which organic material is converted back into simpler, inorganic forms.
Zooplankton: Passively floating animals that consume phytoplankton.