P-limited Environments Research Articles

Phosphate as a limiting resource: introduction

Phosphorus (P) is commonly a limiting nutrient for both terrestrial and aquatic productivity, with the consequence that it is considered important in determining the biodiversity and biomass of natural ecosystems. P-limitation of terrestrial plants is not a recent development. Karandashov and Bucher (2005) argued that the evolutionary transition of plants from the aquatic to terrestrial habitats was contingent on the presence of arbuscular mycorrhiza, which facilitated P acquisition. As a consequence of persistent P-limitations, terrestrial plants have evolved a wide range of P acquisition strategies, including mechanisms that increase the range of chemical forms that can be accessed, the range of concentrations that can be taken up and the effective absorbing area of the roots (Lambers et al. 2008). Likewise, plants have a range of strategies for conserving P that enable them to persist in P-deficient habitats, including sclerophyllous leaves and serotinous cones. In order to ensure successful recruitment in P-limited environments they also produce P-rich seeds (e.g. Groom and Lamont 2010, this volume). P is also often a limiting nutrient in agriculture (e.g. Sanchez 2010), deficiency being redressed through applications of P-fertilisers (globally ca. 20×10 kg P annum; Smit et al. 2009). Alarmingly, the finite global stocks of P (2,400×10 kg P) are likely to be depleted within 125 years (Smit et al. 2009; Vaccari 2009). Anthropogenic modification of the global P cycle by fertiliser use as well as waste streams and detergent use have effectively doubled global P cycling since the mid-19th century (Filippelli 2002). A consequence is that many natural ecosystems are threatened by super-abundance of a formerly limiting resource, with resulting biodiversity losses (e.g. Tilman et al. 2001). This is likely to be especially true in systems where P was formerly most-limiting, such as in Mediterranean terrestrial ecosystems (Sala et al. 2000), oligotrophic lakes (Schindler et al. 2008) and nutrient-impoverished oceans (Rabalais et al. 2008). Apart from the direct biodiversity consequences of P-eutrophication, release from P-limitation combined with increased atmospheric CO2 concentration and N deposition may exacerbate the loss of biodiversity.

Competition for inorganic and organic forms of nitrogen and phosphorous between phytoplankton and bacteria during an <i>Emiliania huxleyi</i> spring bloom

Abstract. Using 15N and 33P, we measured the turnover of organic and inorganic nitrogen (N) and phosphorus (P) substrates, and the partitioning of N and P from these sources into two size fractions of marine osmotrophs during the course of a phytoplankton bloom in a nutrient manipulated mesocosm. The larger size fraction (>0.8 μm), mainly consisting of the coccolithophorid Emiliania huxleyi, but also including an increasing amount of large particle-associated bacteria as the bloom proceeded, dominated uptake of the inorganic forms NH4+, NO3−, and PO43−. The uptake of N from leucine, and P from ATP and dissolved DNA, was initially dominated by the 0.8–0.2 μm size fraction, but shifted towards dominance by the >0.8 μm size fraction as the system turned to an increasing degree of N-deficiency. Normalizing uptake to biomass of phytoplankton and heterotrophic bacteria revealed that organisms in the 0.8–0.2 μm size fraction had higher specific affinity for leucine-N than those in the >0.8 μm size fraction when N was deficient, whereas the opposite was the case for NH4+. There was no such difference regarding the specific affinity for P substrates. Since heterotrophic bacteria seem to acquire N from organic compounds like leucine more efficiently than phytoplankton, our results suggest different structuring of the microbial food chain in N-limited relative to P-limited environments.

Dynamics of Stoichiometric Bacteria-Algae Interactions in the Epilimnion

Bacteria-algae interaction in the epilimnion is modeled with the explicit consideration of carbon (energy) and phosphorus (nutrient). Global qualitative analysis and bifurcation diagrams of this model are presented. We hypothesize that there are three dynamical scenarios determined by the basic reproductive numbers of bacteria and algae. Effects of key environmental conditions are examined through these scenarios and from systematic and extensive simulations. It is also shown that excessive sunlight will destroy bacterial communities. Bifurcation diagrams for the depth of epilimnion mimic the profile of Lake Biwa, Japan. Competition of bacterial strains are modeled to examine Nishimura's hypothesis that in severely P-limited environments such as Lake Biwa, P-limitation exerts more severe constraints on the growth of bacterial groups with higher nucleic acid contents, which allows low nucleic acid bacteria to be competitive.

Vertical and Seasonal Variations of Bacterioplankton Subgroups with Different Nucleic Acid Contents: Possible Regulation by Phosphorus

We used flow cytometry to examine seasonal variations in basin-scale distributions of bacterioplankton in Lake Biwa, Japan, a large mesotrophic freshwater lake with an oxygenated hypolimnion. The bacterial communities were divided into three subgroups: bacteria with very high nucleic acid contents (VHNA bacteria), bacteria with high nucleic acid contents (HNA bacteria), and bacteria with low nucleic acid contents (LNA bacteria). During the thermal stratification period, the relative abundance of VHNA bacteria (%VHNA) increased with depth, while the reverse trend was evident for LNA bacteria. Seasonally, the %VHNA was strongly positively correlated (r = 0.87; P < 0.001) with the concentration of dissolved inorganic phosphorus, but not with the concentration of chlorophyll a. The growth of VHNA bacteria was significantly enhanced by addition of phosphate or phosphate plus glucose but not by addition of glucose alone. Although the growth of VHNA and HNA bacteria generally exceeded that of LNA bacteria, our data also revealed that LNA bacteria grew faster than and were grazed as fast as VHNA bacteria in late August, when nutrient limitation was presumably severe. Based on these results, we hypothesize that in severely P-limited environments such as Lake Biwa, P limitation exerts more severe constraints on the growth of bacterial groups with higher nucleic acid contents, which allows LNA bacteria to be competitive and become an important component of the microbial loop.

Optimal nitrogen-to-phosphorus stoichiometry of phytoplankton.

Redfield noted the similarity between the average nitrogen-to-phosphorus ratio in plankton (N:P = 16 by atoms) and in deep oceanic waters (N:P = 15; refs 1, 2). He argued that this was neither a coincidence, nor the result of the plankton adapting to the oceanic stoichiometry, but rather that phytoplankton adjust the N:P stoichiometry of the ocean to meet their requirements through nitrogen fixation, an idea supported by recent modelling studies. But what determines the N:P requirements of phytoplankton? Here we use a stoichiometrically explicit model of phytoplankton physiology and resource competition to derive from first principles the optimal phytoplankton stoichiometry under diverse ecological scenarios. Competitive equilibrium favours greater allocation to P-poor resource-acquisition machinery and therefore a higher N:P ratio; exponential growth favours greater allocation to P-rich assembly machinery and therefore a lower N:P ratio. P-limited environments favour slightly less allocation to assembly than N-limited or light-limited environments. The model predicts that optimal N:P ratios will vary from 8.2 to 45.0, depending on the ecological conditions. Our results show that the canonical Redfield N:P ratio of 16 is not a universal biochemical optimum, but instead represents an average of species-specific N:P ratios.

QUANTIFICATION OF MYO-INOSITOL HEXAKISPHOSPHATE IN ALKALINE SOIL EXTRACTS BY SOLUTION 31P NMR SPECTROSCOPY AND SPECTRAL DECONVOLUTION

Inositol phosphates are the dominant class of organic phosphorus (P) compounds in most soils, but they are poorly understood because they are not easily identified in soil extracts. This study reports a relatively simple technique using solution 31P NMR spectroscopy and spectral deconvolution for the quantification of myo-inositol hexakisphosphate (phytic acid), the most abundant soil inositol phosphate, in alkaline soil extracts. An authentic myo-inositol hexakisphosphate standard added to a re-dissolved soil extract gave signals at 5.85, 4.92, 4.55, and 4.43 ppm in the ratio 1:2:2:1. Spectral deconvolution quantified these signals accurately (102 ± 4%) in solutions containing a mixture of model P compounds by resolving the envelope of signals in the orthophosphate monoester region. In NaOH-EDTA extracts from a range of lowland permanent pasture soils in England and Wales, concentrations of myo-inositol hexakisphosphate determined by spectral deconvolution ranged between 26 and 189 mg P kg- 1 soil, equivalent to between 11 and 35% of the extracted organic P. Concentrations were positively correlated with oxalate-extractable aluminum and iron but were not correlated with total carbon, total nitrogen, clay, or the microbial biomass. This suggests that myo-inositol hexakisphosphate accumulates in soils by mechanisms at least partially independent of those controlling organic matter stabilization and dynamics. Furthermore, myo-inositol hexakisphosphate concentrations were positively correlated with plant-available inorganic P and negatively correlated with the carbon-to-organic P ratio, suggesting that biological P availability may, in part, regulate myo-inositol hexakisphosphate concentrations in soils, perhaps because organisms capable of degrading this compound are favored in more P-limited environments. Solution 31P NMR spectroscopy and spectral deconvolution offers a relatively simple method of quantifying myo-inositol hexakisphosphate in soil extracts.

Phosphate Uptake by Microorganisms in Lake Water: Deviations from Simple Michaelis–Menten Kinetics

Orthophosphate (31Pi) uptake rates by natural Lake Michigan microbial assemblages were measured to test a hypothesis that the instantaneous velocity of31Piuptake at low added substrate concentrations is higher than predicted by the simple Michaelis–Menten equation. Analysis of data from most experiments verified this prediction:31Piturnover times (Tcalc) obtained by back-extrapolating from "low" substrate regions in Woolf plots ranged from 25% to nearly 3000% of those calculated from "high" substrate regions. Simulation analysis demonstrated that deviations in Tcalccould be at least an order of magnitude higher than previously predicted. Large (&gt;1000%) discrepancies from the simple Michaelis–Menten equation could be caused by "skewed" or "clumped" distributions, where the range in both species half-saturation constants (Kt) and relative abundances is very wide and species with the lowest Ktvalues are most abundant. A comparison of Ktvalues for mixed microbial assemblages in Lake Michigan (0.16–19.4 μg P∙L−1) with those from laboratory culture studies (11–364 μg P∙L−1) demonstrates that natural microbial populations have adapted to P-limited environments by synthesizing uptake systems that have Ktvalues at least an order of magnitude below those detected in culture studies.