Colimitation and the coupling of N and P uptake kinetics in oligotrophic mountain streams

Ecosystem element cycles can be tightly linked by both abiotic and biotic processes. Evidence for multi-element limitation (i.e., colimitation) of a variety of ecosystem processes is growing rapidly, yet our ability to quantify patterns of coupled nutrient dynamics at the ecosystem level has been hindered by logistical and methodological constraints. Here we quantify coupled nitrogen and phosphorus uptake kinetics in three oligotrophic mountain streams by using novel experimental techniques that quantify colimitation dynamics across a range of nutrient concentrations and stoichiometries. We show that relative demand for NO₃-N and PO₄-P varied across streams, but that short term availability of one nutrient consistently resulted in elevated, but variable, uptake of the other nutrient at all sites. We used temporally offset, pulsed nutrient additions to parameterize dual-nutrient Michaelis–Menten uptake surface models that represent NO₃-N and PO₄-P uptake at any given concentration or dissolved NO₃-N:PO₄-P stoichiometry. Our results indicated that the uptake of N and P were strongly enhanced in the presence of the other nutrient. Surface models quantitatively reflect patterns of colimitation and multi-element demand in streams, and should allow for parameterization of more realistic stream network models that explicitly account for interactions among element cycles.     

Growth characteristics and growth modeling of <Emphasis Type="Italic">Microcystis aeruginosa</Emphasis> and <Emphasis Type="Italic">Planktothrix agardhii</Emphasis> under iron limitation

Although iron is a key nutrient for algal growth just as are nitrogen and phosphorus in aquatic systems, the effects of iron on algal growth are not well understood. The growth characteristics of two species of cyanobacteria, Microcystis aeruginosa and Planktothrix agardhii, in iron-limited continuous cultures were investigated. The relationships between dissolved iron concentration, cell quota of iron, and population growth rate were determined applying two equations, Monod’s and Droop’s equations. Both species produced hydroxamate-type siderophores, but neither species produced catechol-type siderophores. The cell quota of nitrogen for both M. aeruginosa and P. agardhii decreased with decreasing cell quota of iron. The cell quota of phosphorus for M. aeruginosa decreased with decreasing cell quota of iron, whereas those for P. agardhii did not decrease. Iron uptake rate was measured in ironlimited batch cultures under different degrees of iron starvation. The results of the iron uptake experiments suggest that iron uptake rates are independent of the cell quota of iron for M. aeruginosa and highly dependent on the cell quota for P. agardhii. A kinetic model under iron limitation was developed based on the growth characteristics determined in our study, and this model predicted accurately the algal population growth and iron consumption. The model simulation suggested that M. aeruginosa is a superior competitor under iron limitation. The differences in growth characteristics between the species would be important determinants of the dominance of these algal species.     

Plant nitrogen and phosphorus limitation in 98 North American grassland soils

The availability of nutrients is a critical determinant of ecological dynamics in grasslands, but the relationships between soil resource availability and nutrient limitation across ecosystems are not clear. To better understand how soil nutrient availability determines nutrient limitation in vegetation, we grew the same species of grass (Schizachyrium scoparium) in 98 North American grassland soils and fertilized them factorially with nitrogen (N) and phosphorus (P). On average adding N, P, and the two nutrients together increased biomass relative to unfertilized plants by 81%, 22%, and 131%, respectively. Plants grown on low-P soils were not primarily limited by P. Instead, these plants were colimited by N and P, while plants grown on high-P soils were primarily limited by N and only secondarily limited by P. Limitation was not predicted by total soil N. The preponderance of colimitation between N and P on low-P soils suggests that low P availability alters the N cycle to constrain supplies to plants such that N and P are made available in proportion to their demand by plants.     

Independent colimitation for carbon dioxide and inorganic phosphorus

Simultaneous limitation of plant growth by two or more nutrients is increasingly acknowledged as a common phenomenon in nature, but its cellular mechanisms are far from understood. We investigated the uptake kinetics of CO(2) and phosphorus of the algae Chlamydomonas acidophila in response to growth at limiting conditions of CO(2) and phosphorus. In addition, we fitted the data to four different Monod-type models: one assuming Liebigs Law of the minimum, one assuming that the affinity for the uptake of one nutrient is not influenced by the supply of the other (independent colimitation) and two where the uptake affinity for one nutrient depends on the supply of the other (dependent colimitation). In addition we asked whether the physiological response under colimitation differs from that under single nutrient limitation.We found no negative correlation between the affinities for uptake of the two nutrients, thereby rejecting a dependent colimitation. Kinetic data were supported by a better model fit assuming independent uptake of colimiting nutrients than when assuming Liebigs Law of the minimum or a dependent colimitation. Results show that cell nutrient homeostasis regulated nutrient acquisition which resulted in a trade-off in the maximum uptake rates of CO(2) and phosphorus, possibly driven by space limitation on the cell membrane for porters for the different nutrients. Hence, the response to colimitation deviated from that to a single nutrient limitation. In conclusion, responses to single nutrient limitation cannot be extrapolated to situations where multiple nutrients are limiting, which calls for colimitation experiments and models to properly predict growth responses to a changing natural environment. These deviations from single nutrient limitation response under colimiting conditions and independent colimitation may also hold for other nutrients in algae and in higher plants.     

Nitrogen availability limits phosphorus uptake in an intertidal macroalga

Nutrients such as nitrogen (N) and phosphorus (P) limit primary productivity, and recent anthropogenic activities are changing the availability of these nutrients, leading to alterations in the type and magnitude of nutrient limitation. Recent work highlights the potential for N and P to interact to limit primary production in terrestrial and freshwater systems. However, mechanisms underlying co-limitation are not well described. Documentation of ambient nutrient levels and tissue nutrients of the intertidal macroalga Fucus vesiculosus for 2 years in the southern Gulf of Maine, USA, indicates that N availability may be impacting the ability of F. vesiculosus to access P, despite relatively high ambient P concentrations. To experimentally validate these observations, F. vesiculosus individuals were enriched with N or P for 6 weeks, followed by an uptake experiment to examine how the interactions between these nutrients affected macroalgal N and P uptake efficiency. Results illustrate that exposure of seaweed to different nutrient regimes influenced nutrient uptake efficiency. Notably, seaweeds enriched with N displayed the highest P uptake efficiency at low, biologically relevant, P concentrations. Our results confirm that N availability may be mediating the ability of primary producers to access P. These interactions between limiting nutrients have implications for not only the growth and functioning of primary producers who rely directly on these nutrients but also the entire communities that they support.     

Rocks create nitrogen hotspots and N:P heterogeneity by funnelling rain

We postulated that soil nutrient heterogeneity arises not only through physical and biological processes in the soil, but also through emergent rocks diverting precipitation containing nutrients to the surrounding soil. To test this idea—which we call the ‘funnelling effect’ of such rocks—we placed ion-exchange resin in small boxes beside rocks and in open soil on a pristine glacial forefield site in Switzerland, and measured the amounts of NH₄ ⁺, NO₃ ^?, NO₂ ^? and PO₄ ^3? that were adsorbed. We also placed resin bags beneath PVC funnels of different sizes so that we could calibrate the natural funnelling effect of rocks. We obtained strong linear relationships between nitrogen (N) adsorbed and rain-collecting area of both rocks and funnels. Although the mean rain-collecting area of rocks was only 0.02 m², mean N adsorption was around 10 times higher within 1 cm of rocks than further away. In contrast, phosphorus (P) was not concentrated beside rocks, so that N:P stoichiometry varied spatially. Rumex scutatus and Agrostis gigantea plants that rooted beside rocks had significantly higher foliar N concentrations than those growing further away, in line with the resin data. However, the two species showed differing responses in foliar P and N:P. We propose that R. scutatus benefits from the increased N supply by increasing its uptake of soil P, while A. gigantea is unable to do so. This study clearly demonstrates that aboveground rain-funnelling structures can produce spatial heterogeneity in N supply, thereby creating a diversity of nutritional niches for plants.     

Root architecture and hydraulic conductance in nutrient deprived Pistacia lentiscus L. seedlings

Plants respond to low nutrient availability by modifying root morphology and root system topology. Root responses to nitrogen (N) and phosphorus (P) limitation may affect plant capacity to withstand water stress. But studies on the effect of nutrient availability on plant ability to uptake and transport water are scarce. In this study, we assess the effect of nitrogen and phosphorus limitation on root morphology and root system topology in Pistacia lentiscus L seedlings, a common Mediterranean shrub, and relate these changes to hydraulic conductivity of the whole root system. Nitrogen and phosphorus deprivation had no effect on root biomass, but root systems were more branched in nutrient limited seedlings. Total root length was higher in seedlings subjected to phosphorus deprivation. Root hydraulic conductance decreased in nutrient-deprived seedlings, and was related to the number of root junctions but not to other architectural traits. Our study shows that changes in nutrient availability affect seedling water use by modifying root architecture. Changes in nutrient availability should be taken into account when evaluating seedling response to drought.     

Influence of nitrogen and phosphorus on polyphosphate accumulation in Gigaspora margarita during spore germination

Polyphosphate (polyP) is the form in which phosphorus (P) is transferred from extraradical hyphae into arbuscles in the symbiotic stage of arbuscular mycorrhizal fungi. However, polyP dynamics in the presymbiotic stage are less understood. In this study, we aimed to investigate polyP accumulation in Gigaspora margarita as influenced by nitrogen (N) and/or P supply during germination. Spores of G. margarita were incubated on medium with or without P or N addition. PolyP content in the fungal tissue was monitored using a polyP kinase/luciferase system, and polyP synthetic activity was determined with ³²P labeling. The results showed that both N and P were necessary for polyP accumulation in germ tubes. Nitrate increased the polyP content in germ tubes, but ammonium did not. Along with germination, polyP content decreased in spores, but increased in germ tubes. ³²P labeling indicated that polyP synthetic activity increased in germ tubes along with germination, but was negligible in spores. Our results suggest that, in the presymbiotic stage of G. margarita, uptake of environmental N and P increases polyP content in germ tubes, and that polyP synthesis occurs mainly therein, leading to polyP accumulation. The possible mechanism of transfer of polyP from spores to hyphae remains to be elucidated.     

NITRATE AND PHOSPHATE UPTAKE INTERACTIONS IN A MARINE PRYMNESIOPHYTE1

The short- and long-term uptake of nitrate and phosphate ions, and their interactions, were studied as functions of the preconditioning of Pavlova lutheri (Droop) Green. Populations were preconditioned in continuous culture at a variety of growth rates and N:P supply ratios. The maximum uptake rates cell^?1 for nitrate and phosphate were of similar magnitudes, in spite of the forty-fold smaller requirement for phosphorus. Short-term phosphate uptake was independent of the nitrate concentration, but the short-term nitrate uptake rate was reduced in the presence of phosphate. The severity of inhibition of nitrate uptake by phosphate was positively correlated with the preconditioning N:P supply ratio and the preconditioning growth rate. In response to large additions of nutrients, P. lutheri was able to increase its phosphorus content sixty-fold, but was only able to take up enough nitrate to double its nitrogen content. The high rate of phosphate uptake relative to its requirement, the inhibition of nitrate uptake by phosphate, and the large capacity for phosphorus storage relative to its requirement, all of which were observed even under N limitation, may imply that even where nitrogen is limiting there can be interspecific competition for available phosphate.     

GROWTH RATE VARIATION IN THE N:P REQUIREMENT RATIO OF PHYTOPLANKTON1

Theoretical considerations predict that the cell N:P ratio at transition from nitrogen limitation to phosphorus limitation of phytoplankton growth (critical ratio, R_c) varies, as a function of population growth rate. This prediction is confirmed by experimental, data from the literature along with new experimental data for the marine, prymnesiophyte Pavlova lutheri (Droop) Green. R_c passes through a maximum at intermediate growth rates for the three phytoplankton species for which data, are available, but there is significant interspecific variability in its value. There is no theoretical or experimental evidence to support the idea that the ratio of subsistence N and P cell quotas is equal to R_c over the range of growth rates, or that the subsistence quota ratio equals the ratio of the N and P cell quotas minus a storage fraction. Examination of N:P composition ratios can be used to determine which nutrient is limiting, but cannot be used to determine relative growth rates or competitive advantage between species limited by the same nutrient. Growth rates are determined by environmental conditions and by the cell quota of the limiting nutrient, without reference to the cell quota of the non-limiting nutrient.     

Heterogeneity in the nutrient limitation of different bacterioplankton groups in the Eastern Mediterranean Sea

The heterotrophic bacterial community of the Eastern Mediterranean Sea is believed to be limited by phosphorus (P) availability. This observation assumes that all bacterial groups are equally limited, something that has not been hitherto examined. To test this hypothesis, we performed nutrient addition experiments and investigated the response of probe-identified groups using microautoradiography combined with catalyzed reporter deposition fluorescence in situ hybridization. Our results show contrasting responses between the bacterial groups, with Gammaproteobacteria being the group more affected by P availability. The Roseobacter clade was likely colimited by P and nitrogen (N), whereas Bacteroidetes by P, N and organic carbon (C). In contrast, SAR11 cells were active regardless of the nutrient concentration. These results indicate that there is high heterogeneity in the nutrient limitation of the different components of the bacterioplankton community.     

Growth rate of alpine phytoplankton assemblages from contrasting watersheds and N‐deposition regimes exposed to nitrogen and phosphorus enrichments

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Monitoring cellular C:N ratio in phytoplankton by means of FTIR‐spectroscopy

Statistical growth rate modelling can be applied in a variety of ecological and biotechnological applications. Such models are frequently based on Monod or Droop equations and, especially for the latter, require reliable determination of model input parameters such as C:N quotas. Besides growth rate modelling, a C:N quota quantification can be useful for monitoring and interpretation of physiological acclimation to abiotic and biotic disturbances (e.g., nutrient limitations). However, as high throughput C:N quota determination is difficult to perform, alternatives need to be established. Fourier‐transformed infrared (FTIR) spectroscopy is used to analyze a variety of biochemical, chemical, and physiological parameters in phytoplankton. Hence, a quantification of the C:N quota should also be feasible. Therefore, using FTIR spectroscopy, six phytoplankton species from among different phylogenetic groups have been analyzed to determine the effect of nutrient limitation on C:N quota patterns. The typical species‐specific response to increasing nitrogen limitation was an increase in the C:N quota. Irrespective of this species specificity, we were able to develop a reliable multi‐species C:N quota prediction model based on FTIR spectroscopy using the partial least square regression (PLSR) algorithm. Our data demonstrate that the PLSR approach is more robust in C:N quota quantification (R² = 0.93) than linear correlation of C:N quota versus growth rate (R² ranges from 0.74 to 0.86) or biochemical information based on FTIR spectra (R² ranges from 0.82 to 0.89). This accurate prediction of C:N values may support high throughput measurements in a broad range of future approaches.     

Steady-State Growth and Chemical Composition of the Marine Chlorophyte Dunaliella tertiolecta in Nitrogen-Limited Continuous Cultures

The marine chlorophyte Dunaliella tertiolecta was grown in continuous cultures under NH₄⁺-N, NO₂⁻-N, NO₃⁻-N, and urea-N limitations. The effect of the nitrogen cell quota (Q_n) on the steady-state growth rate (μ) was the same regardless of the N source. The relationship between μ and Q_n was well described by the Droop equation, but only up to the true maximum growth rate ^μ (= cell washout rate). The ratio between the minimum cell quota (k_Q) and the maximum cell quota (Q_m) was 0.19. Hence, there is no substitute for determining ^μ experimentally. That there was no difference in growth response to different N sources suggests that no internal pooling of inorganic nitrogen occurred. Both the carbon (Q_c) and phosphorus (Q_p) cell quotas under N limitation increased with increasing μ in a threshold fashion: virtually no change in either cell quota up to ~0.8 ^μ, followed by a rapid and large increase up to ^μ. In addition, in the region of low μ, there was an increase in Q_p with a decreasing medium N/P ratio of between 15 and 5 (by atoms). The results generally indicate the physiological limits in cellular constituency under N limitation. The usefulness of this information, however, in describing the response of natural populations of marine phytoplankton to transient nutrient exposures on the temporal and spatial microscales that most likely exist is of limited value.     

Phosphorus and nitrogen allocation in Allium ursinum on an alluvial floodplain (Eastern France). Is there an effect of flooding history?

The change in phosphorus and nitrogen content in a common geophyte spring species, Allium ursinum, is studied in alluvial forests in relation to three flooding histories related to river regulation: (1) annually flooded, (2) unflooded for 30 years, and (3) unflooded for 200 years. Flood suppression leads to a reduction of available P soil content as well as decreasing the biomass and the amount of phosphorus in plants, but has no significant effect on N plant content. Plant N:P ratio increases with the suppression of floods and is primarily driven by soil N:P ratios, in turn markedly linked to the total nitrogen in the soil. We highlighted a lower nutrient accumulation in leaves during plant growth in unflooded forests. Overall, our results suggest that P was the main limiting factor in unflooded forests while nitrogen was the main limiting factor in annually flooded forests. Flood suppression strongly affects the morphology and nutrient uptake by Allium ursinum and thus nutrient cycling in riverine forests.     

Relationship between the Relative Limitation and Resorption Efficiency of Nitrogen vs Phosphorus in Woody Plants

Most previous studies have ascribed variations in the resorption of a certain plant nutrient to its corresponding environmental availability or level in tissues, regardless of the other nutrients’ status. However, given that plant growth relies on both sufficient and balanced nutrient supply, the nutrient resorption process should not only be related to the absolute nutrient status, but also be regulated by the relative limitation of the nutrient. Here, based on a global woody-plants dataset from literature, we test the hypothesis that plants resorb proportionately more nitrogen (or phosphorus) when they are nitrogen (or phosphorus) limited, or similar proportions of nitrogen (N) and phosphorus (P) when co-limited by both nutrients (the relative resorption hypothesis). Using the N:P ratio in green foliage as an indicator of nutrient limitation, we found an inverse relationship between the difference in the proportionate resorption of N vs P and this foliar N:P ratio, consistent across species, growth-forms, and vegetation-types globally. Moreover, according to the relative resorption hypothesis, communities with higher/lower foliar N:P (more likely P/N limited) tend to produce litter with disproportionately higher/lower N:P, causing a worsening status of P/N availability; this positive feedback may somehow be counteracted by several negative-feedback mechanisms. Compared to N, P generally shows higher variability in resorption efficiency (proportion resorbed), and higher resorption sensitivity to nutrient availability, implying that the resorption of P seems more important for plant nutrient conservation and N:P stoichiometry. Our findings elucidate the nutrient limitation effects on resorption efficiency in woody plants at the global scale, and thus can improve the understanding of nutrient resorption process in plants. This study also suggests the importance of the foliar N:P ratio as a key parameter for biogeochemical modeling, and the relative resorption hypothesis used to deduce the critical (optimal) N:P ratio for a specific plant community.     

Effects of simultaneous infections of endophytic fungi and arbuscular mycorrhizal fungi on the growth of their shared host grass Achnatherum sibiricum under varying N and P supply

Grasses can be infected by endophytic fungi and arbuscular mycorrhizal (AM) fungi simultaneously. Here, we investigated the interactions of a native grass, Achnatherum sibiricum, with both endophytic and AM fungi (Glomus mosseae, GM and Glomus etunicatum, GE) at different nitrogen (N) and phosphorus (P) levels. The results showed that endophyte infection significantly suppressed the colonization rates and spore density of GE, but had no effect on those of GM. Endophyte infection increased shoot biomass regardless of the nutrient conditions. The effects of AM fungi on host growth were dependent on mycorrhizal species. There was no significant interaction between endophytic fungi and GE on host growth; however, a significant interaction between endophytic fungi and GE occurred in total phenolic concentrations and P uptake. As for GM, a significant interaction among endophytic fungi, AM fungi and nutrient availability occurred in shoot growth. Under sufficient N and P conditions, endophyte infection alleviated the detrimental effects of GM colonization on host growth.     

Effects of artificial grassland establishment on soil nutrients and carbon properties in a black-soil-type degraded grassland

Despite a growing knowledge of nutrient limitation for mangrove species and how mangroves adapt to low nutrients, there is scant information about the relative importance of N:P ratio and leaf phenolics variability in determining nutrient conservation. In this study, we evaluated possible nutrient conservation strategies of a mangrove Rhizophora stylosa under nutrient limitation. 1. The leaf nutrient concentrations of R. stylosa changed with season, with the highest N concentration in winter and the highest P concentration in spring for both mature and senescent leaves. Leaf N and P concentrations decreased significantly during leaf senescence. Based on N:P ratios R. stylosa forest was N-limited. Accordingly, the nitrogen resorption efficiency (NRE) was significantly higher than phosphorus resorption efficiency (PRE) for the R. stylosa leaves during leaf senescence. The NRE and PRE both reached the highest in the autumn. Average N and P concentrations in the senescent leaves were 0.15% and 0.06% for R. stylosa, respectively, indicating a complete resorption of N and an incomplete resorption of P. There was a significant negative correlation between nitrogen resorption proficiency (NRP) and NRE, meanwhile phosphorus resorption proficiency (PRP) and PRE correlation was also highly significantly. 2. R. stylosa leaves contained relatively high tannin level. Total phenolics, extractable condensed tannins and total condensed tannins contents increased during leaf senescence, and changed between seasons. The lowest concentrations of total phenolics, extractable condensed tannins and total condensed tannins occurred in summer, total phenolics concentrations were inversely related to nitrogen or phosphorus concentrations. 3. Our results confirmed that resorption efficiency during leaf senescence depends on the type of nutrient limitation, and NRE was much higher than PRE under N-limited conditions. R. stylosa forest developed several nutrient conservation strategies in the intertidal coastline surroundings, including high nitrogen resorption efficiency, low nutrient losses and high tannins level.     

Influence of N/P ratio on competitive abilities for nitrogen and phosphorus by <Emphasis Type="Italic">Microcystis aeruginosa</Emphasis> and <Emphasis Type="Italic">Aulacoseira distans</Emphasis>

Microcystis aeruginosa and Aulacoseira distans strains were grown in batch cultures to investigate the consequences of N/P ratio on the growth of these species and on their abilities to take up nitrogen and phosphorus. N/P ratio did not influence the growth rates, which were similar under all the experimental conditions. However, exponential growth lasted longer in Microcystis than in Aulacoseira, especially under low N/P ratio conditions. Distinct patterns of nutrient uptake for Aulacoseira and Microcystis were observed. N-uptake was higher in Microcystis, but not influenced by N/P ratio. However, the amount absorbed was proportional to the concentration in the culture medium for both strains studied. Although Microcystis showed lower uptake of N per biomass unit, a greater yield of Microcystis growth relative to the diatom was observed. This could have resulted from its ability to produce biomass using less nitrogen per unit of biomass. A variation of N/P ratio in the culture medium during the growth of both species was observed. This owed to the uptake of nutrients, with Microcystis showing greater potential than Aulacoseira to influence the N/P ratio. Thus, in contrast to what has been stated in the literature, our results indicated that a low N/P ratio could be a consequence of the capacities and rates of cyanobacterial uptake of nitrogen and phosphorus.