Saturating relationship between phytoplankton growth rate and nutrient concentration explained by macromolecular allocation

Phytoplankton account for about a half of photosynthesis in the world, making them a key player in the ecological and biogeochemical systems. One of the key traits of phytoplankton is their growth rate because it indicates their productivity and affects their competitive capability. The saturating relationship between phytoplankton growth rate and environmental nutrient concentration has been widely observed yet the mechanisms behind the relationship remain elusive. Here we use a mechanistic model and metadata of phytoplankton to show that the saturating relationship between growth rate and nitrate concentration can be interpreted by intracellular macromolecular allocation. At low nitrate levels, the diffusive nitrate transport linearly increases with the nitrate concentration, while the internal nitrogen requirement increases with the growth rate, leading to a non-linear increase in the growth rate with nitrate. This increased nitrogen requirement is due to the increased allocation to biosynthetic and photosynthetic molecules. The allocation to these molecules reaches a maximum at high nitrate concentration and the growth rate ceases to increase despite high nitrate availability due to carbon limitation. The produced growth rate and nitrate relationships are consistent with the data of phytoplankton across taxa. Our study provides a macromolecular interpretation of the widely observed growth-nutrient relationship and highlights that the key control of the phytoplankton growth exists within the cell

Saturating growth rate against phosphorus concentration explained by macromolecular allocation

The saturating relationship between phytoplankton growth rate and environmental nutrient concentration has been widely observed, yet the mechanisms behind the relationship remain elusive. Here, we use a mechanistic model of phytoplankton and show that the saturating relationship between growth rate and phosphorous concentration can be interpreted by intracellular macromolecular allocation. At low nutrient levels, the diffusive nutrient transport linearly increases with the phosphorous concentration, while the internal phosphorous requirement increases with the growth rate, leading to a non-linear increase in the growth rate with phosphorous. This increased phosphorous requirement is due to the increased allocation to biosynthetic and photosynthetic molecules. The allocation to these molecules reaches a maximum at high-phosphorous concentration, and the growth rate no longer increases despite the rise in phosphorous concentration. The produced growth rate and phosphorous relationships are consistent with the data of phytoplankton across taxa. Our study suggests that the key control of phytoplankton growth is internal, and nutrient uptake is only a single step in the overall process

Patterns in the temporal complexity of global chlorophyll concentration

Decades of research have relied on satellite-based estimates of chlorophyll-a concentration to identify oceanographic processes and plan in situ observational campaigns; however, the patterns of intrinsic temporal variation in chlorophyll-a concentration have not been investigated on a global scale. Here we develop a metric to quantify time series complexity (i.e., a measure of the ups and downs of sequential observations) in chlorophyll-a concentration and show that seemingly disparate regions (e.g., Atlantic vs Indian, equatorial vs subtropical) in the global ocean can be inherently similar. These patterns can be linked to the regularity of chlorophyll-a concentration change and the likelihood of anomalous events within the satellite record. Despite distinct spatial changes in decadal chlorophyll-a concentration, changes in time series complexity have been relatively consistent. This work provides different metrics for monitoring the global ocean and suggests that the complexity of chlorophyll-a time series can be independent of its magnitude

A quantitative analysis of the direct and indirectcosts of nitrogen fixation: a model based onAzotobacter vinelandii

Nitrogen fixation is advantageous in microbial competition when bioavailable nitrogen is scarce, but has substantial costs for growth rate and growth efficiency. To quantify these costs, we have developed a model of a nitrogen-fixing bacterium that constrains mass, electron and energy flow at the scale of the individual. When tested and calibrated with laboratory data for the soil bacterium Azotobacter vinelandii, the model reveals that the direct energetic cost of nitrogen fixation is small relative to the cost of managing intracellular oxygen. It quantifies the costs and benefits of several potential oxygen protection mechanisms present in nature including enhanced respiration (respiratory protection) as well as the production of extracellular polymers as a barrier to O2 diffusion, and increasing cell size. The latter mechanisms lead to higher growth efficiencies relative to respiratory protection alone. This simple, yet mechanistic framework provides a quantitative model of nitrogen fixation, which can be applied in ecological simulations

Impact of Increased Nutrients and Lowered pH on Photosynthesis and Growth of Three Marine Phytoplankton Communities From the Coastal South West Atlantic (Patagonia, Argentina)

Effect of global change variables on the structure and photosynthesis of phytoplankton communities was evaluated in three different sites of the Patagonian coast of Argentina: enclosed bay (Puerto Madryn, PM), estuarine (Playa Unión, PU), and open waters (Isla Escondida, IE). We exposed samples to two contrasting scenarios: Present (nutrients at in situ levels) vs. Future (with lowered pH and higher nutrients inputs), and determined growth and photosynthetic responses after 2 days of acclimation. Under the Future condition phytoplankton growth was higher in the estuarine site compared to those in PM and IE. This effect was the most pronounced on large diatoms. While the increase of photosynthetic activity was not always observed in the Future scenario, the lower photosynthetic electron requirement for carbon fixation (Φe,C = ETR/PmB) in this scenario compared to the Present, suggests a more effective energy utilization. Long-term experiments were also conducted to assess the responses along a 4 days acclimation period in PU. Diatoms benefited from the Future conditions and had significantly higher growth rates than in the Present. In addition, Φe,C was lower after the acclimation period in the Future scenario, compared to the Present. Our results suggest that the availability, frequency and amount of nutrients play a key role when evaluating the effects of global change on natural phytoplankton communities. The observed changes in diatom growth under the Future scenario in PU and IE and photosynthesis may have implications in the local trophodynamics by bottom up control

The balance between photosynthesis and respiration explains the niche differentiation between Crocosphaera and Cyanothece

Crocosphaera and Cyanothece are both unicellular, nitrogen-fixing cyanobacteria that prefer different environments. Whereas Crocosphaera mainly lives in nutrient-deplete, open oceans, Cyanothece is more common in coastal, nutrient-rich regions. Despite their physiological similarities, the factors separating their niches remain elusive. Here we performed physiological experiments on clone cultures and expand upon a simple ecological model to show that their different niches can be sufficiently explained by the observed differences in their photosynthetic capacities and rates of carbon (C) consumption. Our exper- iments revealed that Cyanothece has overall higher photosynthesis and respiration rates than Crocosphaera. A simple growth model of these microorganisms suggests that C storage and consumption are previously under-appreciated factors when evaluating the occupation of niches by different marine nitrogen fixers

Development of a cell flux model and its application to nitrogen fixers

Thesis: Ph. D., Massachusetts Institute of Technology, Department of Earth, Atmospheric, and Planetary Sciences, 2016.Cataloged from PDF version of thesis.Includes bibliographical references..Quantifying and modeling the macroscopic ecological and biogeochemical effects of cellular physiology and metabolism is a challenge: most quantitative "systems biology" models are focused at the metabolic and individual scale. In this study, we develop and apply a simplified metabolic model at the individual scale, which we call "the cell flux model", in order to quantify costs and benefits of nitrogen fixers. In Chapter 2, we develop the cell flux model for heterotrophic nitrogen fixers in order to examine and quantify the direct and indirect energy costs of nitrogen fixation. We have tested the model using data from Azotobacter vinelandii grown in continuous culture. The model indicates that the direct energy cost of nitrogen fixation is relatively small, whereas oxygen management to protect nitrogenase becomes dominant as the oxygen concentration increases. In Chapter 3, we have adapted the cell flux model of Azotobacter vinelandii to consider the organisms' response to the presence of ammonium in the environment. The model shows that even under high oxygen concentrations and with high ambient concentrations of fixed nitrogen, nitrogen fixation occurs if there is sufficient carbohydrate resource available to fully consume intracellular oxygen. Most nitrogen fixers in the ocean are photoautotrophic. Thus, in Chapter 4, we extend the cell flux model to resolve phototrophy and use it simulate and study light and nutrient colimitation of Synechococcus spp. as observed in published continuous culture studies. In order to capture the observed variations in elemental composition with light and resource availability, we resolve the macromolecular composition of the cells. The highly simplified model is able to simulate key aspects of the laboratory cultures including explicit prediction of the average elemental composition and maximum growth rates under different environmental limitations. In Chapter 5, we have applied the cell flux model to simulate laboratory studies, and interpreted the ecological costs for the photoautotrophic nitrogen fixer Crocosphaera watsonii. Our model suggests that these organism also utilize multiple oxygen protection strategies, including scavenging oxygen with excess respiration, changing their size, and using extracellular polymeric substances as a barrier to the invasion of oxygen into the cell.by Keisuke Inomura.Ph. D

Modeled temperature dependencies of macromolecular allocation and elemental stoichiometry in phytoplankton

Warming oceans may affect how phytoplankton allocate nutrients to essential cellular processes. Despite the potential impact of such processes on future biogeochemical cycles, questions remain about how temperature affects macromolecular allocation and elemental stoichiometry within phytoplankton cells. Here, we present a macromolecular model of phytoplankton and the effect of increasing temperature on the intracellular allocation of nutrients at a constant growth rate. When temperature increases under nitrogen (N) and phosphorus (P) co-limitation, the model shows less investment in phosphorus-rich RNA molecules relative to nitrogen-rich proteins, leading to a more severe decrease in cellular P:C than N:C causing increased cellular N:P values. Under P limitation, the model shows a similar pattern, but when excess P is available under N limitation, we predict lowered N:P due to the effect of luxury uptake of P. We reflected our model result on the surface ocean showing similar latitudinal patterns in N:P and P:C to observation and other model predictions, suggesting a considerable impact of temperature on constraining the elemental stoichiometry in the ocean

Modeling the elemental stoichiometry and silicon accumulation in diatoms

Diatoms are important microorganisms involved in global primary production, nutrient cycling, and carbon sequestration. A unique feature of diatoms is their silica frustules, which impact sinking speed, defense against predators and viruses, and growth cycling. Thus, frustules are inherently linked to their role in ecosystems and biogeochemical cycles. However, constraints on cellular silicon levels remain unclear and few existing models resolve diatom elemental stoichiometry to specifically include variable silicon levels. Here, we use a coarse-grained model of the diatom, Thalassiosira pseudonana, compared with laboratory results to illustrate the relationship of silicon uptake with elemental stoichiometry of other nutrients. The model-data comparison suggests the balance between growth rate and silicon uptake constrains the amount of cellular silicon. Additionally, it expresses relationships between silicon, nitrogen, phosphorus, and carbon to changing growth rates in nitrogen-limited and phosphorus-limited regimes. First, our model-data comparison suggests Si uptake hits a maximum cellular quota at low growth rates and below this maximum there is independent Si uptake. In each nutrient regime, Si:N, Si:P, and Si:C decrease exponentially with growth rate when Si is below the maximum limit. This is explained by independent Si uptake and increased loss of Si to new cells. These results provide predictions of diatom stoichiometry and allocation, which can be used in ecosystem models to differentiate phytoplankton types to better represent diatoms’ contribution to global biogeochemical cycles and ecosystems