Interactions between growth-dependent changes in cell size, nutrient supply and cellular elemental stoichiometry of marine Synechococcus

Abstract

The factors that control elemental ratios within phytoplankton, like carbon:nitrogen:phosphorus (C:N:P), are key to biogeochemical cycles. Previous studies have identified relationships between nutrientlimited growth and elemental ratios in large eukaryotes, but little is known about these interactions in small marine phytoplankton like the globally important Cyanobacteria. To improve our understanding of these interactions in picophytoplankton, we asked how cellular elemental stoichiometry varies as a function of steady-state, N-and P-limited growth in laboratory chemostat cultures of Synechococcus WH8102. By combining empirical data and theoretical modeling, we identified a previously unrecognized factor (growth-dependent variability in cell size) that controls the relationship between nutrient-limited growth and cellular elemental stoichiometry. To predict the cellular elemental stoichiometry of phytoplankton, previous theoretical models rely on the traditional Droop model, which purports that the acquisition of a single limiting nutrient suffices to explain the relationship between a cellular nutrient quota and growth rate. Our study, however, indicates that growth-dependent changes in cell size have an important role in regulating cell nutrient quotas. This key ingredient, along with nutrient-uptake protein regulation, enables our model to predict the cellular elemental stoichiometry of Synechococcus across a range of nutrient-limited conditions. Our analysis also adds to the growth rate hypothesis, suggesting that P-rich biomolecules other than nucleic acids are important drivers of stoichiometric variability in Synechococcus. Lastly, by comparing our data with field observations, our study has important ecological relevance as it provides a framework for understanding and predicting elemental ratios in ocean regions where small phytoplankton like Synechococcus dominates.

Interactions between Thermal Acclimation, Growth Rate, and Phylogeny Influence Prochlorococcus Elemental Stoichiometry

“…Such a change in cell size means that you cannot simply extrapolate from an increase or a decrease in an individual cell quota (like Q P ) to the stoichiometric ratio. Thus, our study adds to an emerging concept, whereby changes in cell size due to physiological responses to different environmental conditions are important for regulating the elemental composition and ratios in marine Cyanobacteria [16]. …”

“…The main suggested controls include nutrient availability, growth rate, temperature, and life history. Extensive experimental and model studies have demonstrated a strong effect of nutrient availability, whereby a low supply of nitrogen or phosphorus leads to a low cell quota ( Q ) of the corresponding element [13–16]. Another important factor is the cellular allocation towards P rich ribosomes at elevated growth rates.…”

“…Coined the ‘Growth Rate Hypothesis’ [17], fast growth is hypothesized to result in high Q P and corresponding low C/P and N/P ratios. However, this growth effect on stoichiometry appears to vary extensively by organism and environmental conditions [16,18,19]. Thus, the genetic and environmental contexts (and possible interactions) for changes in growth rate may be important to consider.…”

Autotrophic Stoichiometry Emerging from Optimality and Variable Co-limitation

“…These patterns can be categorized into 3 broad classes: (1) both N:C and P:C increasing with dilution rate under N-and P-limitation (B. pendula, Ågren, 2004); (2) only the limiting nutrient correlates with dilution rate (Scenedesmus sp., Rhee, 1974); (3) the asymmetric response, i.e., N:C increasing with dilution rate both at N-and P-limitation, but P:C increases only when P is limiting, (S. linearis and S. minutum, Elrifi and Turpin, 1985;Healey, 1985). Also using a Synechococcus strain, however in a constrained range of growth rates, Garcia et al (2016) found similar asymmetric patterns. Those patterns were previously addressed by alternative model approaches (e.g., Ågren, 2004;Flynn, 2008;Bougaran et al, 2010;Bonachela et al, 2013;Pahlow et al, 2013).…”

Evolutionary Pathway Determines the Stoichiometric Response of Escherichia coli Adapted to High Temperature

“…Some of the difference may have to do with cooccurring mutations, e.g., cardiolipin synthetase (cls) association with rho or rod-shape genes, which affect cell shape, and their association with rpoB (Tenaillon et al, 2012). Size of the cell may directly impact the cell stoichiometry, as seen in marine bacteria (Garcia et al, 2016). These affiliated mutations may be affecting the composition of cell membranes, for example, resulting in differential C:N:P.…”