Use of Agent-Based Modeling To Explore the Mechanisms of Intracellular Phosphorus Heterogeneity in Cultured Phytoplankton

Neil D Fredrick,Daliangelis Nuï¿½Ez-Milland,John A Berges,Benjamin S Twining,Ferdi L Hellweger

doi:10.1128/aem.00487-13

Abstract

There can be significant intraspecific individual-level heterogeneity in the intracellular P of phytoplankton, which can affect the population-level growth rate. Several mechanisms can create this heterogeneity, including phenotypic variability in various physiological functions (e.g., nutrient uptake rate). Here, we use modeling to explore the contribution of various mechanisms to the heterogeneity in phytoplankton grown in a laboratory culture. An agent-based model simulates individual cells and their intracellular P. Heterogeneity is introduced by randomizing parameters (e.g., maximum uptake rate) of daughter cells at division. The model was calibrated to observations of the P quota of individual cells of the centric diatom Thalassiosira pseudonana, which were obtained using synchrotron X-ray fluorescence (SXRF). A number of simulations, with individual mechanisms of heterogeneity turned off, then were performed. Comparison of the coefficient of variation (CV) of these and the baseline simulation (i.e., all mechanisms turned on) provides an estimate of the relative contribution of these mechanisms. The results show that the mechanism with the largest contribution to variability is the parameter characterizing the maximum intracellular P, which, when removed, results in a CV of 0.21 compared to a CV of 0.37 with all mechanisms turned on. This suggests that nutrient/element storage capabilities/mechanisms are important determinants of intrapopulation heterogeneity.

Highlights

There can be significant intraspecific individual-level heterogeneity in the intracellular P of phytoplankton, which can affect the population-level growth rate
While P quota is generally easier to measure on a cellspecific basis, it is the internal P content that is important for many physiological processes
We develop a model which includes a number of mechanisms of heterogeneity and apply it to the data of Nuñez-Milland et al [21], who grew the marine diatom Thalassiosira pseudonana in batch culture and measured P quota using synchrotron X-ray fluorescence (SXRF)

Summary

Introduction

There can be significant intraspecific individual-level heterogeneity in the intracellular P of phytoplankton, which can affect the population-level growth rate. Several mechanisms can create this heterogeneity, including phenotypic variability in various physiological functions (e.g., nutrient uptake rate). Recent observations of intracellular P in individual cells have shown significant intraspecific heterogeneity in laboratory and field populations, with coefficients of variations (CV) ranging from 0.08 to 2.11 for P quota and 0.10 to 2.10 for internal P content (Table 1). Phenotypic variability, when cell division creates two daughter cells that are not exactly the same in properties (e.g., size) [14] or physiology (e.g., nutrient uptake) [15], leads to heterogeneity in intracellular P directly (i.e., uneven division of P) or indirectly (e.g., as a result of different uptake rates). Prochlorococcus Synechococcus Thalassiosira pseudonana Microcystis aeruginosa Dinophysis norvegica Microcystis aeruginosa Ceratium hirendenella Asterionella formosa Anabaena spiroides Spirulina platensis Cyclotella meneghiniana Cyclotella meneghiniana

Methods

Results

Conclusion