Dataset Information

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 nutrient-limited 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.

SUBMITTER: Garcia NS

PROVIDER: S-EPMC5113841 | biostudies-other | 2016 Nov

REPOSITORIES: biostudies-other

ACCESS DATA

Publications

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

Garcia Nathan S NS Bonachela Juan A JA Martiny Adam C AC

The ISME journal 20160408 11

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 nutrient-limited 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 var ...[more]

PMID: 27058506

Similar Datasets

Project description:Nutrient acquisition is a critical determinant for the competitive advantage for auto- and osmohetero- trophs alike. Nutrient limited growth is commonly described on a whole cell basis through reference to a maximum growth rate (Gmax) and a half-saturation constant (KG). This empirical application of a Michaelis-Menten like description ignores the multiple underlying feedbacks between physiology contributing to growth, cell size, elemental stoichiometry and cell motion. Here we explore these relationships with reference to the kinetics of the nutrient transporter protein, the transporter rate density at the cell surface (TRD; potential transport rate per unit plasma-membrane area), and diffusion gradients. While the half saturation value for the limiting nutrient increases rapidly with cell size, significant mitigation is afforded by cell motion (swimming or sedimentation), and by decreasing the cellular carbon density. There is thus potential for high vacuolation and high sedimentation rates in diatoms to significantly decrease KG and increase species competitive advantage. Our results also suggest that Gmax for larger non-diatom protists may be constrained by rates of nutrient transport. For a given carbon density, cell size and TRD, the value of Gmax/KG remains constant. This implies that species or strains with a lower Gmax might coincidentally have a competitive advantage under nutrient limited conditions as they also express lower values of KG. The ability of cells to modulate the TRD according to their nutritional status, and hence change the instantaneous maximum transport rate, has a very marked effect upon transport and growth kinetics. Analyses and dynamic models that do not consider such modulation will inevitably fail to properly reflect competitive advantage in nutrient acquisition. This has important implications for the accurate representation and predictive capabilities of model applications, in particular in a changing environment.

Project description:Temperature and nutrients are key factors affecting the growth, cell size, and physiology of marine phytoplankton. In the ocean, temperature and nutrient availability often co-vary because temperature drives vertical stratification, which further controls nutrient upwelling. This makes it difficult to disentangle the effects of temperature and nutrients on phytoplankton purely from observational studies. In this study, we carried out a factorial experiment crossing two temperatures (13°and 19°C) with two growth regimes (P-limited, semi-continuous batch cultures ["-P"] and nutrient replete batch cultures in turbidostat mode ["+P"]) for three species of common marine haptophytes (Emiliania huxleyi, Chrysochromulina rotalis and Prymnesium polylepis) to address the effects of temperature and nutrient limitation on elemental content and stoichiometry (C:N:P), total RNA, cell size, and growth rate. We found that the main gradient in elemental content and RNA largely was related to nutrient regime and the resulting differences in growth rate and degree of P-limitation, and observed reduced cell volume-specific content of P and RNA (but also N and C in most cases) and higher N:P and C:P in the slow growing -P cultures compared to the fast growing +P cultures. P-limited cells also tended to be larger than nutrient replete cells. Contrary to other recent studies, we found lower N:P and C:P ratios at high temperature. Overall, elemental content and RNA increased with temperature, especially in the nutrient replete cultures. Notably, however, temperature had a weaker-and in some cases a negative-effect on elemental content and RNA under P-limitation. This interaction indicates that the effect of temperature on cellular composition may differ between nutrient replete and nutrient limited conditions, where cellular uptake and storage of excess nutrients may overshadow changes in resource allocation among the non-storage fractions of biomass (e.g. P-rich ribosomes and N-rich proteins). Cell size decreased at high temperature, which is in accordance with general observations.

Project description:Marine phytoplankton and heterotrophic bacteria share a very close but usually changeable relationship. However, the ultimate fate of their unstable relationship on a long-term scale is unclear. Here, the relationship between Synechococcus and heterotrophic bacterial communities underwent a dramatic shift from antagonism to commensalism and eventually to mutualism during long-term cocultivation. The relationship change is attributed to the different (even opposite) effects of diverse bacterial members on Synechococcus and the ratio of beneficial to harmful bacteria. Different bacterial members also interact with each other (e.g., quorum-sensing communication, hostility, or mutual promotion) and drive a dynamic succession in the entire community structure that corresponds exactly to the shift in its relationship with Synechococcus. In the final mutualism stage, a self-sufficient nitrogen cycle, including nitrogen fixation, denitrification, and organic nitrogen degradation, contributed to the healthy survival of Synechococcus for 2 years without an exogenous nutrient supply. This natural selective trait of Synechococcus and heterotrophic bacteria toward mutualism under long-term coexistence provides a novel clue for understanding the ubiquity and competitive advantage of Synechococcus in global oceans. IMPORTANCE Phytoplankton and heterotrophic bacteria have a close but usually changeable relationship. Uncovering the dynamic changes and driving factors of their interrelationships is of great significance for an in-depth understanding of the ecological processes and functions of marine microorganisms. Here, we observed that Synechococcus and heterotrophic bacterial communities underwent a dramatic change in their relationship from antagonism to mutualism during a long-term cocultivation process. We revealed that the interactions between different members of the bacterial community and the combined effects of different bacterial individuals on Synechococcus promoted the dynamic changes of the Synechococcus-bacterium relationship. In the end, a self-sufficient nutrient cycle (especially nitrogen) established by Synechococcus and bacterial communities supported their long-term survival without any external nutrition supply. This study provides novel insight into the interaction between Synechococcus and heterotrophic bacteria in the ocean and provides a novel clue for understanding the ubiquity and competitive advantage of Synechococcus in global oceans.

Dataset Information

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

Publications

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

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure