Superposition of Individual Activities: Urea-Mediated Suppression of Nitrate Uptake in the Dinoflagellate Prorocentrum minimum Revealed at the Population and Single-Cell Levels.

Olga Matantseva,Maren Voss,Hendrik Schubert,Iris Liskow,Angela Vogts,Sergei Skarlato,Ilya Pozdnyakov

doi:10.3389/fmicb.2016.01310

Abstract

Dinoflagellates readily use diverse inorganic and organic compounds as nitrogen sources, which is advantageous in eutrophied coastal areas exposed to high loads of anthropogenic nutrients, e.g., urea, one of the most abundant organic nitrogen substrates in seawater. Cell-to-cell variability in nutritional physiology can further enhance the diversity of metabolic strategies among dinoflagellates of the same species, but it has not been studied in free-living microalgae. We applied stable isotope tracers, isotope ratio mass spectrometry and nanoscale secondary ion mass spectrometry (NanoSIMS) to investigate the response of cultured nitrate-acclimated dinoflagellates Prorocentrum minimum to a sudden input of urea and the effect of urea on the concurrent nitrate uptake at the population and single-cell levels. We demonstrate that inputs of urea lead to suppression of nitrate uptake by P. minimum, and urea uptake exceeds the concurrent uptake of nitrate. Individual dinoflagellate cells within a population display significant heterogeneity in the rates of nutrient uptake and extent of the urea-mediated inhibition of the nitrate uptake, thus forming several groups characterized by different modes of nutrition. We conclude that urea originating from sporadic sources is rapidly utilized by dinoflagellates and can be used in biosynthesis or stored intracellularly depending on the nutrient status; therefore, sudden urea inputs can represent one of the factors triggering or supporting harmful algal blooms. Significant physiological heterogeneity revealed at the single-cell level is likely to play a role in alleviation of intra-population competition for resources and can affect the dynamics of phytoplankton populations and their maintenance in natural environments.

Highlights

Unicellular photosynthetic eukaryotes play a crucial role in oceanic primary production, sequestration of inorganic carbon and biogeochemical cycling of macro- and micronutrients (Falkowski et al, 1998; Morel and Price, 2003; Chassot et al, 2010; Matantseva and Skarlato, 2013)
We studied how photosynthetic nitrateacclimated dinoflagellates Prorocentrum minimum responded to a sudden urea input at the population level and how this net response was realized at the level of single cells
The uptake of urea by bacteria present in the culture was less than 1% of the urea uptake by dinoflagellates and could be neglected

Summary

Introduction

Unicellular photosynthetic eukaryotes play a crucial role in oceanic primary production, sequestration of inorganic carbon and biogeochemical cycling of macro- and micronutrients (Falkowski et al, 1998; Morel and Price, 2003; Chassot et al, 2010; Matantseva and Skarlato, 2013). Interactions between microalgae and environment have been studied primarily at the population level. Only a limited number of works report usage of NanoSIMS in phytoplankton ecology and biogeochemistry research. Such works explore the symbiotic relationships, where microalgae act as symbionts or host organisms (Foster et al, 2011; Pernice et al, 2012, 2015; Kopp et al, 2013; Zehr, 2015), whereas nutritional heterogeneity within populations of microalgae remains largely ignored. Numerous studies on bacteria and mammalian cellular lineages showed that variability among cells of the same population is ubiquitous and in many cases highly significant for the interpretation of bulk observations (Altschuler and Wu, 2010), which can be true for populations of environmentally important protists

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