Phosphorus availability regulates intracellular nucleotides in marine eukaryotic phytoplankton

Abstract

Marine eukaryotic phytoplankton adapt to low phosphorus (P) in the oceans through a variety of step-wise mechanisms including lipid substitution and decreased nucleic acid content. Here, we examined the impact of low P concentrations on intracellular metabolites whose abundances can be quickly adjusted by cellular regulation within laboratory cultures of three model phytoplankton and in field samples from the Atlantic and Pacific Oceans. We quantified the relative abundances of monophosphate nucleotides and their corresponding nucleosides, using a combination of targeted and untargeted metabolomics methods. Under P-deficient conditions, we observed a marked decrease in adenosine 5 0 -monophosphate (AMP) with a concomitant increase in adenosine. This shift occurred within all detected pairs of monophosphate nucleotides and nucleosides, and was consistent with previous work showing transcriptional changes in nucleotide synthesis and salvage under P-deficient conditions for model eukaryotes. In the field, we observed AMP-to-adenosine ratios that were similar to those in laboratory culture under P-deficient conditions. This is an open access article under the terms of the Creative Commons Attribution-NonCommercial License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes. Scientific Significance StatementPhosphorus (P) is a central element in cellular metabolism that can limit primary production of eukaryotic phytoplankton in the ocean. Adaptation to low P is known to drive metabolic restructuring in eukaryotic phytoplankton, but the specific adaptive responses of cellular metabolites are poorly understood. Here we show that three model phytoplankton alter their metabolites under P deficiency, relative to P-replete conditions. We present evidence for a new model of P allocation within cells, where monophosphate nucleotides can act as a flexible P storage pool, allowing rapid and dynamic distribution of P to cellular processes.

Transcriptional Shifts Highlight the Role of Nutrients in Harmful Brown Tide Dynamics

“…Compared to S1 and S2, there were increases in the relative expression of lipid processing, and purine metabolism in S3. It has recently been shown that A. anophagefferens , and other eukaryotic phytoplankton, modulate intracellular metabolites related to purine metabolism when P-deficient (Kujawinski et al, 2017). Eukaryotic phytoplankton are also well known to remodel their membrane lipids in response to P deficiency (Van Mooy et al, 2009).…”

High-Resolution Liquid Chromatography Tandem Mass Spectrometry Enables Large Scale Molecular Characterization of Dissolved Organic Matter

“…These molecules have been identified in culture experiments and/or detected in field samples to highlight some of the important microbial interactions in the surface ocean (Amin et al, 2015;Johnson et al, 2016;Repeta et al, 2016;Heal et al, 2017;Kujawinski et al, 2017). Targeted metabolomic studies focus on individual, well-characterized substrates whose concentrations and cycling can be followed precisely in incubations and in field settings.…”

“…This approach paired with high acquisitions speed (>1 Hz) of state of the art instruments results in thousands of spectra per LC-MS/MS run. For a reliable data analysis and reproducible interpretation of the results, bioinformatic workflows including comprehensive databases and statistical significance estimation are crucial (da Silva et al, 2015;Böcker, 2017;Scheubert et al, 2017;Weber et al, 2017) and have been very recently employed for marine metabolomic studies Hartmann et al, 2017;Kujawinski et al, 2017;Longnecker and Kujawinski, 2017). With these new bioinformatic tools and instrumental improvements in sensitivity, acquisition speed and resolution we anticipate that the techniques used for DOM characterization will further shift toward non-targeted analyses using high-resolution LC-MS/MS that provide inventories of molecular structures in complex environmental datasets.…”

Advanced Molecular Techniques Provide New Rigorous Tools for Characterizing Organic Matter Quality in Complex Systems

“…LC MS/MS analysis of organic matter composition using orbital ion‐trap and quadrupole time of flight MS has been employed to identify potential structure and chemical formula of organic compounds through comparison to library mass spectra, mainly in marine systems (Kujawinski et al, ; Longnecker & Kujawinski, ). These instrumentations have lower resolving power compared to the FTICRMS and are characterized by significantly higher scan speeds due to the coupling with liquid chromatography.…”