The Transcriptome and Proteome of the Diatom Thalassiosira pseudonana Reveal a Diverse Phosphorus Stress Response

Abstract

Phosphorus (P) is a critical driver of phytoplankton growth and ecosystem function in the ocean. Diatoms are an abundant class of marine phytoplankton that are responsible for significant amounts of primary production. With the control they exert on the oceanic carbon cycle, there have been a number of studies focused on how diatoms respond to limiting macro and micronutrients such as iron and nitrogen. However, diatom physiological responses to P deficiency are poorly understood. Here, we couple deep sequencing of transcript tags and quantitative proteomics to analyze the diatom Thalassiosira pseudonana grown under P-replete and P-deficient conditions. A total of 318 transcripts were differentially regulated with a false discovery rate of <0.05, and a total of 136 proteins were differentially abundant ( p <0.05). Significant changes in the abundance of transcripts and proteins were observed and coordinated for multiple biochemical pathways, including glycolysis and translation. Patterns in transcript and protein abundance were also linked to physiological changes in cellular P distributions, and enzyme activities. These data demonstrate that diatom P deficiency results in changes in cellular P allocation through polyphosphate production, increased P transport, a switch to utilization of dissolved organic P through increased production of metalloenzymes, and a remodeling of the cell surface through production of sulfolipids. Together, these findings reveal that T. pseudonana has evolved a sophisticated response to P deficiency involving multiple biochemical strategies that are likely critical to its ability to respond to variations in environmental P availability.

Accumulation and enhanced cycling of polyphosphate by Sargasso Sea plankton in response to low phosphorus

“…Thus, both field and culture observations from Synechococcus appear to discount a polyP overplus response. The modest net polyP breakdown upon P-stress might mask substantial intracellular recycling: cells have multiple polyP pools with distinct physiological functions and dynamics (33,34), and enzymes to synthesize and degrade polyP are both up-regulated in P-stressed cultures (31). Moreover, P-stressed Trichodesmium cultures have polyP:TPP ratios indistinguishable from those of natural Sargasso Sea Trichodesmium populations (30), which is consistent with our Synechococcus observations.…”

Functional group-specific traits drive phytoplankton dynamics in the oligotrophic ocean

“…Such genes or their protein products are frequently used as proxies to identify limitation in the field (39). In E1 and E2, there was a decrease in diatom-associated glycerophosphoryl phosphodiesterase (22) and adenosylhomocysteinase (40), indicative of phosphorus and vitamin limitation, respectively (Fig. 3).…”

“…Molecular-level tools that can track transcripts, proteins, or even metabolites and biochemicals in a taxon-specific way are increasingly being used in cultures and field populations to track metabolic capacity and physiological responses (16)(17)(18)(19)(20)(21)(22)(23). Molecular assessment of physiology for eukaryotic populations is most tractable in coastal systems with high biomass (17,18); thus, in oligotrophic ocean regions, molecular studies of physiology have typically been limited to the numerically abundant members of the microbial community: picoplankton (cyanobacteria, heterotrophic bacteria, and small picoeukaryotes).…”

Dissolved organic matter (DOM) release by phytoplankton in the contemporary and future ocean

“…For example, does P limitation limit the ability of phytoplankton to repair their cell membranes, resulting in significant leakage? Dyhrman et al (2012) showed that Thalassiosira pseudonana changes the composition of its lipids in response to P limitation, though they did not investigate whether these changes affected DOM release by the diatom.…”

“…A new understanding of the diatom genome has led to research on gene expression in stressed diatoms using transcriptomic and proteomic approaches. For example, recent work with T. pseudonana has shown that it has a sophisticated suite of biochemical strategies to deal with phosphorus deficiency (Dyhrman et al, 2012) and putative death-related genes play a role in acclimation to low iron conditions (Thamatrakoln et al, 2012). Similar approaches could be used to investigate gene expression associated with metabolic pathways and transport proteins associated with exudation and leakage.…”