Genome-wide diel growth state transitions in the diatom Thalassiosira pseudonana

Abstract

Marine diatoms are important primary producers that thrive in diverse and dynamic environments. They do so, in theory, by sensing changing conditions and adapting their physiology accordingly. Using the model species Thalassiosira pseudonana, we conducted a detailed physiological and transcriptomic survey to measure the recurrent transcriptional changes that characterize typical diatom growth in batch culture. Roughly 40% of the transcriptome varied significantly and recurrently, reflecting large, reproducible cell-state transitions between four principal states: (i) "dawn," following 12 h of darkness; (ii) "dusk," following 12 h of light; (iii) exponential growth and nutrient repletion; and (iv) stationary phase and nutrient depletion. Increases in expression of thousands of genes at the end of the reoccurring dark periods (dawn), including those involved in photosynthesis (e.g., ribulose-1,5-bisphosphate carboxylase oxygenase genes rbcS and rbcL), imply large-scale anticipatory circadian mechanisms at the level of gene regulation. Repeated shifts in the transcript levels of hundreds of genes encoding sensory, signaling, and regulatory functions accompanied the four cell-state transitions, providing a preliminary map of the highly coordinated gene regulatory program under varying conditions. Several putative light sensing and signaling proteins were associated with recurrent diel transitions, suggesting that these genes may be involved in light-sensitive and circadian regulation of cell state. These results begin to explain, in comprehensive detail, how the diatom gene regulatory program operates under varying environmental conditions. Detailed knowledge of this dynamic molecular process will be invaluable for new hypothesis generation and the interpretation of genetic, environmental, and metatranscriptomic data from field studies.

Diatom Phytochromes Reveal the Existence of Far-Red-Light-Based Sensing in the Ocean

“…To explore DPH function, we first monitored DPH expression by RT-qPCR in P. tricornutum cells grown under 12-h-ligh/12-h-dark cycles or maintained in prolonged darkness for 48 h. This revealed that Pt-DPH transcripts exhibited a pronounced diurnal rhythmic expression pattern, with an accumulation at the end of the light period, as observed for Tp-DPH (Ashworth et al, 2013) (Figure 2A). In contrast, in prolonged darkness, Pt-DPH mRNA levels remained at a constant low level (Figure 2A).…”

Transcriptional responses of three model diatoms to nitrate limitation of growth

“…These findings suggest that hypomethylation may play an important role in regulating the expression of sets of genes (e.g., transporters) under a given set of environmental conditions (Veluchamy et al, 2013). Additionally, Ashworth et al (2013) identified transcription factors that putatively control different regulatory networks in T. pseudonana, resulting in co-expression of thousands of genes in response to different environmental conditions including the day/night cycle and the transition from nutrient-replete growth to nitrate limitation. Koester et al (2012) found evidence that transcription factors within T. pseudonana are under positive selection, implying that mutations within the genes encoding transcription factors convey adaptive phenotypes.…”

“…Despite these general commonalities, relatively few othologs shared by the two diatoms display similar transcriptional patterns under nitrogen limitation (Maheswari et al, 2010). Some of the genes with shared transcriptional patterns are involved in nitrogen assimilation (e.g., nitrate/nitrite reductase) and the first step of the urea cycle (e.g., carbamoyl phosphate synthetase) Allen et al, 2011;Hockin et al, 2012;Ashworth et al, 2013). However, the remainder of the urea cycle genes and genes encoding urease and nitrate and ammonium transporters, are transcribed differently by the two diatoms; e.g., urease gene expression is elevated in T. pseudonana under nitrate limitation vs. nutrient-replete conditions, whereas this gene exhibits constitutive expression in P. tricornutum (Allen et al, 2011;Hockin et al, 2012).…”

Metatranscriptomes reveal functional variation in diatom communities from the Antarctic Peninsula

“…Subcellular localization data were inferred from annotated diatom gene sequences and the available literature (Armbrust et al, 2004;Bowler et al, 2008;Brown et al, 2009;Kinoshita et al, 2009;Allen et al, 2011). A caveat to the following discussion is that variation in diurnal timing (for BFS) could have transcriptome-wide effects on relative enrichment (Ashworth et al, 2013;Chauton et al, 2013). In contrast to ammonium and urea transporters discussed in the previous section, nitrate transporters were less abundant in the more oceanic BFS community, despite high NO 3 − levels in the water column (Figure 1b).…”