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

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 110; no. 18; pp. 7518 - 7523
• Main Authors: Ashworth, Justin, Coesel, Sacha, Lee, Allison, Armbrust, E. Virginia, Orellana, Mónica V., Baliga, Nitin S.
• Format: Journal Article
• Language: English
• Published: Washington, DC National Academy of Sciences 30-04-2013; National Acad Sciences
• Subjects: Algae; Biological and medical sciences; Biological Sciences; Cell division; Cell Membrane - metabolism; Cell Membrane - radiation effects; Chromatin; Chromatin - metabolism; Circadian Rhythm - genetics; Circadian Rhythm - radiation effects; Classical genetics, quantitative genetics, hybrids; Diatoms; Diatoms - cytology; Diatoms - genetics; Diatoms - growth & development; Diatoms - radiation effects; Environmental conditions; Fundamental and applied biological sciences. Psychology; Gene expression; Gene Expression Profiling; Gene Expression Regulation - radiation effects; Gene Regulatory Networks - genetics; Genes; Genetics of eukaryotes. Biological and molecular evolution; Genome - genetics; Genomes; Light; Nutrients; Photoreceptors; Photosynthesis; Physical Sciences; Plankton; Plant cytology, morphology, systematics, chorology and evolution; Proteins; Signal Transduction - genetics; Signal Transduction - radiation effects; Steepest descent method; Thallophyta; Transcription factors; Transcription Factors - metabolism; Transcription, Genetic - radiation effects; Transcriptome - genetics; Thalassiosira pseudonana; Growth; Algae; Daily variation; Oceanography; Circadian rhythm; Gene expression; Heterokontophyta; Bacillariophyta; Plankton; Phytoplankton; diurnal cycle; Genome; Photosynthesis
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.1300962110

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.