Whole transcriptome analysis of the silicon response of the diatom Thalassiosira pseudonana.

Roshan Prakash Shrestha,Trina Norden-Krichmar,Benoit Tesson,Stephen Federowicz,Andrew E Allen,Mark Hildebrand

doi:10.1186/1471-2164-13-499

Abstract

BackgroundSilicon plays important biological roles, but the mechanisms of cellular responses to silicon are poorly understood. We report the first analysis of cell cycle arrest and recovery from silicon starvation in the diatom Thalassiosira pseudonana using whole genome microarrays.ResultsThree known responses to silicon were examined, 1) silicified cell wall synthesis, 2) recovery from silicon starvation, and 3) co-regulation with silicon transporter (SIT) genes. In terms of diatom cell wall formation, thus far only cell surface proteins and proteins tightly associated with silica have been characterized. Our analysis has identified new genes potentially involved in silica formation, and other genes potentially involved in signaling, trafficking, protein degradation, glycosylation and transport, which provides a larger-scale picture of the processes involved. During silicon starvation, an overrepresentation of transcription and translation related genes were up-regulated, indicating that T. pseudonana is poised to rapidly recover from silicon starvation and resume cell cycle progression upon silicon replenishment. This is in contrast to other types of limitation, and provides the first molecular data explaining the well-established environmental response of diatoms to grow as blooms and to out-compete other classes of microalgae for growth. Comparison of our data with a previous diatom cell cycle analysis indicates that assignment of the cell cycle specific stage of particular cyclins and cyclin dependent kinases should be re-evaluated. Finally, genes co-varying in expression with the SITs enabled identification of a new class of diatom-specific proteins containing a unique domain, and a putative silicon efflux protein.ConclusionsAnalysis of the T. pseudonana microarray data has provided a wealth of new genes to investigate previously uncharacterized cellular phenomenon related to silicon metabolism, silicon’s interaction with cellular components, and environmental responses to silicon.

Highlights

Silicon plays important biological roles, but the mechanisms of cellular responses to silicon are poorly understood
The three datasets analyzed in this study have provided new insights into diverse aspects of silicon-related processes in diatoms, and further characterization of these genes could increase our understanding of biological interactions with silicon
Far only cell surface proteins and proteins tightly associated with silica involved in diatom cell wall formation have been characterized, and our current understanding of the molecular details of frustule formation is mostly static

Summary

Introduction

Silicon plays important biological roles, but the mechanisms of cellular responses to silicon are poorly understood. Based on our current understanding, it is clear that the three major cellular processes affected by or involving silicon are the cell cycle, silicon transport, and cell wall synthesis. Mechanisms triggering cell cycle arrest or progression upon silicon starvation or addition remain unknown, but probably involve signaling processes that result in control over cell cycle-related genes. Most diatoms exhibit a dependence on silicon for cell cycle progression, and limitation for silicon will arrest the cell cycle at particular stages, which can vary depending on the species [8]. Oftentimes, the majority of cells in a culture arrest at the same stage, and upon silicon replenishment, they progress synchronously through the cell cycle, which enables characterization of cell cycle-related processes [5]. Synchronization allows for enrichment of genes and proteins induced during these processes, enabling their identification and characterization [9]

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