Abstract
BackgroundMarine diatoms constitute a major component of eukaryotic phytoplankton and stand at the crossroads of several evolutionary lineages. These microalgae possess peculiar genomic features and novel combinations of genes acquired from bacterial, animal and plant ancestors. Furthermore, they display both DNA methylation and gene silencing activities. Yet, the biogenesis and regulatory function of small RNAs (sRNAs) remain ill defined in diatoms.ResultsHere we report the first comprehensive characterization of the sRNA landscape and its correlation with genomic and epigenomic information in Phaeodactylum tricornutum. The majority of sRNAs is 25 to 30 nt-long and maps to repetitive and silenced Transposable Elements marked by DNA methylation. A subset of this population also targets DNA methylated protein-coding genes, suggesting that gene body methylation might be sRNA-driven in diatoms. Remarkably, 25-30 nt sRNAs display a well-defined and unprecedented 180 nt-long periodic distribution at several highly methylated regions that awaits characterization. While canonical miRNAs are not detectable, other 21-25 nt sRNAs of unknown origin are highly expressed. Besides, non-coding RNAs with well-described function, namely tRNAs and U2 snRNA, constitute a major source of 21-25 nt sRNAs and likely play important roles under stressful environmental conditions.ConclusionsP. tricornutum has evolved diversified sRNA pathways, likely implicated in the regulation of largely still uncharacterized genetic and epigenetic processes. These results uncover an unexpected complexity of diatom sRNA population and previously unappreciated features, providing new insights into the diversification of sRNA-based processes in eukaryotes.Electronic supplementary materialThe online version of this article (doi:10.1186/1471-2164-15-698) contains supplementary material, which is available to authorized users.
Highlights
Marine diatoms constitute a major component of eukaryotic phytoplankton and stand at the crossroads of several evolutionary lineages
Genome-wide distribution and length distribution of small RNA populations To characterize the population of P. tricornutum small RNAs, we generated five small RNA libraries within the 18 to 36 nt RNA fraction extracted from cells grown under different conditions: Normal Light (NL), High Light (HL), Low Light (LL), Dark (D), and Iron starvation (−Fe)
While miRNAs seem not to play a major regulatory role in P. tricornutum, other ncRNA types with well-described function, such as transfer RNAs (tRNAs) and U2 small nuclear RNAs (snRNAs), represent a major source of small RNAs (sRNAs) and could play important functional roles in P. tricornutum’s responses to environmental stresses such as iron starvation. This discovery implies that complex and interconnected networks of ncRNA pathways exist in diatom cells, and their fine-tuning is likely to be fundamental for the biology of these organisms and their extraordinary ability to proliferate worldwide
Summary
Marine diatoms constitute a major component of eukaryotic phytoplankton and stand at the crossroads of several evolutionary lineages These microalgae possess peculiar genomic features and novel combinations of genes acquired from bacterial, animal and plant ancestors. Small RNAs, and siRNAs, can guide AGORISC onto sequence complementary DNA targets to direct cytosine DNA methylation and/or chromatin modifications resulting in their transcriptional gene silencing [11] Besides these small RNA species, a variety of new small RNA classes, involved in novel biological functions such as DNA elimination and DNA repair [12,13,14,15], continues to be discovered in different organisms. This pathway has been mostly characterized in the male germ line, where piRNAs presumably direct transcriptional silencing of TEs through DNA methylation [17,18], a mechanism that is analogous to RNA-directed DNA methylation (RdDM) initially described in plants [19]
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