Entry and exit of Fragilariopsis cylindrus diatoms from the polar night: evidence for chromatin-mediated genome control

Abstract

Regulation of the epigenome landscape plays a crucial role in adaptation to environmental changes. However, the molecular mechanisms by which epigenome landscapes are established and tuned to adjust the cellular status to environmental cues remain poorly understood, especially in unicellular photosynthetic eukaryotes. Polar microalgae must adapt to extreme variations in light and temperature for survival and therefore represent excellent models to understand the diversity of gene regulatory mechanisms, yet chromatin-based mechanisms have never been explored in these organisms. In this study, we combined genome-wide profiling of histone and DNA modifications with transcriptomic analyses of the marine polar diatom Fragilariopsis cylindrus upon entry and exit of a 3-month-long polar night. We show that, in agreement with its established role in transcription facilitation, histone H2B monobiquitination (H2Bub) is modulated at active genes upon prolonged darkness to light re-exposure. In contrast, histone H3 lysine 27 trimethylation (H3K27me3) and DNA cytosine methylation (CG methylation), two modifications typically associated with the silencing of genes or transposable elements (TEs), remained stable throughout the transitions, reinforcing their role in transcriptional repression, particularly at TEs but also at a few genes. We further demonstrate that H3K27me3 and DNA methylation are physically associated at TEs, probably reflecting a dual locking system enabling F.cylindrus cells to cope with the invasive nature of these genetic elements under extreme environmental conditions. These findings enhance our understanding of genome and epigenome regulation in diatoms in response to environmental variability and open new avenues for exploring the role played by chromatin-level regulation in the unique evolutionary history of polar unicellular eukaryotes.