Abstract

Polycomb (PcG) and Trithorax (TrxG) complexes are two evolutionarily conserved epigenetic regulatory components that act antagonistically to regulate the expression of genes involved in a plethora of biological processes. Both complexes were studied mainly in multicellular organisms with highlighted roles in development and their discovery in recent years in single-cell species raises important questions in respect to the extent of their existence, their role and significance in unicellular species. Using a highly sensitive method for the detection and annotation of protein domain architecture called eDAF, our work reports an unprecedented diversity of Polycomb and Trithorax groups of proteins from lab cultures and the environment at broad scale in Tara Oceans genomics datasets and shows significant correlations with environmental factors measured during the expedition. Both complexes are histone writers responsible for the deposition of important key histone marks including H3K27me3 and H3K4me3 deposited by Polycomb and Trithorax complexes respectively. To better understand the role of these proteins, we used the model diatom Phaeodactylum tricornutum to profile genome wide a trithorax deposited mark, H3K4me3 and showed its conserved role as an activating mark. We compared its profile with previously published marks among which the antagonizing Polycomb associated mark H3K27me3 which we found to co-occur in an exclusive manner with a balanced expression suggesting a bivalency. Our work puts under the spot light these complexes which were thought to be present only in multicellular organisms and highlights the ancestral function of these complexes in a broader evolutionary context than is currently appreciated.

Highlights

  • Polycomb (PcG) and trithorax (TrxG) protein complexes were initially isolated in Drosophila as factors responsible for the maintenance of expression of HOX genes, important determinants of body patterning (Schuettengruber et al, 2007)

  • To further investigate the diversity of Polycomb and Trithorax complexes in single-cell species, we first made an extensive scan of the Marine Microbial Eukaryote Transcriptome Sequencing Project database (MMETSP) database using eDAF and reference sequences (Supplementary Table S1)

  • Using the VEFS-Box of the polycomb domain to construct the phylogenetic tree of Su(z)12, we found that Chlorophytes and diatom Su(z)12 sequence formed a well-supported cluster like E(z), but with a few exceptions such as some pennate diatoms, Pseudo-nitzschia delicatissima, P. arenysensis and Fragilariopsis kerguelensis which were found to cluster with Rhizaria and Fungi (Figure 2C)

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Summary

Introduction

Polycomb (PcG) and trithorax (TrxG) protein complexes were initially isolated in Drosophila as factors responsible for the maintenance of expression of HOX genes, important determinants of body patterning (Schuettengruber et al, 2007). PcG and TrxG complexes have been shown to act antagonistically to modify chromatin via histone-modifying or chromatinremodeling activities that repress or activate their target genes, respectively (Geisler and Paro, 2015). Both complexes are highly conserved among eukaryotes and their recent discovery in single celled species raises important questions about their function and role in unicellular organisms and in the evolution of multicellularity. The PRC2 complex comprises four core components: a histone methyltransferase, enhancer of zeste E(z), a WD40 domain protein, extra sex combs (ESC), a zinc finger protein, suppressor of zeste 12 (Su(z)12), and another WD40 domain protein, Nurf-55 (Margueron and Reinberg, 2011)

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