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Sequence-dependent activity and compartmentalization of foreign DNA in a eukaryotic nucleus [Mnase-Seq]

ABSTRACT: In eukaryotes, DNA-associated protein complexes co-evolve with genomic sequence to orchestrate chromatin folding into functional chromosomes. Here, we investigate the relationship between DNA sequence and the spontaneous loading and activity of chromatin components in the absence of co-evolutions. Using bacterial genomes integrated into S. cerevisiae, which diverged from yeast up to 1.5 billion years ago, we show that nucleosomes, cohesins and the transcriptional machinery can lead to the formation of two different chromatin archetypes, one being transcribed and the other silent. These two archetypes also form on eukaryotic exogenous sequences, and depend on sequence composition. They do not mix in the nucleus, leading to a bipartite nuclear compartmentalisation reminiscent of the organization of vertebrate nuclei. Our findings represent a significant advance in understanding the primary molecular mechanisms that govern the co-option or silencing of DNA sequences integrated into foreign genomes during natural horizontal gene transfers, or in synthetic genomics projects.

ORGANISM(S): Saccharomyces cerevisiae

PROVIDER: GSE217018 | GEO | 2025/02/14

REPOSITORIES: GEO

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Project description:Chromatin-organizing factors, like CTCF and cohesins, have been implicated in the control of complex viral regulatory programs. We investigated the role of CTCF and cohesin in the control of the latent to lytic switch for Kaposi's Sarcoma-Associated Herpesvirus (KSHV). We found that cohesin subunits, but not CTCF, were required for the repression of KSHV immediate early gene transcription. Depletion of cohesin subunits Rad21, SMC1, or SMC3 resulted in lytic cycle gene transcription and viral DNA replication. In contrast, depletion of CTCF failed to induce lytic transcription or DNA replication. ChiP-Seq analysis revealed that cohesins and CTCF bound to several sites within the immediate early control regions for ORF50 and more distal 5' sites that also regulate the divergently transcribed ORF45-46-47 gene cluster. Rad21 depletion led to a robust increase in ORF45 and ORF47 transcripts, with similar kinetics to that observed with chemical induction by sodium butyrate. During latency, the chromatin between the ORF45 and ORF50 transcription start sites was enriched in histone H3K4me3 with elevated H3K9ac at the ORF45 promoter and elevated H3K27me3 at the ORF50 promoter. A paused form of RNA pol II was loosely associated with the ORF45 promoter region during latency, but was converted to an active elongating form upon reactivation induced by Rad21 depletion. Butyrate-induced transcription of ORF45 and ORF47 was resistant to cyclohexamide, suggesting that these genes have immediate early features similar to ORF50. Butyrate-treatment caused the rapid dissociation of cohesins and loss of CTCF binding at the immediate early gene locus, suggesting that cohesins may be a direct target of butyrate-mediated lytic induction. Our findings implicate cohesins as a major repressor of KSHV lytic gene activation, and function coordinately with CTCF to regulate the switch between latent and lytic gene activity. Study of chromatin-organizing factors, like CTCF and cohesins.

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Sequence-dependent activity and compartmentalization of foreign DNA in a eukaryotic nucleus [Mnase-Seq]

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