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Coupling chromosome organization to genome segregation in Archaea

ABSTRACT: Chromosome segregation is a fundamental process in all life forms and requires coordination with genome organization, replication and cell division. The mechanism that mediates chromosome segregation in archaea remains enigmatic, despite the centre-stage role assumed by these organisms in the discourse about the origin of eukaryotes. Previously, we identified two proteins, SegA and SegB, which form a minimalist chromosome partition machine in Sulfolobales. Here we uncover patterns and mechanisms that the SegAB system employs to link chromosome organization to genome segregation. Deletion of the genes causes growth and chromosome partition defects. ChIP-seq investigations revealed that SegB binds to multiple sites scattered across the chromosome, but mainly localised close to the segAB locus in most of the examined archaeal genera. The sites are predominantly present in intragenic regions. Recent chromosome conformation studies have shown that the chromosome of Sulfolobales members is organised into two spatially segregated compartments, designated A and B. Interestingly, SegB sites are predominantly located in the A compartment, whose shaping factors have remained elusive so far. We show that SegB coalesces into multiple foci through the nucleoid, exhibiting a biased localisation towards the cell periphery, which hints at potential tethers to the cell membrane. This clue is further strengthened by the structural similarities of SegB orthologues with predicted b-helix domains to membrane-associate proteins, including the distant bactofilin. Atomic force microscopy experiments provided mechanistic insights into how SegB binds DNA and uncovered short-range DNA compaction and long-range looping of distant sites by SegB. These activities point to a significant role for SegB in chromosome condensation that in turn enables genome segregation. Collectively, our data put forward SegAB as important players in bridging chromosome organization to genome segregation in archaea.

ORGANISM(S): Sulfolobus acidocaldarius DSM 639

PROVIDER: GSE297822 | GEO | 2025/06/22

REPOSITORIES: GEO

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Project description:The three-dimensional organization of chromosomes is tightly related to their biological function. Both imaging and chromosome conformation capture studies have revealed several layers of organization, including segregation into active and inactive compartments at the megabase scale, and partitioning into domains (TADs) and associated loops at the sub-megabase scale. Yet, it remains unclear how these layers of genome organization form, interact with one another, and contribute to or result from genome activities. TADs seem to have critical roles in regulating gene expression by promoting or preventing interactions between promoters and distant cis-acting regulatory elements, and different architectural proteins, including cohesin, have been proposed to play central roles in their formation. But so far, experimental depletions of these proteins have resulted in marginal changes in chromosome organization. Here, we show that deletion of the cohesin-loading factor, Nipbl, leads to loss of chromosome-associated cohesin and results in dramatic genome reorganization. TADs and associated loops vanish globally, even in the absence of transcriptional changes. In contrast, segregation into compartments is preserved and even reinforced. Strikingly, the disappearance of TADs unmasks a finer compartment structure that accurately reflects the underlying epigenetic landscape. These observations demonstrate that the 3D organization of the genome results from the independent action of two distinct mechanisms: 1) cohesin-independent segregation of the genome into fine-scale compartment regions, defined by the underlying chromatin state; and 2) cohesin-dependent formation of TADs possibly by the recently proposed loop extrusion mechanism, enabling long-range and target-specific activity of promiscuous enhancers. The interplay between these mechanisms creates an architecture that is more complex than a simple structural hierarchy and can be central to guiding normal development.

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Coupling chromosome organization to genome segregation in Archaea

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