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. SegB binds to multiple sites scattered across the chromosome, but mainly localised close to the segAB locus in most archaeal genera. The sites are predominantly intragenic and enriched in one of the two compartments into which the chromosome folds. 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. The short-range DNA compaction activity of SegB and long-range looping of distant sites 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.