Coupling chromosome organization to genome segregation in Archaea

Abstract

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. Previously, we identified two proteins, SegA and SegB, which form a minimalist chromosome partition machine in Sulfolobales. Here we uncover patterns and mechanisms that SegAB employ to link chromosome organization to genome segregation. Deletion of the genes causes growth and chromosome partition defects. ChIP-seq investigations reveal 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 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. Atomic force microscopy experiments disclose short-range DNA compaction and long-range looping of distant sites by SegB, pointing 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.