Two-step chromosome segregation in the stalked budding bacterium Hyphomonas neptunium

Alexandra Jung,Kristina Heinrich,Javier Serrania,Anne Raßbach,Muriel C F Van Teeseling,Patrick Sobetzko,Anke Becker,Martin Thanbichler,Revathi L Pulpetta

doi:10.1038/s41467-019-11242-5

Abstract

Chromosome segregation typically occurs after replication has finished in eukaryotes but during replication in bacteria. Here, we show that the alphaproteobacterium Hyphomonas neptunium, which proliferates by bud formation at the tip of a stalk-like cellular extension, segregates its chromosomes in a unique two-step process. First, the two sister origin regions are targeted to opposite poles of the mother cell, driven by the ParABS partitioning system. Subsequently, once the bulk of chromosomal DNA has been replicated and the bud exceeds a certain threshold size, the cell initiates a second segregation step during which it transfers the stalk-proximal origin region through the stalk into the nascent bud compartment. Thus, while chromosome replication and segregation usually proceed concurrently in bacteria, the two processes are largely uncoupled in H. neptunium, reminiscent of eukaryotic mitosis. These results indicate that stalked budding bacteria have evolved specific mechanisms to adjust chromosome segregation to their unusual life cycle.

Highlights

Chromosome segregation typically occurs after replication has finished in eukaryotes but during replication in bacteria
Bacteria can display a transverse chromosome arrangement, with the ori and ter regions positioned around midcell and the two chromosomal arms segregated to opposite cell halves[13,14,15,16]
Chromosomal DNA was prepared from synchronized H. neptunium cells shortly after their entry into S-phase and subjected to high-throughput sequencing

Summary

Introduction

Chromosome segregation typically occurs after replication has finished in eukaryotes but during replication in bacteria. While chromosome replication and segregation usually proceed concurrently in bacteria, the two processes are largely uncoupled in H. neptunium, reminiscent of eukaryotic mitosis. Eukaryotic cells cope with this issue by temporally uncoupling the replication and segregation process After they have reached the end of S-phase, their sister chromatids cohere for an extended period of time, condensing into compact structures that are pulled apart simultaneously to opposite cell halves by the mitotic spindle apparatus[1,2]. The subcellular location of these landmark sites varies among species[3,6], the majority of organisms analyzed to date show a longitudinal (ori–ter) pattern, in which the ori and ter regions are located at or close to opposite cell poles, while the two chromosomal arms are arranged side by side in-between these two fixed points[4,9,10,11,12]. After decatenation and chromosome dimer resolution[7], the ter regions are partitioned with the help of DNA translocases that help to clear the division site of nonsegregated DNA27,28

Objectives

Methods

Results

Conclusion