Cell morphology and nucleoid dynamics in dividing Deinococcus radiodurans

Kevin Floc’H,Dominique Bourgeois,Joanna Timmins,Françoise Lacroix,Jean-Philippe Kleman,Yung-Sing Wong,Pascale Servant

doi:10.1038/s41467-019-11725-5

Abstract

Our knowledge of bacterial nucleoids originates mostly from studies of rod- or crescent-shaped bacteria. Here we reveal that Deinococcus radiodurans, a relatively large spherical bacterium with a multipartite genome, constitutes a valuable system for the study of the nucleoid in cocci. Using advanced microscopy, we show that D. radiodurans undergoes coordinated morphological changes at both the cellular and nucleoid level as it progresses through its cell cycle. The nucleoid is highly condensed, but also surprisingly dynamic, adopting multiple configurations and presenting an unusual arrangement in which oriC loci are radially distributed around clustered ter sites maintained at the cell centre. Single-particle tracking and fluorescence recovery after photobleaching studies of the histone-like HU protein suggest that its loose binding to DNA may contribute to this remarkable plasticity. These findings demonstrate that nucleoid organization is complex and tightly coupled to cell cycle progression in this organism.

Highlights

Our knowledge of bacterial nucleoids originates mostly from studies of rod- or crescentshaped bacteria
These unusual features have been suggested to facilitate genome maintenance and repair[29,30]. Using both spinning-disk time-lapse microscopy and superresolution imaging, we have performed a detailed analysis of the morphological changes that occur at the cellular and nucleoid level, as D. radiodurans grows and divides in alternating perpendicular planes. These data reveal that D. radiodurans nucleoids are highly condensed, while remaining surprisingly dynamic, adopting multiple distinct configurations as the bacterium progresses through its cell cycle
We followed the choreography of the oriC and ter loci of chromosome 1 during the various stages of the cell cycle and show that they exhibit very different distributions within the cell with the oriC loci being radially distributed around the centrally located ter sites. These findings demonstrate that the properties of D. radiodurans make it well suited for the study of nucleoid organization in cocci and provide new, compelling evidence, indicating that bacterial nucleoids are complex and dynamic entities that are tightly coupled to cell shape, cell cycle progression and septal growth

Summary

Introduction

Our knowledge of bacterial nucleoids originates mostly from studies of rod- or crescentshaped bacteria. Using both spinning-disk time-lapse microscopy and superresolution imaging, we have performed a detailed analysis of the morphological changes that occur at the cellular and nucleoid level, as D. radiodurans grows and divides in alternating perpendicular planes These data reveal that D. radiodurans nucleoids are highly condensed, while remaining surprisingly dynamic, adopting multiple distinct configurations as the bacterium progresses through its cell cycle. We followed the choreography of the oriC and ter loci of chromosome 1 during the various stages of the cell cycle and show that they exhibit very different distributions within the cell with the oriC loci being radially distributed around the centrally located ter sites Taken together, these findings demonstrate that the properties of D. radiodurans make it well suited for the study of nucleoid organization in cocci and provide new, compelling evidence, indicating that bacterial nucleoids are complex and dynamic entities that are tightly coupled to cell shape, cell cycle progression and septal growth

Methods

Results

Conclusion