Stress-induced nucleoid remodeling inDeinococcus radioduransis associated with major changes in HU abundance and dynamics

Abstract

ABSTRACTBacteria have developed a wide range of strategies to respond to stress, one of which is the rapid large-scale reorganization of their nucleoid, which is often associated with a major reprogramming of the gene expression profile. Nucleoid associated proteins (NAPs) are believed to be major actors in this process, but the molecular mechanisms underlying stress-induced nucleoid remodeling remain poorly understood. Here, using the radiation resistant bacterium,D. radiodurans, as a model, and advanced fluorescence microscopy approaches, we examined the changes in nucleoid morphology and compaction induced by either entry into stationary phase or exposure to UV-C light, and characterized the associated changes in abundance and dynamics of the major NAP inD. radiodurans, the heat-unstable (HU) protein. While both types of stress induced a similar macroscopic rearrangement of the nucleoid into a more compact structure, HU diffusion was significantly reduced in stationary phase cells, but was instead dramatically increased following exposure to UV-C, suggesting that the underlying mechanisms of remodeling are distinct. Furthermore, a detailed comparison of the cellular response to sublethal and lethal doses of UV-C light revealed that UV-induced nucleoid remodeling involves a rapid nucleoid condensation step associated with increased HU diffusion and abundance, followed by a slower decompaction phase to restore normal nucleoid morphology and HU dynamics, before cell growth and division can resume. Together, these findings shed light on the diversity and complexity of stressed-induced nucleoid remodeling processes in bacteria.